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Popov IV, Popov IV, Chebotareva IP, Tikhmeneva IA, Peshkova DA, Krikunova AA, Tkacheva EV, Algburi AR, Abdulhameed AM, Jargalsaikhan A, Ganbold O, Chikindas ML, Venema K, Ermakov AM. Differences in gut microbiota composition, diversity, and predicted functional activity between wild and captive zoo Carollia perspicillata in a One Health perspective. Braz J Microbiol 2025; 56:1291-1302. [PMID: 39961999 PMCID: PMC12095714 DOI: 10.1007/s42770-025-01630-z] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/21/2024] [Accepted: 01/29/2025] [Indexed: 05/22/2025] Open
Abstract
Bats play an important role in global microbial ecology, as they are the host of various microbes. Carollia perspicillata is one of the most popular bat species in zoos. The influence of the captive environment on the gut microbiota of this species is underinvestigated. In this study, we compared gut microbiota composition, diversity, and the potential functional activity of wild and captive C. perspicillata from Panama and Russia (Moscow Zoo), respectively, based on high-throughput 16S rRNA sequencing data. The abundance of 13 bacterial phyla and 35 bacterial genera significantly differed. Environment- and farm animal health-related bacteria (Mannheimia, unclassified Pasteurellaceae, Staphylococcus, and Mycoplasma) dominated wild bats, while bacteria important for public health (Bacteroides, Clostridium sensu stricto 1, and Acinetobacter) were higher in zoo bats. We also observed significantly greater alpha diversity in zoo bats, while there were no significant differences in beta diversity. These findings were accompanied by significant differences in the abundance of 32 functional pathways of gut bacteria, which are probably associated with the different diets of wild and zoo bats. This study shows that the rearing environment significantly affects the gut microbiota of C. perspicillata and highlights that the outcomes of microbiome research of captive bats need to be interpreted with care. Such differences in gut bacterial communities should be the basis for the development of new handling and veterinary care protocols, and also be the justification for further studies of the impact of microbiota of wild and zoo bats on One Health.
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Affiliation(s)
- Ilia V Popov
- Faculty "Bioengineering and Veterinary Medicine" and Center for Agrobiotechnology, Rostov-on-Don, 344000, Russian Federation
| | - Igor V Popov
- Faculty "Bioengineering and Veterinary Medicine" and Center for Agrobiotechnology, Rostov-on-Don, 344000, Russian Federation.
- Division of Immunobiology and Biomedicine, Center of Genetics and Life Sciences, Sirius University of Science and Technology, Federal Territory Sirius, 354340, Russian Federation.
| | - Iuliia P Chebotareva
- Division of Nanobiomedicine, Center of Genetics and Life Sciences, Sirius University of Science and Technology, Federal Territory Sirius, 354340, Russian Federation
| | - Iuliia A Tikhmeneva
- Faculty "Bioengineering and Veterinary Medicine" and Center for Agrobiotechnology, Rostov-on-Don, 344000, Russian Federation
| | - Daria A Peshkova
- Division of Immunobiology and Biomedicine, Center of Genetics and Life Sciences, Sirius University of Science and Technology, Federal Territory Sirius, 354340, Russian Federation
| | - Anastasia A Krikunova
- Faculty "Bioengineering and Veterinary Medicine" and Center for Agrobiotechnology, Rostov-on-Don, 344000, Russian Federation
| | - Elizaveta V Tkacheva
- Faculty "Bioengineering and Veterinary Medicine" and Center for Agrobiotechnology, Rostov-on-Don, 344000, Russian Federation
| | - Ammar R Algburi
- Department of Microbiology, Veterinary Medicine College, University of Diyala, Baqubah, 32001, Iraq
| | - Alyaa M Abdulhameed
- Department of Microbiology, Veterinary Medicine College, University of Diyala, Baqubah, 32001, Iraq
| | - Ariunbold Jargalsaikhan
- Department of Biology, School of Mathematics and Natural Science, Mongolian National University of Education, Ulaanbaatar, 210646, Mongolia
| | - Onolragchaa Ganbold
- Department of Biology, School of Mathematics and Natural Science, Mongolian National University of Education, Ulaanbaatar, 210646, Mongolia
| | - Michael L Chikindas
- Faculty "Bioengineering and Veterinary Medicine" and Center for Agrobiotechnology, Rostov-on-Don, 344000, Russian Federation
- Health Promoting Naturals Laboratory, School of Environmental and Biological Sciences, Rutgers State University, New Brunswick, NJ, 08901, USA
- Department of General Hygiene, I.M. Sechenov First Moscow State Medical University, Moscow, 119435, Russia
| | - Koen Venema
- Beneficial Microbes® Consultancy, Wageningen, 6709 TN, The Netherlands
| | - Alexey M Ermakov
- Faculty "Bioengineering and Veterinary Medicine" and Center for Agrobiotechnology, Rostov-on-Don, 344000, Russian Federation
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Wang B, Guo Y, Li X, Dong C, Sha H, Li H, Zhao Z, Li T. Phytostabilization potential and microbial response to the reclamation of native Cynodon dactylon in spoil heaps from a multiple-metal mining site in Southwest China. JOURNAL OF ENVIRONMENTAL MANAGEMENT 2025; 378:124758. [PMID: 40031421 DOI: 10.1016/j.jenvman.2025.124758] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 10/30/2024] [Revised: 02/26/2025] [Accepted: 02/27/2025] [Indexed: 03/05/2025]
Abstract
Phytocapping offers a sustainable approach for managing exposed tailings by mitigating pollutant spread and enhancing phytoremediation. This study investigates the potential of Bermudagrass (Cynodon dactylon) as a pioneering plant for rehabilitating tailings from an open-pit lead-zinc mine in Southwest China. Our findings demonstrate that Bermudagrass significantly improved soil quality and multifunctionality compared to adjacent bare tailings. Soil improvements included increases in organic matter (107%), total and available nitrogen (50% and 110%, respectively), available phosphorus (170%), and soil enzyme activities, including β-glucosidase (170%), sucrase (1729%), alkaline phosphatase (3722%), and acid phosphatase (168%). The reclamation process also promoted microbial community succession, altering community composition, improving microbial diversity, and enhancing bacterial biomass from (0.89 ± 0.54) × 1015 to (9.06 ± 3.25) × 1015 copies/g in rhizosphere soils. Greenhouse experiments further confirmed Bermudagrass's resilience to cadmium (Cd), with both mining and non-mining ecotypes thriving in tailing soils and Cd2+ hydroponic solutions (up to 44.5 μM) without evident phytotoxicity. Bermudagrass roots exhibited exceptional Cd accumulation (bioconcentration factor: 181-1006) while minimizing Cd translocation to shoots (translocation factor: <0.13). Inoculation with Funneliformis mosseae, a restored root-mutually symbiotic fungus, further mitigated Cd-induced phytotoxicity and enhanced plant growth. These findings highlight Bermudagrass as a promising pioneer species for phytostabilization in severely contaminated mining environments, with its rhizosphere microbiome playing a critical role in facilitating ecosystem restoration. Sustainable plant establishment in mine waste rock requires concurrent development of belowground fertility and healthy rhizospheric soil. Ultimately, successful revegetation depends on integrated above and belowground development to achieve long-term ecological restoration.
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Affiliation(s)
- Bowen Wang
- State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, 650091, China
| | - Yanying Guo
- Kunming Dianchi & Plateau Lake Research Institute, Kunming, 650228, China
| | - Xuejiao Li
- State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, 650091, China
| | - Chaoqin Dong
- State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, 650091, China
| | - Haixian Sha
- State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, 650091, China
| | - Haiyan Li
- Medical School of Kunming University of Science and Technology, Kunming, 650504, China
| | - Zhiwei Zhao
- State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, 650091, China.
| | - Tao Li
- State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, 650091, China.
