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Methanogenic patterns in the gut microbiome are associated with survival in a population of feral horses.
Abstract: Gut microbiomes are widely hypothesised to influence host fitness and have been experimentally shown to affect host health and phenotypes under laboratory conditions. However, the extent to which they do so in free-living animal populations and the proximate mechanisms involved remain open questions. In this study, using long-term, individual-based life history and shallow shotgun metagenomic sequencing data (2394 fecal samples from 794 individuals collected between 2013-2019), we quantify relationships between gut microbiome variation and survival in a feral population of horses under natural food limitation (Sable Island, Canada), and test metagenome-derived predictions using short-chain fatty acid data. We report detailed evidence that variation in the gut microbiome is associated with a host fitness proxy in nature and outline hypotheses of pathogenesis and methanogenesis as key causal mechanisms which may underlie such patterns in feral horses, and perhaps, wild herbivores more generally.
© 2024. The Author(s).
Publication Date: 2024-07-22 PubMed ID: 39039075PubMed Central: PMC11263349DOI: 10.1038/s41467-024-49963-xGoogle Scholar: Lookup The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
Summary
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The research article discusses the link between variations in the gut microbiome and survival rates in a population of feral horses, suggesting a potential influence of gut microbiota on host health.
Research Background and Methods
- In this study, the researchers aimed to explore and understand the role of gut microbiomes in affecting the host’s fitness. While several lab conditions have shown gut microbiomes influencing host health, the extent of this impact in free-living animal populations remains largely unexplored.
- This study was carried out by analyzing gut microbiome data and individual-based life history from a wild horse population living under natural food limitation on Sable Island, Canada.
- The data utilized in this study included 2394 fecal samples from 794 individual horses collected between 2013 and 2019.
- Through metagenomic sequencing of these fecal samples, the researchers aimed to establish the connection between variations in the gut microbiome and the survival of the horses.
Findings and Interpretation
- The research provided substantial evidence demonstrating that variations in the gut microbiome were indeed associated with the horses’ survival rates, serving as a fitness proxy for the host species in nature.
- These findings validate the hypothesis that gut microbiomes could significantly influence host fitness, even in free-living populations outside the laboratory environment.
- The researchers also suggested that the observed patterns might be underpinned by the processes of pathogenesis and methanogenesis. Methanogenic bacteria in the gut are responsible for the production of methane, an important energy source for herbivorous animals. This of energy-producing bacteria could potentially affect the horses’ survival, particularly under conditions of natural food limitation.
Implications and Future Directions
- These findings could reflect broader dynamics at play in wild herbivores, suggesting possible new avenues of research in understanding species survival and fitness in challenging environments.
- Further investigation is needed to fully confirm the proposed causal mechanisms and extend the findings to other wild herbivore populations.
Cite This Article
APA
Stothart MR, McLoughlin PD, Medill SA, Greuel RJ, Wilson AJ, Poissant J.
(2024).
Methanogenic patterns in the gut microbiome are associated with survival in a population of feral horses.
Nat Commun, 15(1), 6012.
https://doi.org/10.1038/s41467-024-49963-x Publication
Researcher Affiliations
- Faculty of Veterinary Medicine, University of Calgary, Calgary, Alberta, Canada. masonstothart@gmail.com.
- Department of Biology, University of Oxford, Oxford, United Kingdom. masonstothart@gmail.com.
- Department of Biology, University of Saskatchewan, Saskatoon, Saskatchewan, Canada.
- Department of Biology, University of Saskatchewan, Saskatoon, Saskatchewan, Canada.
- Department of Biology, University of Saskatchewan, Saskatoon, Saskatchewan, Canada.
- Centre for Ecology and Conservation, University of Exeter, Penryn, United Kingdom.
- Faculty of Veterinary Medicine, University of Calgary, Calgary, Alberta, Canada. jocelyn.poissant@ucalgary.ca.
MeSH Terms
- Animals
- Horses / microbiology
- Gastrointestinal Microbiome / genetics
- Feces / microbiology
- Methane / metabolism
- Animals, Wild / microbiology
- Metagenome
- Fatty Acids, Volatile / metabolism
- Metagenomics / methods
- Male
- Female
- Canada
Grant Funding
- 2016-06459 / Canadian Network for Research and Innovation in Machining Technology, Natural Sciences and Engineering Research Council of Canada (NSERC Canadian Network for Research and Innovation in Machining Technology)
- 2019-04388 / Canadian Network for Research and Innovation in Machining Technology, Natural Sciences and Engineering Research Council of Canada (NSERC Canadian Network for Research and Innovation in Machining Technology)
- 25046 / Canada Foundation for Innovation (Fondation canadienne pour l'innovation)
- D20EQ-05 / Morris Animal Foundation (MAF)
- D20EQ-05 / Morris Animal Foundation (MAF)
- D20EQ-05 / Morris Animal Foundation (MAF)
Conflict of Interest Statement
The authors declare no competing interests.