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Han CJ, Huang JP, Chiang MR, Jean OSM, Nand N, Etebari K, Shelomi M. The hindgut microbiota of coconut rhinoceros beetles ( Oryctes rhinoceros) in relation to their geographical populations. Appl Environ Microbiol 2024; 90:e0098724. [PMID: 39311575 PMCID: PMC11497824 DOI: 10.1128/aem.00987-24] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/21/2024] [Accepted: 08/22/2024] [Indexed: 10/25/2024] Open
Abstract
The coconut rhinoceros beetle (CRB, Oryctes rhinoceros) is a palm tree pest capable of rapidly expanding its population in new territories. Previous studies identified a digestive symbiosis between CRB and its gut microbes. However, no research compared the genetic variation of CRBs with their hindgut microbiota on a global scale. This study aims to investigate the genetic divergence of CRB and the compositional variation of CRB's microbiota across different geographical locations, and explore the association between them and their predicted functional profiles and environmental data. The research reveals a distinct and consistent microbial community within local populations, but it varies across different geographical populations. The microbial functional profiles linked to the production of digestive enzymes, including cellulases and ligninases, are nonetheless globally conserved. This suggests that CRBs employ specific mechanisms to select and maintain microbes with functional benefits, contributing to host adaptability, stress tolerance, and fitness. The CRB microbial communities did not appear to recapitulate the genetic variation of their hosts. Rather than depend on obligate symbionts, CRBs seem to establish similar digestive associations with whatever environmentally acquired microbes are available wherever they are, aiding them in successfully establishing after invading a new location.IMPORTANCECoconut rhinoceros beetles (CRBs) are notorious pests on Arecaceae plants, posing destructive threats to countries highly reliant on coconut, oil palm, and date palm as economic crops. In the last century, CRBs have rapidly expanded their presence to territories that were once free of these beetles. The United States, for instance, has officially designated CRBs as invasive and alien pests. Given their remarkable ability to swiftly adapt to new environments, their gut microbes may play a crucial role in this process. While the microbiota of CRBs vary depending on geographical location, these beetles consistently exhibit a functionally identical digestive association with locally acquired microbes. This underscores the significance of CRB-microbe association in shaping the adaptive strategies of this agricultural pest.
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Affiliation(s)
- Chiao-Jung Han
- Department of Entomology, National Taiwan University, Taipei, Taiwan
| | - Jen-Pan Huang
- Biodiversity Research Center, Academia Sinica, Taipei, Taiwan
| | - Min-Rou Chiang
- Department of Entomology, National Taiwan University, Taipei, Taiwan
| | | | - Nitesh Nand
- Plant Health Laboratory, The Pacific Community, Suva, Fiji
| | - Kayvan Etebari
- Faculty of Science, School of Agriculture and Food Sustainability, The University of Queensland, Gatton, Australia
| | - Matan Shelomi
- Department of Entomology, National Taiwan University, Taipei, Taiwan
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Fathima S, Al Hakeem WG, Shanmugasundaram R, Lourenco J, Selvaraj RK. The effect of supplemental arginine on the gut microbial homeostasis of broilers during sub-clinical necrotic enteritis challenge. Front Physiol 2024; 15:1463420. [PMID: 39355151 PMCID: PMC11442325 DOI: 10.3389/fphys.2024.1463420] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/11/2024] [Accepted: 09/02/2024] [Indexed: 10/03/2024] Open
Abstract
Necrotic enteritis (NE) is an enteric disease of poultry that alters the structure of the gut microbial community causing dysbiosis. This 28 day experiment investigated the effects of 125% and 135% arginine diets on the gut microbial diversity and composition of broilers during a subclinical NE challenge. One hundred and twenty one-day-old chicks were randomly allocated to 4 treatments with six replicates each- Uninfected + Basal, NE + Basal, NE + Arg 125%, and NE + Arg 135% diet groups. NE was induced by inoculating 1 × 104 E. maxima sporulated oocysts on day 14 and 1 × 108 CFU C. perfringens on days 19, 20, and 21 of age. The NE challenge significantly decreased the number of observed amplicon sequence variants (p = 0.03), the abundance of the phylum Firmicutes (p < 0.01), and the species Mediterraneibacter cottocaccae (p = 0.01) in the ceca of birds on day 21. The NE challenge significantly increased the Bray-Curtis index (p < 0.01), and the abundance of the phylum Bacteroidota (p < 0.01), family Odoribacteraceae (p < 0.01), genus Odoribacter (p < 0.01), and species O. splanchnicus (p = 0.01) on day 21. During NE, the 125% arginine diet restored the abundance of the phylum Bacteroidota (p = 0.03), family Odoribacteraceae (p = 0.03) and Oscillospiraceae (p = 0.03), genus Odoribacter (p = 0.03), and species O. splanchnicus (p = 0.03) and M. cottocaccae (p < 0.01) on day 21. The 135% arginine diet effectively restored the loss in alpha diversity (p = 0.01) caused by NE, the abundance of the phylum Firmicutes (p = 0.01) and Bacteroidota (p < 0.01), family Oscillospiraceae (p = 0.03) and Odoribacteraceae (p < 0.01), genus Odoribacter (p < 0.01), and species O. splanchnicus (p < 0.01) and M. cottocaccae (p < 0.01) on day 21. On day 28, the treatments had a significant effect on the cecal propionate (p = 0.01), butyrate (p = 0.04), and total SCFA (p = 0.04) concentrations. In conclusion, the 125% and 135% arginine diets restored gut microbial composition during a subclinical NE challenge, but not the cecal SCFA profile. Hence, arginine in combination with other feed additives could be used in restoring gut microbial homeostasis during NE in poultry.
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Affiliation(s)
- Shahna Fathima
- Department of Poultry Science, University of Georgia, Athens, GA, United States
| | - Walid G Al Hakeem
- Department of Poultry Science, University of Georgia, Athens, GA, United States
| | - Revathi Shanmugasundaram
- Toxicology and Mycotoxin Research Unit, U.S. National Poultry Research Center, Athens, GA, United States
| | - Jeferson Lourenco
- Department of Animal and Dairy Science, University of Georgia, Athens, GA, United States
| | - Ramesh K Selvaraj
- Department of Poultry Science, University of Georgia, Athens, GA, United States
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Stapleton TE, Lindsey LM, Sundar H, Dearing MD. Rodents consuming the same toxic diet harbor a unique functional core microbiome. Anim Microbiome 2024; 6:43. [PMID: 39080711 PMCID: PMC11289948 DOI: 10.1186/s42523-024-00330-7] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/30/2024] [Accepted: 07/16/2024] [Indexed: 08/02/2024] Open
Abstract
Gut microbiota are intrinsic to an herbivorous lifestyle, but very little is known about how plant secondary compounds (PSCs), which are often toxic, influence these symbiotic partners. Here we interrogated the possibility of unique functional core microbiomes in populations of two species of woodrat (Neotoma lepida and bryanti) that have independently converged to feed on the same toxic diet (creosote bush; Larrea tridentata) and compared them to populations that do not feed on creosote bush. Leveraging this natural experiment, we collected samples across a large geographic region in the U.S. desert southwest from 20 populations (~ 150 individuals) with differential ingestion of creosote bush and analyzed three gut regions (foregut, cecum, hindgut) using16S sequencing and shotgun metagenomics. In each gut region sampled, we found a distinctive set of microbes in individuals feeding on creosote bush that were more abundant than other ASVs, enriched in creosote feeding woodrats, and occurred more frequently than would be predicted by chance. Creosote core members were from microbial families e.g., Eggerthellaceae, known to metabolize plant secondary compounds and three of the identified core KEGG orthologs (4-hydroxybenzoate decarboxylase, benzoyl-CoA reductase subunit B, and 2-pyrone-4, 6-dicarboxylate lactonase) coded for enzymes that play important roles in metabolism of plant secondary compounds. The results support the hypothesis that the ingestion of creosote bush sculpts the microbiome across all major gut regions to select for functional characteristics associated with the degradation of the PSCs in this unique diet.