References
This article includes 92 references
- Lynch JB, Hsiao EY. Microbiomes as sources of emergent host phenotypes. Science 365, 1405–1409 (2019).
- Kohl KD, Carey HV. A place for host-microbe symbiosis in the comparative physiologist’s toolbox. J. Exp. Biol. 219, 3496–3504 (2016).
- Alberdi A, Aizpurua O, Bohmann K, Zepeda-Mendoza ML, Gilbert MTP. Do vertebrate gut metagenomes confer rapid ecological adaptation?. Trends Ecol. Evol. 31, 689–699 (2016).
- Zaneveld JR, McMinds R, Vega Thurber R. Stress and stability: Applying the Anna Karenina principle to animal microbiomes. Nat. Microbiol 2, 1–8 (2017).
- Henry LP, Bruijning M, Forsberg SKG, Ayroles JF. The microbiome extends host evolutionary potential. Nat. Commun. 12, 1–13 (2021).
- Rosenberg E, Zilber-Rosenberg I. The hologenome concept of evolution after 10 years. Microbiome 6, 1–14 (2018).
- Ryu EP, Davenport ER. Host genetic determinants of the microbiome across animals: From Caenorhabditis elegans to cattle. Annu Rev. Anim. Biosci. 10, 203–226 (2022).
- Grieneisen L et al. Gut microbiome heritability is nearly universal but environmentally contingent. Science 373, 181–186 (2021).
- Suzuki TA. Links between natural variation in the microbiome and host fitness in wild mammals. Integr. Comp. Biol. 57, 756–769 (2017).
- Gould AL et al. Microbiome interactions shape host fitness. Proc. Natl. Acad. Sci. USA 115, 11951–11960 (2018).
- Kohl KD, Weiss RB, Cox J, Dale C, Denise Dearing M. Gut microbes of mammalian herbivores facilitate intake of plant toxins. Ecol. Lett. 17, 1238–1246 (2014).
- Worsley SF et al. Gut microbiome composition, not alpha diversity, is associated with survival in a natural vertebrate population. Anim. Microbiome 3, 1–18 (2021).
- Risely A et al. Climate change drives loss of bacterial gut mutualists at the expense of host survival in wild meerkats. Glob. Chang Biol. 29, 1–13 (2023).
- Hammer TJ, Sanders JG, Fierer N. Not all animals need a microbiome. FEMS Microbiol Lett. 366, 1–11 (2019).
- Costa MC et al. Characterization and comparison of the bacterial microbiota in different gastrointestinal tract compartments in horses. Vet. J. 205, 74–80 (2015).
- Stothart MR, McLoughlin PD, Poissant J. Shallow shotgun sequencing of the microbiome recapitulates 16S amplicon results and provides functional insights. Mol. Ecol. Resour. 23, 549–564 (2023).
- Lindenberg F et al. Development of the equine gut microbiota. Sci. Rep. 9, 1–9 (2019).
- Shade A. Diversity is the question, not the answer. ISME J. 11, 1–6 (2017).
- Reese AT, Dunn RR. Drivers of microbiome biodiversity: a review of general rules, feces, and ignorance. mBio 9, 1–14 (2018).
- Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57, 289–300 (1995).
- Paterson GK, Mitchell TJ. The biology of Gram-positive sortase enzymes. Trends Microbiol 12, 89–95 (2004).
- Vázquez-Torres A, Bäumler AJ. Nitrate, nitrite and nitric oxide reductases: From the last universal common ancestor to modern bacterial pathogens. Curr. Opin. Microbiol 29, 1–8 (2016).
- Mohapatra NP et al. Combined deletion of four Francisella novicida acid phosphatases attenuates virulence and macrophage vacuolar escape. Infect. Immun. 76, 3690–3699 (2008).
- Holter JB, Young AJ. Methane prediction in dry and lactating holstein cows. J. Dairy Sci. 75, 2165–2175 (1992).
- Johnson KA, Johnson DE. Methane emissions from cattle. J. Anim. Sci. 73, 2483–2492 (1995).
- Clauss M et al. Comparative methane production in mammalian herbivores. Animal 14, 113–123 (2020).
- Jenkins E et al. Not playing by the rules: Unusual patterns in the epidemiology of parasites in a natural population of feral horses (Equus caballus) on Sable Island, Canada. Int J. Parasitol. Parasites Wildl. 11, 183–190 (2020).