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Affiliation(s)
- Tess E Stapleton
- School of Biological Sciences, University of Utah, 257 South 1400 East, Salt Lake City, UT, 84112, USA.
| | - LeAnn M Lindsey
- School of Computing, University of Utah, 50 Central Campus Dr, Salt Lake City, UT, 84112, USA
| | - Hari Sundar
- School of Computing, University of Utah, 50 Central Campus Dr, Salt Lake City, UT, 84112, USA
| | - M Denise Dearing
- School of Biological Sciences, University of Utah, 257 South 1400 East, Salt Lake City, UT, 84112, USA
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Wang W, Portal-Gonzalez N, Wang X, Li J, Li H, Portieles R, Borras-Hidalgo O, He W, Santos-Bermudez R. Insights into the microbial assembly and metabolites associated with ginger (Zingiber officinale L. Roscoe) microbial niches and agricultural environments. THE SCIENCE OF THE TOTAL ENVIRONMENT 2024; 947:174395. [PMID: 38992353 DOI: 10.1016/j.scitotenv.2024.174395] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 05/04/2024] [Revised: 06/27/2024] [Accepted: 06/28/2024] [Indexed: 07/13/2024]
Abstract
Ginger, a vegetable export from China, is well-known for its spicy flavour and use in traditional Chinese medicine. By examining the interactions of ginger plants' microbiome and metabolome, we can gain insights to advance agriculture, the environment, and other fields. Our study used metataxonomic analysis to investigate ginger plants' prokaryotic and fungal microbiomes in open fields and greenhouses. We also conducted untargeted metabolomic analysis to identify specific metabolites closely associated with ginger microbiome assembly under both agricultural conditions. Various bacteria and fungi were classified as generalists or specialists based on their ability to thrive in different environments and microbial niches. Our results indicate that ginger plants grown in greenhouses have a greater prokaryotic diversity, while those grown in open fields exhibit a greater fungal diversity. We have identified specific co-occurring prokaryotic and fungal genera associated with ginger plant agroecosystems that can enhance the health and growth of ginger plants while maintaining a healthy environment. In the open field these genera include Sphingomonas, Methylobacterium-Methylorubrum, Bacillus, Acidovorax, Rhizobium, Microbacterium, unclassified_f_Comamonadaceae, Herbaspirillum, Klebsiella, Enterobacter, Chryseobacterium, Nocardioides, Subgroup_10, Enterococcus, Pseudomonas, Devosia, g_unclassified_f_Chaetomiaceae, Pseudaleuria, Mortierella, Cheilymenia, and Pseudogymnoascus. In the greenhouse, the enriched genera were Rhizobium, Stenotrophomonas, Aureimonas, Bacillus, Nocardioides, Pseudomonas, Enterobacter, Delftia, Trichoderma, Mortierella, Cheilymenia, Schizothecium, and Actinomucor. Our research has identified several previously unknown microbial genera for ginger plant agroecosystems. Furthermore, our study has important implications for understanding the correlation between ginger's microbiome and metabolome profiles in diverse environments and may pave the way for future research. Specific microbial genera in crop production environments are associated with essential metabolites, including Safingol, Docosatrienoic acid, P-acetaminophen, and Hypoglycin B.
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Affiliation(s)
- Wenbo Wang
- School of Biological Science and Technology, University of Jinan, No. 336, West Road of Nan Xinzhuang, Jinan 250022, Shandong, People's Republic of China.
| | - Nayanci Portal-Gonzalez
- School of Biological Science and Technology, University of Jinan, No. 336, West Road of Nan Xinzhuang, Jinan 250022, Shandong, People's Republic of China
| | - Xia Wang
- School of Biological Science and Technology, University of Jinan, No. 336, West Road of Nan Xinzhuang, Jinan 250022, Shandong, People's Republic of China
| | - Jialin Li
- School of Biological Science and Technology, University of Jinan, No. 336, West Road of Nan Xinzhuang, Jinan 250022, Shandong, People's Republic of China.
| | - Hui Li
- School of Biological Science and Technology, University of Jinan, No. 336, West Road of Nan Xinzhuang, Jinan 250022, Shandong, People's Republic of China.
| | - Roxana Portieles
- Joint R&D Center of Biotechnology, RETDA, Yota Bio-Engineering Co., Ltd., 99 Shenzhen Road, Rizhao 276826, Shandong, People's Republic of China.
| | - Orlando Borras-Hidalgo
- Joint R&D Center of Biotechnology, RETDA, Yota Bio-Engineering Co., Ltd., 99 Shenzhen Road, Rizhao 276826, Shandong, People's Republic of China.
| | - Wenxing He
- School of Biological Science and Technology, University of Jinan, No. 336, West Road of Nan Xinzhuang, Jinan 250022, Shandong, People's Republic of China.
| | - Ramon Santos-Bermudez
- School of Biological Science and Technology, University of Jinan, No. 336, West Road of Nan Xinzhuang, Jinan 250022, Shandong, People's Republic of China.
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De Meester L, Vázquez-Domínguez E, Kassen R, Forest F, Bellon MR, Koskella B, Scherson RA, Colli L, Hendry AP, Crandall KA, Faith DP, Starger CJ, Geeta R, Araki H, Dulloo EM, Souffreau C, Schroer S, Johnson MTJ. A link between evolution and society fostering the UN sustainable development goals. Evol Appl 2024; 17:e13728. [PMID: 38884021 PMCID: PMC11178947 DOI: 10.1111/eva.13728] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/28/2023] [Revised: 05/16/2024] [Accepted: 05/17/2024] [Indexed: 06/18/2024] Open
Abstract
Given the multitude of challenges Earth is facing, sustainability science is of key importance to our continued existence. Evolution is the fundamental biological process underlying the origin of all biodiversity. This phylogenetic diversity fosters the resilience of ecosystems to environmental change, and provides numerous resources to society, and options for the future. Genetic diversity within species is also key to the ability of populations to evolve and adapt to environmental change. Yet, the value of evolutionary processes and the consequences of their impairment have not generally been considered in sustainability research. We argue that biological evolution is important for sustainability and that the concepts, theory, data, and methodological approaches used in evolutionary biology can, in crucial ways, contribute to achieving the UN Sustainable Development Goals (SDGs). We discuss how evolutionary principles are relevant to understanding, maintaining, and improving Nature Contributions to People (NCP) and how they contribute to the SDGs. We highlight specific applications of evolution, evolutionary theory, and evolutionary biology's diverse toolbox, grouped into four major routes through which evolution and evolutionary insights can impact sustainability. We argue that information on both within-species evolutionary potential and among-species phylogenetic diversity is necessary to predict population, community, and ecosystem responses to global change and to make informed decisions on sustainable production, health, and well-being. We provide examples of how evolutionary insights and the tools developed by evolutionary biology can not only inspire and enhance progress on the trajectory to sustainability, but also highlight some obstacles that hitherto seem to have impeded an efficient uptake of evolutionary insights in sustainability research and actions to sustain SDGs. We call for enhanced collaboration between sustainability science and evolutionary biology to understand how integrating these disciplines can help achieve the sustainable future envisioned by the UN SDGs.
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Affiliation(s)
- Luc De Meester
- Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB) Berlin Germany
- Laboratory of Aquatic Ecology, Evolution and Conservation KU Leuven Leuven Belgium
- Institute of Biology Freie University Berlin Berlin Germany
- Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB) Berlin Germany
| | - Ella Vázquez-Domínguez
- Departamento de Ecología de la Biodiversidad, Instituto de Ecología, Universidad Nacional Autónoma de México Ciudad Universitaria Ciudad de México Mexico
- Conservation and Evolutionary Genetics Group Estación Biológica de Doñana (EBD-CSIC) Sevilla Spain
| | - Rees Kassen
- Department of Biology McGill University Montreal Quebec Canada
| | | | - Mauricio R Bellon
- Comisión Nacional Para el Conocimiento y Uso de la Biodiversidad (CONABIO) México City Mexico
- Swette Center for Sustainable Food Systems Arizona State University Tempe Arizona USA
| | - Britt Koskella
- Department of Integrative Biology University of California Berkeley California USA
| | - Rosa A Scherson
- Laboratorio Evolución y Sistemática, Departamento de Silvicultura y Conservación de la Naturaleza Universidad de Chile Santiago Chile
| | - Licia Colli
- Dipartimento di Scienze Animali, Della Nutrizione e Degli Alimenti, BioDNA Centro di Ricerca Sulla Biodiversità e Sul DNA Antico, Facoltà di Scienze Agrarie, Alimentari e Ambientali Università Cattolica del Sacro Cuore Piacenza Italy
| | - Andrew P Hendry
- Redpath Museum & Department of Biology McGill University Montreal Quebec Canada
| | - Keith A Crandall
- Department of Biostatistics and Bioinformatics George Washington University Washington DC USA
- Department of Invertebrate Zoology, US National Museum of Natural History Smithsonian Institution Washington DC USA
| | | | - Craig J Starger
- School of Global Environmental Sustainability Colorado State University Fort Collins Colorado USA
| | - R Geeta
- Department of Botany University of Delhi New Delhi India
| | - Hitoshi Araki
- Research Faculty of Agriculture Hokkaido University Sapporo Japan
| | - Ehsan M Dulloo
- Effective Genetic Resources Conservation and Use Alliance of Bioversity International and CIAT Rome Italy
| | - Caroline Souffreau
- Laboratory of Aquatic Ecology, Evolution and Conservation KU Leuven Leuven Belgium
| | - Sibylle Schroer
- Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB) Berlin Germany
| | - Marc T J Johnson
- Department of Biology & Centre for Urban Environments University of Toronto Mississauga Mississauga Ontario Canada
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Chui ZSW, Chan LML, Zhang EWH, Liang S, Choi EPH, Lok KYW, Tun HM, Kwok JYY. Effects of microbiome-based interventions on neurodegenerative diseases: a systematic review and meta-analysis. Sci Rep 2024; 14:9558. [PMID: 38664425 PMCID: PMC11045862 DOI: 10.1038/s41598-024-59250-w] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/07/2023] [Accepted: 04/08/2024] [Indexed: 04/28/2024] Open
Abstract
Neurodegenerative diseases (NDDs) are characterized by neuronal damage and progressive loss of neuron function. Microbiome-based interventions, such as dietary interventions, biotics, and fecal microbiome transplant, have been proposed as a novel approach to managing symptoms and modulating disease progression. Emerging clinical trials have investigated the efficacy of interventions modulating the GM in alleviating or reversing disease progression, yet no comprehensive synthesis have been done. A systematic review of the literature was therefore conducted to investigate the efficacy of microbiome-modulating methods. The search yielded 4051 articles, with 15 clinical trials included. The overall risk of bias was moderate in most studies. Most microbiome-modulating interventions changed the GM composition. Despite inconsistent changes in GM composition, the meta-analysis showed that microbiome-modulating interventions improved disease burden (SMD, - 0.57; 95% CI - 0.93 to - 0.21; I2 = 42%; P = 0.002) with a qualitative trend of improvement in constipation. However, current studies have high methodological heterogeneity and small sample sizes, requiring more well-designed and controlled studies to elucidate the complex linkage between microbiome, microbiome-modulating interventions, and NDDs.
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Affiliation(s)
- Zara Siu Wa Chui
- School of Biomedical Sciences, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong SAR, China
| | - Lily Man Lee Chan
- School of Nursing, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong SAR, China
| | - Esther Wan Hei Zhang
- Faculty of Medicine, The Chinese University of Hong Kong, Shatin, Hong Kong SAR, China
| | - Suisha Liang
- HKU-Pasteur Research Pole, School of Public Health, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong SAR, China
- Microbiota I-Center (MagIC), Hong Kong SAR, China
| | - Edmond Pui Hang Choi
- School of Nursing, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong SAR, China
| | - Kris Yuet Wan Lok
- School of Nursing, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong SAR, China
| | - Hein Min Tun
- The Jockey Club School of Public Health and Primary Care, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong SAR, China
- Microbiota I-Center (MagIC), Hong Kong SAR, China
- Li Ka Shing Institute of Health Sciences, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong SAR, China
| | - Jojo Yan Yan Kwok
- School of Nursing, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong SAR, China.
- Centre on Behavioral Health, The University of Hong Kong, Pokfulam, Hong Kong SAR, China.
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9
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Siriarchawatana P, Harnpicharnchai P, Phithakrotchanakoon C, Kitikhun S, Mayteeworakoon S, Chunhametha S, Eurwilaichitr L, Ingsriswang S. Elucidating potential bioindicators from insights in the diversity and assembly processes of prokaryotic and eukaryotic communities in the Mekong River. ENVIRONMENTAL RESEARCH 2024; 243:117800. [PMID: 38056615 DOI: 10.1016/j.envres.2023.117800] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 07/27/2023] [Revised: 11/23/2023] [Accepted: 11/25/2023] [Indexed: 12/08/2023]
Abstract
Drivers for spatio-temporal distribution patterns of overall planktonic prokaryotes and eukaryotes in riverine ecosystems are generally not fully understood. This study employed amplicon metabarcoding to investigate the distributions and assembly mechanisms of bacterial and eukaryotic communities in the Mekong River. The prevailing bacteria taxa were found to be Betaproteobacteria, Actinobacteria, and Bacteroidetes, while the dominant eukaryotic organisms were cryptophytes, chlorophytes, and diatoms. The community assemblages were influenced by a combination of stochastic and deterministic processes. Drift (DR) and dispersal limitation (DL), signifying the stochastic mechanism, were the main processes shaping the overall prokaryotic and eukaryotic communities. However, homogeneous selection (HoS), indicating deterministic mechanism, played a major role in the assembly process of core prokaryotic communities, especially in the wet season. In contrast, the core eukaryotic communities including Opisthokonta, Sar, and Chlorophyta were dominated by stochastic processes. The significance of HoS within prokaryotic communities was also found to exhibit a decreasing trend from the upstream sampling sites (Chiang Saen and Chiang Khan, Nong Khai) towards the downstream sites (Mukdahan, and Khong Chiam) of the Mekong River. The environmental gradients resulting from the site-specific variations and the gradual decrease in elevation along the river may have a potential influence on the role of HoS in community assembly. Crucial environmental factors that shape the phylogenetic structure within distinct bins of the core prokaryotic communities including water depth, temperature, chloride, sodium, and sulphate were identified, as inferred by their correlation with the beta Net Relatedness Index (betaNRI) during the wet season. Overall, these findings enhance understanding of the complex mechanisms governing the spatio-temporal dynamics of prokaryotic and eukaryotic communities in the Mekong River. Finally, insights gained from this study could provide information on further use of specific core bacteria as microbial-based bioindicators that are effective for the assessment and conservation of the Mekong River ecosystem.
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Affiliation(s)
- Paopit Siriarchawatana
- Thailand Bioresource Research Center (TBRC), National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Pathumthani, Thailand
| | - Piyanun Harnpicharnchai
- Thailand Bioresource Research Center (TBRC), National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Pathumthani, Thailand
| | - Chitwadee Phithakrotchanakoon
- Thailand Bioresource Research Center (TBRC), National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Pathumthani, Thailand
| | - Supattra Kitikhun
- Thailand Bioresource Research Center (TBRC), National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Pathumthani, Thailand
| | - Sermsiri Mayteeworakoon
- Thailand Bioresource Research Center (TBRC), National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Pathumthani, Thailand
| | - Suwanee Chunhametha
- Thailand Bioresource Research Center (TBRC), National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Pathumthani, Thailand
| | - Lily Eurwilaichitr
- National Energy Technology Center (ENTEC), National Science and Technology Development Agency (NSTDA), Pathumthani, Thailand
| | - Supawadee Ingsriswang
- Thailand Bioresource Research Center (TBRC), National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Pathumthani, Thailand.
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10
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Yin P, Du T, Yi S, Zhang C, Yu L, Tian F, Chen W, Zhai Q. Response differences of gut microbiota in oligofructose and inulin are determined by the initial gut Bacteroides/Bifidobacterium ratios. Food Res Int 2023; 174:113598. [PMID: 37986462 DOI: 10.1016/j.foodres.2023.113598] [Citation(s) in RCA: 7] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/30/2023] [Revised: 10/07/2023] [Accepted: 10/13/2023] [Indexed: 11/22/2023]
Abstract
Prebiotics are known to modulate the gut microbiota, but there is host variability, mainly due to differences in carbohydrate-utilisation by gut microbiota. Bifidobacterium and Bacteroides are powerful carbohydrate-utilising bacteria, and the ratio of both is closely related to the utilisation of prebiotics. However, the differential impact of prebiotics on the composition and function of the gut microbiota and its metabolites in participants with different Bacteroides/Bifidobacterium (Ba/Bi) ratios have not been studied. Here, we conducted a 4-week randomised double-blind, parallel four-arm trial using two prebiotics (oligofructose and inulin) in two populations with high Ba/Bi (H) and low Ba/Bi (L). The response to prebiotics in both populations was influenced by the baseline microbiota background specificity. Notably, at an overall level, FOS was slightly better than inulin in modulating the gut microbiota. Difference in gut microbiota regulation by FOS across microbiota contexts were significant between the two groups. Butyric acid-producing bacteria were significantly more abundant in H and further elevated butyric acid and related metabolite levels, with H more likely to benefit from the FOS intervention. The two groups showed only metabolic differences in their response to inulin, with L showing a significant increase in propionic acid and being enriched in glycolysis functions, whereas H was enriched in amino acids and aminoglycolysis functions. Overall, these results provide a basis for selecting appropriate prebiotics for participants with different gut backgrounds.