- Pereira AM, de Lurdes Nunes Enes Dapkevicius M, Borba AES. Alternative pathways for hydrogen sink originated from the ruminal fermentation of carbohydrates: Which microorganisms are involved in lowering methane emission?. Anim. Microbiome 4, 1–12 (2022).
- Tapio I, Snelling TJ, Strozzi F, Wallace RJ. The ruminal microbiome associated with methane emissions from ruminant livestock. J. Anim. Sci. Biotechnol. 8, 1–11 (2017).
- Wallace RJ et al. The rumen microbial metagenome associated with high methane production in cattle. BMC Genomics 16, 1–14 (2015).
- Ruaud A et al. Syntrophy via interspecies H2 transfer between Christensenella and Methanobrevibacter underlies their global cooccurrence in the human gut. mBio 11, 1–16 (2020).
- Kamke J et al. Rumen metagenome and metatranscriptome analyses of low methane yield sheep reveals a Sharpea-enriched microbiome characterised by lactic acid formation and utilisation. Microbiome 4, 1–16 (2016).
- Ungerfeld EM. Metabolic hydrogen flows in rumen fermentation: principles and possibilities of interventions. Front Microbiol 11, 1–21 (2020).
- Foti M et al. Diversity, activity, and abundance of sulfate-reducing bacteria in saline and hypersaline soda lakes. Appl. Environ. Microbiol 73, 2093–2100 (2007).
- Kojima H, Fukui M. Sulfuricella denitrificans gen. nov., sp. nov., a sulfur-oxidizing autotroph isolated from a freshwater lake. Int J. Syst. Evol. Microbiol 60, 2862–2866 (2010).
- Yoon J, Maharjan S, Choi H. Polyphasic taxonomic analysis of Paracoccus ravus sp. nov., an Alphaproteobacterium isolated from marine sediment. FEMS Microbiol Lett. 366, 1–6 (2019).
- Gibson GR, Cummings JH, Macfarlane GT. Use of a three-stage continuous culture system to study the effect of mucin on dissimilatory sulfate reduction and methanogenesis by mixed populations of human gut bacteria. Appl. Environ. Microbiol 54, 2750–2755 (1988).
- Rey FE et al. Metabolic niche of a prominent sulfate-reducing human gut bacterium. Proc. Natl. Acad. Sci. USA 110, 13582–13587 (2013).
- De Luca G, De Philip P, Rousset M, Belaich JP, Dermoun Z. The NADP-reducing hydrogenase of Desulfovibrio fructosovorans: evidence for a native complex with hydrogen-dependent methyl-viologen-reducing activity. Biochem. Biophys. Res. Commun. 248, 591–596 (1998).
- Pereira FC et al. Rational design of a microbial consortium of mucosal sugar utilizers reduces Clostridiodes difficile colonization. Nat. Commun. 11, 1–15 (2020).
- Reichardt N et al. Phylogenetic distribution of three pathways for propionate production within the human gut microbiota. ISME J. 8, 1323–1335 (2014).
- Louis P, Flint HJ. Formation of propionate and butyrate by the human colonic microbiota. Environ. Microbiol 19, 29–41 (2017).
- Neumann AP, Suen G. The phylogenomic diversity of herbivore-associated Fibrobacter spp. is correlated to lignocellulose-degrading potential. mSphere 3, 1–18 (2018).
- Asanuma N, Iwamoto M, Hino T. Effect of the addition of fumarate on methane production by ruminal microorganisms in vitro. J. Dairy Sci. 82, 780–787 (1999).
- Stewart RD et al. Compendium of 4,941 rumen metagenome-assembled genomes for rumen microbiome biology and enzyme discovery. Nat. Biotechnol. 37, 953–961 (2019).
- Chaucheyras-Durand F, Masséglia S, Fonty G, Forano E. Influence of the composition of the cellulolytic flora on the development of hydrogenotrophic microorganisms, hydrogen utilization, and methane production in the rumens of gnotobiotically reared lambs. Appl Environ. Microbiol 76, 7931–7937 (2010).
- Yeoman CJ et al. In Vivo competitions between Fibrobacter succinogenes, Ruminococcus flavefaciens, and Ruminoccus albus in a gnotobiotic sheep model revealed by multi-omic analyses. mBio 12, 1–16 (2021).
- Janssen PH. Influence of hydrogen on rumen methane formation and fermentation balances through microbial growth kinetics and fermentation thermodynamics. Anim. Feed Sci. Technol. 160, 1–22 (2010).
- Regan MD et al. Nitrogen recycling via gut symbionts increases in ground squirrels over the hibernation season. Science 375, 460–463 (2022).
- Zhang X et al. Widespread protein lysine acetylation in gut microbiome and its alterations in patients with Crohn’s disease. Nat. Commun. 11, 1–12 (2020).