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Affiliation(s)
- Pingping Yin
- State Key Laboratory of Food Science and Resources, Jiangnan University, Wuxi 214122, China; School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
| | - Ting Du
- State Key Laboratory of Food Science and Resources, Jiangnan University, Wuxi 214122, China; School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
| | - Shanrong Yi
- State Key Laboratory of Food Science and Resources, Jiangnan University, Wuxi 214122, China; School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
| | - Chengcheng Zhang
- State Key Laboratory of Food Science and Resources, Jiangnan University, Wuxi 214122, China; School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
| | - Leilei Yu
- State Key Laboratory of Food Science and Resources, Jiangnan University, Wuxi 214122, China; School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
| | - Fengwei Tian
- State Key Laboratory of Food Science and Resources, Jiangnan University, Wuxi 214122, China; School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
| | - Wei Chen
- State Key Laboratory of Food Science and Resources, Jiangnan University, Wuxi 214122, China; School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China; National Engineering Research Center for Functional Food, Jiangnan University, Wuxi, Jiangsu 214122, China
| | - Qixiao Zhai
- State Key Laboratory of Food Science and Resources, Jiangnan University, Wuxi 214122, China; School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China.
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11
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Bloemendaal M, Vlaming P, de Boer A, Vermeulen-Kalk K, Bouman A, Kleefstra T, Arias Vasquez A. The role of the gut microbiota in patients with Kleefstra syndrome. Am J Med Genet B Neuropsychiatr Genet 2023; 192:124-138. [PMID: 36630271 DOI: 10.1002/ajmg.b.32926] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/31/2022] [Revised: 12/15/2022] [Accepted: 12/16/2022] [Indexed: 01/12/2023]
Abstract
Kleefstra Syndrome (KS) is a rare monogenetic syndrome, caused by haploinsufficiency of the euchromatic histone methyl transferase 1 (EHMT1) gene, an important regulator of neurodevelopment. The clinical features of KS include intellectual disability, autistic behavior and gastrointestinal problems. The gut microbiota, an important modifier of the gut-brain-axis, may constitute an unexplored mechanism underlying clinical KS variation. We investigated the gut microbiota composition of 23 individuals with KS (patients) and 40 of their family members, to test whether (1) variation in the gut microbiota associates with KS diagnosis and (2) variation within the gut microbiota relates with KS syndrome symptoms. Both alpha and beta diversity of patients were different from their family members. Genus Coprococcus 3 was lower in abundance in patients compared to family members. Moreover, abundance of genus Merdibacter was lower in patients versus family members, but only in participants reporting intestinal complaints. Within the patient group, behavioral problems explained 7% of beta diversity variance. Also, within this group, we detected higher levels of Atopobiaceae - uncultured and Ruminococcaceae Subdoligranulum associated with higher symptom severity. These significant signatures in the gut microbiota composition in patients with KS suggest that microbiota differences are part of the KS phenotype.
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Affiliation(s)
- Mirjam Bloemendaal
- Department of Human Genetics, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands
- Department of Psychiatry, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands
| | - Priscilla Vlaming
- Department of Human Genetics, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands
| | - Anneke de Boer
- Karakter Child and Adolescent Psychiatry University Centre, Nijmegen, The Netherlands
| | - Karlijn Vermeulen-Kalk
- Department of Human Genetics, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands
- Karakter Child and Adolescent Psychiatry University Centre, Nijmegen, The Netherlands
| | - Arianne Bouman
- Department of Human Genetics, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands
| | - Tjitske Kleefstra
- Department of Human Genetics, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands
- Department of Psychiatry, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands
- Centre of Excellence for Neuropsychiatry, Vincent van Gogh Institute for Psychiatry, Venray, The Netherlands
| | - Alejandro Arias Vasquez
- Department of Human Genetics, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands
- Department of Psychiatry, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands
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12
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Chung CJ, Hermes BM, Gupta Y, Ibrahim S, Belheouane M, Baines JF. Genome-wide mapping of gene-microbe interactions in the murine lung microbiota based on quantitative microbial profiling. Anim Microbiome 2023; 5:31. [PMID: 37264412 DOI: 10.1186/s42523-023-00250-y] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/22/2022] [Accepted: 05/10/2023] [Indexed: 06/03/2023] Open
Abstract
BACKGROUND Mammalian lungs comprise a complex microbial ecosystem that interacts with host physiology. Previous research demonstrates that the environment significantly contributes to bacterial community structure in the upper and lower respiratory tract. However, the influence of host genetics on the makeup of lung microbiota remains ambiguous, largely due to technical difficulties related to sampling, as well as challenges inherent to investigating low biomass communities. Thus, innovative approaches are warranted to clarify host-microbe interactions in the mammalian lung. RESULTS Here, we aimed to characterize host genomic regions associated with lung bacterial traits in an advanced intercross mouse line (AIL). By performing quantitative microbial profiling (QMP) using the highly precise method of droplet digital PCR (ddPCR), we refined 16S rRNA gene amplicon-based traits to identify and map candidate lung-resident taxa using a QTL mapping approach. In addition, the two abundant core taxa Lactobacillus and Pelomonas were chosen for independent microbial phenotyping using genus-specific primers. In total, this revealed seven significant loci involving eight bacterial traits. The narrow confidence intervals afforded by the AIL population allowed us to identify several promising candidate genes related to immune and inflammatory responses, cell apoptosis, DNA repair, and lung functioning and disease susceptibility. Interestingly, one genomic region associated with Lactobacillus abundance contains the well-known anti-inflammatory cytokine Il10, which we confirmed through the analysis of Il10 knockout mice. CONCLUSIONS Our study provides the first evidence for a role of host genetic variation contributing to variation in the lung microbiota. This was in large part made possible through the careful curation of 16S rRNA gene amplicon data and the incorporation of a QMP-based methods. This approach to evaluating the low biomass lung environment opens new avenues for advancing lung microbiome research using animal models.
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Affiliation(s)
- C J Chung
- Max Planck Institute for Evolutionary Biology, August-Thienemann-Str. 2, 24306, Plön, Germany
- Section of Evolutionary Medicine, Institute for Experimental Medicine, Kiel University, Arnold-Heller-Str. 3, 24105, Kiel, Germany
| | - B M Hermes
- Max Planck Institute for Evolutionary Biology, August-Thienemann-Str. 2, 24306, Plön, Germany
- Section of Evolutionary Medicine, Institute for Experimental Medicine, Kiel University, Arnold-Heller-Str. 3, 24105, Kiel, Germany
| | - Y Gupta
- Division of Nephrology, Department of Medicine, Columbia University Irving Medical Center, New York, NY, 10032, USA
| | - S Ibrahim
- College of Medicine and Health Sciences, Khalifa University, Abu Dhabi, UAE
| | - Meriem Belheouane
- Max Planck Institute for Evolutionary Biology, August-Thienemann-Str. 2, 24306, Plön, Germany.
- Section of Evolutionary Medicine, Institute for Experimental Medicine, Kiel University, Arnold-Heller-Str. 3, 24105, Kiel, Germany.
- Research Center Borstel, Evolution of the Resistome, Leibniz Lung Center, Parkallee 1-40, 23845, Borstel, Germany.
| | - John F Baines
- Max Planck Institute for Evolutionary Biology, August-Thienemann-Str. 2, 24306, Plön, Germany.
- Section of Evolutionary Medicine, Institute for Experimental Medicine, Kiel University, Arnold-Heller-Str. 3, 24105, Kiel, Germany.
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13
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Prüter H, Gillingham MAF, Krietsch J, Kuhn S, Kempenaers B. Sexual transmission may drive pair similarity of the cloacal microbiome in a polyandrous species. J Anim Ecol 2023. [PMID: 37230950 DOI: 10.1111/1365-2656.13961] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/24/2022] [Accepted: 05/05/2023] [Indexed: 05/27/2023]
Abstract
All animals host a microbial community within and on their reproductive organs, known as the reproductive microbiome. In free-living birds, studies on the sexual transmission of bacteria have typically focused on a few pathogens instead of the bacterial community as a whole, despite a potential link to reproductive function. Theory predicts higher sexual transmission of the reproductive microbiome in females via the males' ejaculates and higher rates of transmission in promiscuous systems. We studied the cloacal microbiome of breeding individuals of a socially polyandrous, sex-role-reversed shorebird, the red phalarope (Phalaropus fulicarius). We expected (i) higher microbial diversity in females compared to males; (ii) low compositional differentiation between sexes; (iii) lower variation in composition between individuals (i.e. microbiome dispersion) in females than in males; (iv) convergence in composition as the breeding season progresses as a consequence of sexual transmission and/or shared habitat use; and (v) higher similarity in microbial composition between social pair members than between two random opposite-sex individuals. We found no or small between-sex differences in cloacal microbiome diversity/richness and composition. Dispersion of predicted functional pathways was lower in females than in males. As predicted, microbiome dispersion decreased with sampling date relative to clutch initiation of the social pair. Microbiome composition was significantly more similar among social pair members than among two random opposite-sex individuals. Pair membership explained 21.5% of the variation in taxonomic composition and 10.1% of functional profiles, whereas temporal and sex effects explained only 0.6%-1.6%. Consistent with evidence of functional convergence of reproductive microbiomes within pairs, some select taxa and predicted functional pathways were less variable between social pair members than between random opposite-sex individuals. As predicted if sexual transmission of the reproductive microbiome is high, sex differences in microbiome composition were weak in a socially polyandrous system with frequent copulations. Moreover, high within-pair similarity in microbiome composition, particularly for a few taxa spanning the spectrum of the beneficial-pathogenic axis, demonstrates the link between mating behaviour and the reproductive microbiome. Our study is consistent with the hypothesis that sexual transmission plays an important role in driving reproductive microbiome ecology and evolution.
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Affiliation(s)
- Hanna Prüter
- Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Biological Intelligence, Seewiesen, Germany
| | - Mark A F Gillingham
- Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Biological Intelligence, Seewiesen, Germany
- Biodiversity Research Institute (CSIC, Oviedo University, Principality of Asturias), University of Oviedo, Mieres, Spain
| | - Johannes Krietsch
- Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Biological Intelligence, Seewiesen, Germany
| | - Sylvia Kuhn
- Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Biological Intelligence, Seewiesen, Germany
| | - Bart Kempenaers
- Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Biological Intelligence, Seewiesen, Germany
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14
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Dietz MW, Matson KD, Versteegh MA, van der Velde M, Parmentier HK, Arts JAJ, Salles JF, Tieleman BI. Gut microbiota of homing pigeons shows summer-winter variation under constant diet indicating a substantial effect of temperature. Anim Microbiome 2022; 4:64. [PMID: 36514126 PMCID: PMC9749179 DOI: 10.1186/s42523-022-00216-6] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/20/2022] [Accepted: 11/29/2022] [Indexed: 12/15/2022] Open
Abstract
BACKGROUND Gut microbiotas play a pivotal role in host physiology and behaviour, and may affect host life-history traits such as seasonal variation in host phenotypic state. Generally, seasonal gut microbiota variation is attributed to seasonal diet variation. However, seasonal temperature and day length variation may also drive gut microbiota variation. We investigated summer-winter differences in the gut bacterial community (GBC) in 14 homing pigeons living outdoors under a constant diet by collecting cloacal swabs in both seasons during two years. Because temperature effects may be mediated by host metabolism, we determined basal metabolic rate (BMR) and body mass. Immune competence is influenced by day length and has a close relationship with the GBC, and it may thus be a link between day length and gut microbiota. Therefore, we measured seven innate immune indices. We expected the GBC to show summer-winter differences and to correlate with metabolism and immune indices. RESULTS BMR, body mass, and two immune indices varied seasonally, other host factors did not. The GBC showed differences between seasons and sexes, and correlated with metabolism and immune indices. The most abundant genus (Lachnoclostridium 12, 12%) and associated higher taxa, were more abundant in winter, though not significantly at the phylum level, Firmicutes. Bacteroidetes were more abundant in summer. The Firmicutes:Bacteroidetes ratio tended to be higher in winter. The KEGG ortholog functions for fatty acid biosynthesis and linoleic acid metabolism (PICRUSt2) had increased abundances in winter. CONCLUSIONS The GBC of homing pigeons varied seasonally, even under a constant diet. The correlations between immune indices and the GBC did not involve consistently specific immune indices and included only one of the two immune indices that showed seasonal differences, suggesting that immune competence may be an unlikely link between day length and the GBC. The correlations between the GBC and metabolism indices, the higher Firmicutes:Bacteroidetes ratio in winter, and the resemblance of the summer-winter differences in the GBC with the general temperature effects on the GBC in the literature, suggest that temperature partly drove the summer-winter differences in the GBC in homing pigeons.
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Affiliation(s)
- Maurine W Dietz
- Groningen Institute for Evolutionary Life Sciences, University of Groningen, Nijenborgh 7, 9747AG, Groningen, The Netherlands.
| | - Kevin D Matson
- Wildlife Ecology and Conservation, Environmental Science Group, Wageningen University & Research, Droevendaalsesteeg 3a, 6708PB, Wageningen, The Netherlands.
| | - Maaike A Versteegh
- Groningen Institute for Evolutionary Life Sciences, University of Groningen, Nijenborgh 7, 9747AG, Groningen, The Netherlands
| | - Marco van der Velde
- Groningen Institute for Evolutionary Life Sciences, University of Groningen, Nijenborgh 7, 9747AG, Groningen, The Netherlands
| | - Henk K Parmentier
- Adaptation Physiology Group, Department of Animal Sciences, Wageningen University & Research, De Elst 1, 6708 WD, Wageningen, The Netherlands
| | - Joop A J Arts
- Adaptation Physiology Group, Department of Animal Sciences, Wageningen University & Research, De Elst 1, 6708 WD, Wageningen, The Netherlands
| | - Joana F Salles
- Groningen Institute for Evolutionary Life Sciences, University of Groningen, Nijenborgh 7, 9747AG, Groningen, The Netherlands
| | - B Irene Tieleman
- Groningen Institute for Evolutionary Life Sciences, University of Groningen, Nijenborgh 7, 9747AG, Groningen, The Netherlands
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15
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He J, Shen X, Zhang N, Sun C, Shao Y. Smartphones as an Ecological Niche of Microorganisms: Microbial Activities, Assembly, and Opportunistic Pathogens. Microbiol Spectr 2022; 10:e0150822. [PMID: 36040152 PMCID: PMC9603676 DOI: 10.1128/spectrum.01508-22] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/26/2022] [Accepted: 08/11/2022] [Indexed: 12/31/2022] Open
Abstract
Smartphone usage and contact frequency are unprecedentedly high in this era, and they affect humans mentally and physically. However, the characteristics of the microorganisms associated with smartphones and smartphone hygiene habits remain unclear. In this study, using various culture-independent techniques, including high-throughput sequencing, real-time quantitative PCR (RT-qPCR), the ATP bioluminescence system, and electron microscopy, we investigated the structure, assembly, quantity, and dynamic metabolic activity of the bacterial community on smartphone surfaces and the user's dominant and nondominant hands. We found that smartphone microbiotas are more similar to the nondominant hand microbiotas than the dominant hand microbiotas and show significantly decreased phylogenetic diversity and stronger deterministic processes than the hand microbiota. Significant interindividual microbiota differences were observed, contributing to an average owner identification accuracy of 70.6% using smartphone microbiota. Furthermore, it is estimated that approximately 1.75 × 106 bacteria (2.24 × 104/cm2) exist on the touchscreen of a single smartphone, and microbial activities remain stable for at least 48 h. Scanning electron microscopy detected large fragments harboring microorganisms, suggesting that smartphone microbiotas live on the secreta or other substances, e.g., human cell debris and food debris. Fortunately, simple smartphone cleaning/hygiene could significantly reduce the bacterial load. Taken together, our results demonstrate that smartphone surfaces not only are a reservoir of microbes but also provide an ecological niche in which microbiotas, particularly opportunistic pathogens, can survive, be active, and even grow. IMPORTANCE Currently, people spend an average of 4.2 h per day on their smartphones. Due to the COVID-19 pandemic, this figure may still be increasing. The high frequency of smartphone usage may allow microbes, particularly pathogens, to attach to-and even survive on-phone surfaces, potentially causing adverse effects on humans. We employed various culture-independent techniques in this study to evaluate the microbiological features and hygiene of smartphones, including community assembly, bacterial load, and activity. Our data showed that deterministic processes drive smartphone microbiota assembly and that approximately 1.75 × 106 bacteria exist on a single smartphone touchscreen, with activities being stable for at least 48 h. Fortunately, simple smartphone cleaning/hygiene could significantly reduce the bacterial load. This work expands our understanding of the microbial ecology of smartphone surfaces and might facilitate the development of electronic device cleaning/hygiene guidelines to support public health.
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Affiliation(s)
- Jintao He
- Max Planck Partner Group, Faculty of Agriculture, Life and Environmental Sciences, Zhejiang University, Hangzhou, China
| | - Xiaoqiang Shen
- Max Planck Partner Group, Faculty of Agriculture, Life and Environmental Sciences, Zhejiang University, Hangzhou, China
| | - Nan Zhang
- Max Planck Partner Group, Faculty of Agriculture, Life and Environmental Sciences, Zhejiang University, Hangzhou, China
| | - Chao Sun
- Analysis Center of Agrobiology and Environmental Sciences, Zhejiang University, Hangzhou, China
| | - Yongqi Shao
- Max Planck Partner Group, Faculty of Agriculture, Life and Environmental Sciences, Zhejiang University, Hangzhou, China
- Key Laboratory for Molecular Animal Nutrition, Ministry of Education, Beijing, China
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16
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Schmid DW, Fackelmann G, Wasimuddin, Rakotondranary J, Ratovonamana YR, Montero BK, Ganzhorn JU, Sommer S. A framework for testing the impact of co-infections on host gut microbiomes. Anim Microbiome 2022; 4:48. [PMID: 35945629 PMCID: PMC9361228 DOI: 10.1186/s42523-022-00198-5] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/01/2021] [Accepted: 07/26/2022] [Indexed: 02/07/2023] Open
Abstract
Parasitic infections disturb gut microbial communities beyond their natural range of variation, possibly leading to dysbiosis. Yet it remains underappreciated that most infections are accompanied by one or more co-infections and their collective impact is largely unexplored. Here we developed a framework illustrating changes to the host gut microbiome following single infections, and build on it by describing the neutral, synergistic or antagonistic impacts on microbial α- and ß-diversity expected from co-infections. We tested the framework on microbiome data from a non-human primate population co-infected with helminths and Adenovirus, and matched patterns reported in published studies to the introduced framework. In this case study, α-diversity of co-infected Malagasy mouse lemurs (Microcebus griseorufus) did not differ in comparison with that of singly infected or uninfected individuals, even though community composition captured with ß-diversity metrices changed significantly. Explicitly, we record stochastic changes in dispersion, a sign of dysbiosis, following the Anna-Karenina principle rather than deterministic shifts in the microbial gut community. From the literature review and our case study, neutral and synergistic impacts emerged as common outcomes from co-infections, wherein both shifts and dispersion of microbial communities following co-infections were often more severe than after a single infection alone, but microbial α-diversity was not universally altered. Important functions of the microbiome may also suffer from such heavily altered, though no less species-rich microbial community. Lastly, we pose the hypothesis that the reshuffling of host-associated microbial communities due to the impact of various, often coinciding parasitic infections may become a source of novel or zoonotic diseases.
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17
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Carranco AS, Romo D, de Lourdes Torres M, Wilhelm K, Sommer S, Gillingham MAF. Egg microbiota is the starting point of hatchling gut microbiota in the endangered yellow-spotted Amazon river turtle. Mol Ecol 2022; 31:3917-3933. [PMID: 35621392 DOI: 10.1111/mec.16548] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/22/2021] [Revised: 04/30/2022] [Accepted: 05/17/2022] [Indexed: 11/29/2022]
Abstract
Establishment and development of gut microbiota during vertebrates' early life are likely to be important predictors of health and fitness. Host-parental and host-environment interactions are essential to these processes. In oviparous reptiles whose nests represent a source of the parent's microbial inocula, the relative role of host-selection and stochastic environmental factors during gut microbial assemblage remains unknown. We sampled eggs incubated in artificial nests as well as hatchlings and juveniles (up to 30 days old) of the yellow-spotted Amazon river turtle (Podocnemis unifilis) developing in tubs filled with river water. We examined the relative role of the internal egg microbiota and the abiotic environment on hatchling and juvenile turtle's cloacal microbiota assemblages during the first 30 days of development. A mean of 71% of ASVs in hatched eggs could be traced to the nest environmental microbiota and in turn a mean of 77% of hatchlings' cloacal ASVs were traced to hatched eggs. Between day 5 and 20 of juvenile turtle's development, the river water environment plays a key role in the establishment of the gut microbiota (accounting for a mean of 13%-34.6% of cloacal ASVs) and strongly influences shifts in microbial diversity and abundance. After day 20, shifts in gut microbiota composition were mainly driven by host-selection processes. Therefore, colonization by environmental microbiota is key in the initial stages of establishing the host's gut microbiota which is subsequently shaped by host-selection processes. Our study provides a novel quantitative understanding of the host-environment interactions during gut microbial assemblage of oviparous reptiles.
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Affiliation(s)
- Ana Sofia Carranco
- Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm, Germany
| | - David Romo
- Tiputini Biodiversity Station, Universidad San Francisco de Quito, Cumbaya-, Quito, Ecuador
| | - Maria de Lourdes Torres
- Laboratorio de Biotecnología Vegetal, Universidad San Francisco de Quito, Cumbaya-, Quito, Ecuador
| | - Kerstin Wilhelm
- Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm, Germany
| | - Simone Sommer
- Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm, Germany
| | - Mark A F Gillingham
- Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm, Germany.,Biodiversity Research Institute (CSIC, Oviedo University, Principality of Asturias), Campus of Mieres, University of Oviedo, 33600, Mieres, Spain
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A Faithful Gut: Core Features of Gastrointestinal Microbiota of Long-Distance Migratory Bats Remain Stable despite Dietary Shifts Driving Differences in Specific Bacterial Taxa. Microbiol Spectr 2021; 9:e0152521. [PMID: 34817279 PMCID: PMC8612142 DOI: 10.1128/spectrum.01525-21] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/20/2022] Open
Abstract
Migratory animals live in a world of constant change. Animals undergo many physiological changes preparing themselves for the migration. Although this field has been studied extensively over the last decades, we know relatively little about the seasonal changes that occur in the microbial communities that these animals carry in their guts. Here, we assessed the V4 region of the 16S rRNA high-throughput sequencing data as a proxy to estimate microbiome diversity of tequila bats from fecal pellets and evaluate how the natural process of migration shapes the microbiome composition and diversity. We collected samples from individual bats at two localities in the dry forest biome (Chamela and Coquimatlán) and one site at the endpoint of the migration in the Sonoran Desert (Pinacate). We found that the gut microbiome of the tequila bats is dominated largely by Firmicutes and Proteobacteria. Our data also provide insights on how microbiome diversity shifts at the same site in consecutive years. Our study has demonstrated that both locality and year-to-year variation contribute to shaping the composition, overall diversity, and “uniqueness” of the gut microbiome of migratory nectar-feeding female bats, with localities from the dry forest biome looking more like each other compared to those from the desert biome. In terms of beta diversity, our data show a stratified effect in which the samples’ locality was the strongest factor influencing the gut microbiome but with significant variation between consecutive years at the same locality. IMPORTANCE Migratory animals live in a world of constant change. The whole-body ecosystem needs a strong adapting capacity to thrive despite the changes. Our study used next-generation sequencing to determine how gut microbial change along the migratory path of the nectar-feeding tequila bats. The study of the gut microbiome is a great tool that can provide important insights that are relevant not just for management and conservation but also an initial investigation of the extent of the adaptation and preparedness of the individual animals, with respect not just to their current environment but also to all the environments involved in their yearly cycle.
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Sun Q, Wang ZL, Liu XC, Ji YC, He Y, Ai Q, Li LQ. Effect of the course of treatment with broad-spectrum antibiotics on intestinal flora and short-chain fatty acids in feces of very low birth weight infants: a prospective study. ZHONGGUO DANG DAI ER KE ZA ZHI = CHINESE JOURNAL OF CONTEMPORARY PEDIATRICS 2021; 23:1008-1014. [PMID: 34719415 DOI: 10.7499/j.issn.1008-8830.2107103] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Subscribe] [Scholar Register] [Indexed: 12/18/2022]
Abstract
OBJECTIVES To study the effect of the course of treatment with broad-spectrum antibiotics on intestinal flora and short-chain fatty acids (SCFAs) in feces of very low birth weight (VLBW) infants. METHODS A total of 29 VLBW infants who were admitted to the Neonatal Diagnosis and Treatment Center of Children's Hospital Affiliated to Chongqing Medical University from June to December 2020 were enrolled as subjects for this prospective study. According to the course of treatment with broad-spectrum antibiotics, they were divided into two groups: ≤7 days (n=9) and >7 days (n=20). Fecal samples were collected on days 14 and 28 of hospitalization, and 16S rDNA high-throughput sequencing and gas chromatography-mass spectrometry were used to analyze the flora and SCFAs in fecal samples. RESULTS There was a significant reduction in Chao index of the intestinal flora in the ≤7 days group and the >7 days group from week 2 to week 4 (P<0.05). In the ≤7 days group, there were significant increases in the proportions of Firmicutes and Clostridium_sensu_stricto_1 and a significant reduction in the proportion of Proteobacteria from week 2 to week 4 (P<0.05). At week 4, compared with the ≤7 days group, the >7 days group had significant reductions in the proportions of Firmicutes and Clostridium_sensu_stricto_1 and a significant increase in the proportion of Proteobacteria (P<0.05), as well as significant reductions in the content of isobutyric acid and valeric acid (P<0.05). CONCLUSIONS The course of treatment with broad-spectrum antibiotics can affect the abundance, colonization, and evolution of intestinal flora and the content of their metabolites SCFAs in VLBW infants. The indication and treatment course for broad-spectrum antibiotics should be strictly controlled in clinical practice.
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Affiliation(s)
- Qian Sun
- Neonatal Diagnosis and Treatment Center, Children's Hospital of Chongqing Medical University/National Clinical Research Center for Child Health and Disorders/Ministry of Education Key Laboratory of Child Development and Disorders/China International Science and Technology Cooperation Base of Child Development and Critical Disorders/Chongqing Key Laboratory of Pediatrics, Chongqing 400014, China (Li L-Q, )
| | - Zheng-Li Wang
- Neonatal Diagnosis and Treatment Center, Children's Hospital of Chongqing Medical University/National Clinical Research Center for Child Health and Disorders/Ministry of Education Key Laboratory of Child Development and Disorders/China International Science and Technology Cooperation Base of Child Development and Critical Disorders/Chongqing Key Laboratory of Pediatrics, Chongqing 400014, China (Li L-Q, )
| | - Xiao-Chen Liu
- Neonatal Diagnosis and Treatment Center, Children's Hospital of Chongqing Medical University/National Clinical Research Center for Child Health and Disorders/Ministry of Education Key Laboratory of Child Development and Disorders/China International Science and Technology Cooperation Base of Child Development and Critical Disorders/Chongqing Key Laboratory of Pediatrics, Chongqing 400014, China (Li L-Q, )
| | - Yan-Chun Ji
- Neonatal Diagnosis and Treatment Center, Children's Hospital of Chongqing Medical University/National Clinical Research Center for Child Health and Disorders/Ministry of Education Key Laboratory of Child Development and Disorders/China International Science and Technology Cooperation Base of Child Development and Critical Disorders/Chongqing Key Laboratory of Pediatrics, Chongqing 400014, China (Li L-Q, )
| | - Yu He
- Neonatal Diagnosis and Treatment Center, Children's Hospital of Chongqing Medical University/National Clinical Research Center for Child Health and Disorders/Ministry of Education Key Laboratory of Child Development and Disorders/China International Science and Technology Cooperation Base of Child Development and Critical Disorders/Chongqing Key Laboratory of Pediatrics, Chongqing 400014, China (Li L-Q, )
| | - Qing Ai
- Neonatal Diagnosis and Treatment Center, Children's Hospital of Chongqing Medical University/National Clinical Research Center for Child Health and Disorders/Ministry of Education Key Laboratory of Child Development and Disorders/China International Science and Technology Cooperation Base of Child Development and Critical Disorders/Chongqing Key Laboratory of Pediatrics, Chongqing 400014, China (Li L-Q, )
| | - Lu-Quan Li
- Neonatal Diagnosis and Treatment Center, Children's Hospital of Chongqing Medical University/National Clinical Research Center for Child Health and Disorders/Ministry of Education Key Laboratory of Child Development and Disorders/China International Science and Technology Cooperation Base of Child Development and Critical Disorders/Chongqing Key Laboratory of Pediatrics, Chongqing 400014, China (Li L-Q, )
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Alpízar P, Risely A, Tschapka M, Sommer S. Agricultural Fast Food: Bats Feeding in Banana Monocultures Are Heavier but Have Less Diverse Gut Microbiota. Front Ecol Evol 2021. [DOI: 10.3389/fevo.2021.746783] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/23/2022] Open
Abstract
Habitat alteration for agriculture can negatively affect wildlife physiology and health by decreasing diet diversity and increasing exposure to agrochemicals for animals foraging in altered landscapes. Such negative effects may be mediated by the disruption of the gut microbiota (termed dysbiosis), yet evidence for associations between habitat alteration, wildlife health, and the gut microbiota remains scarce. We examine the association between management intensity of banana plantations and both the body condition and gut microbiota composition of nectar-feeding bats Glossophaga soricina, which commonly forage within banana plantations across Latin America. We captured and measured 196 bats across conventional monocultures, organic plantations, and natural forests in Costa Rica, and quantified gut microbiome bacterial phylogenetic diversity using 16S rRNA amplicon sequencing. We found that gut microbiota from bats foraging in conventional monocultures were overall less phylogenetically diverse than those from bats foraging in organic plantations or natural forests, both of which were characterized by diverse bacterial assemblages and individualized microbiota. Despite lower diversity, co-occurrence network complexity was higher in conventional monocultures, potentially indicating altered microbial interactions in agricultural landscapes. Bats from both organic and conventional plantations tended to be larger and heavier than their forest counterparts, reflecting the higher food supply. Overall, our study reveals that whilst both conventional monocultures and organic plantations provide a reliable food source for bats, conventional monocultures are associated with less diverse and potentially dysbiotic microbiota, whilst organic plantations promote diverse and individualized gut microbiota akin to their natural forest-foraging counterparts. Whilst the long-term negative effects of anthropogenically-altered microbiota are unclear, our study provides further evidence from a novel perspective that organic agricultural practices are beneficial for wildlife health.
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21
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Yang Z, Xu F, Li H, He Y. Beyond samples: A metric revealing more connections of gut microbiota between individuals. Comput Struct Biotechnol J 2021; 19:3930-3937. [PMID: 34377361 PMCID: PMC8319210 DOI: 10.1016/j.csbj.2021.07.009] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/05/2021] [Revised: 07/03/2021] [Accepted: 07/07/2021] [Indexed: 10/31/2022] Open
Abstract
Studies of gut microbiota explore their complicated connections between individuals of different characteristics by applying different metrics to abundance data obtained from fecal samples. Although classic metrics are capable to quantify differences between samples, the microbiome of fecal sample is not a good surrogate for the gut microbiome of individuals because the microbial populations of the distal colon does not adequately represent that of the entire gastrointestinal tract. To overcome the deficiency of classic metrics in which the differences can be measured between the samples analyzed, but not the corresponding populations, we propose a metric for representing composition differences in the gut microbiota of individuals. Our investigation shows this metric outperforms traditional measures for multiple scenarios. For gut microbiota in diverse geographic populations, this metric presents more explainable data variance than others, not only in regular variance analysis but also in principle component analysis and partition analysis of biologic characteristics. With time-series data, the metric further presents a strong correlation with the time interval of serial sampling. Our findings suggest that the metric is robust and powerfully detects the intrinsic variations in gut microbiota. The metric holds promise for revealing more relations between gut microbiota and human health.
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Affiliation(s)
- Zhen Yang
- Shanghai Fifth People's Hospital, and Shanghai Key Laboratory of Medical Epigenetics, International Co-laboratory of Medical Epigenetics and Metabolism (Ministry of Science and Technology), Institutes of Biomedical Sciences, Fudan University, Shanghai 200032, China
| | - Feng Xu
- Shanghai Fifth People's Hospital, and Shanghai Key Laboratory of Medical Epigenetics, International Co-laboratory of Medical Epigenetics and Metabolism (Ministry of Science and Technology), Institutes of Biomedical Sciences, Fudan University, Shanghai 200032, China
| | - Hongdou Li
- Obstetrics Gynecology Hospital, The Institute of Reproduction and Developmental Biology, Fudan University, Shanghai, China
| | - Yungang He
- Shanghai Fifth People's Hospital, and Shanghai Key Laboratory of Medical Epigenetics, International Co-laboratory of Medical Epigenetics and Metabolism (Ministry of Science and Technology), Institutes of Biomedical Sciences, Fudan University, Shanghai 200032, China
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