- Latorre-Muro P et al. Dynamic acetylation of phosphoenolpyruvate carboxykinase toggles enzyme activity between gluconeogenic and anaplerotic reactions. Mol. Cell 71, 718–732 (2018).
- Banerjee R, Jones JC, Lipscomb JD. Soluble methane monooxygenase. Annu Rev. Biochem 88, 409–431 (2019).
- Froy H et al. Senescence in immunity against helminth parasites predicts adult mortality in a wild mammal. Science 365, 1296–1298 (2019).
- Oliphant K, Allen-Vercoe E. Macronutrient metabolism by the human gut microbiome: Major fermentation by-products and their impact on host health. Microbiome 7, 1–15 (2019).
- Seherf U, Siihling B, Gottsehalk G, Linder D, Gang Buckel W. Succinate-ethanolfermentation in Clostridium kluyveri: Purification and characterisation of4-hydroxybutyryl-CoA dehydratase[vinylacetyl-CoA A 3-A 2-isomerase. Arch Microbiol 161, 239–245 (1994).
- Borrel G et al. Genome sequence of ‘candidatus Methanomethylophilus alvus’ Mx1201, a methanogenic archaeon from the human gut belonging to a seventh order of methanogens. J. Bacteriol. 194, 6940–6941 (2012).
- Newbold CJ, de la Fuente G, Belanche A, Ramos-Morales E, McEwan NR. The role of ciliate protozoa in the rumen. Front Microbiol 6, 1–14 (2015).
- Finlay BJ et al. Some rumen ciliates have endosymbiotic methanogens. FEMS Microbiol Lett. 117, 157–161 (1994).
- Gacesa R et al. Environmental factors shaping the gut microbiome in a Dutch population. Nature 604, 732–739 (2022).
- Bisanz JE, Upadhyay V, Turnbaugh JA, Ly K, Turnbaugh PJ. Meta-analysis reveals reproducible gut microbiome alterations in response to a high-fat diet. Cell Host Microbe 26, 265–272 (2019).
- Knowles SCL, Eccles RM, Baltrūnaitė L. Species identity dominates over environment in shaping the microbiota of small mammals. Ecol. Lett. 22, 1–12 (2019).
- Difford GF et al. Host genetics and the rumen microbiome jointly associate with methane emissions in dairy cows. PLoS Genet 14, 1–22 (2018).
- Waters JL, Ley RE. The human gut bacteria Christensenellaceae are widespread, heritable, and associated with health. BMC Biol. 17, 1–11 (2019).
- Li F et al. Host genetics influence the rumen microbiota and heritable rumen microbial features associate with feed efficiency in cattle. Microbiome 7, 1–17 (2019).
- Roche KE et al. Universal gut microbial relationships in the gut microbiome of wild baboons. Elife 12, 11–27 (2023).
- Björk JR et al. Synchrony and idiosyncrasy in the gut microbiome of wild baboons. Nat. Ecol. Evol. 6, 955–964 (2022).
- Dohm MR. Repeatability estimates do not always set an upper limit to heritability. Funct. Ecol. 16, 273–280 (2002).
- Greyson-Gaito CJ et al. Into the wild: Microbiome transplant studies need broader ecological reality. Proc. R. Soc. B: Biol. Sci. 287, 1–9 (2020).
- Cabrera D et al. Island tameness and the repeatability of flight initiation distance in a large herbivore. Can. J. Zool. 95, 771–778 (2017).
- Gavriliuc S, Stothart MR, Henry A, Poissant J. Long-term storage of feces at −80 °C versus −20 °C is negligible for 16S rRNA amplicon profiling of the equine bacterial microbiome. PeerJ 9, 1–16 (2021).
- Kalbfleisch TS et al. Improved reference genome for the domestic horse increases assembly contiguity and composition. Commun. Biol. 1, 1–8 (2018).
- Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
- Beghini F et al. Integrating taxonomic, functional, and strain-level profiling of diverse microbial communities with biobakery 3. elife 10, 1–42 (2021).
- Bolger AM, Lohse M, Usadel B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
- Menzel P, Ng KL, Krogh A. Fast and sensitive taxonomic classification for metagenomics with Kaiju. Nat. Commun. 7, 1–9 (2016).
- Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59–60 (2014).
- Caspi R et al. The MetaCyc database of metabolic pathways and enzymes-a 2019 update. Nucleic Acids Res. 48, 445–453 (2019).
- Tovo A, Menzel P, Krogh A, Lagomarsino MC, Suweis S. Taxonomic classification method for metagenomics based on core protein families with Core-Kaiju. Nucleic Acids Res 48, 1–13 (2020).
- Hillmann B et al. Evaluating the information content of shallow shotgun metagenomics. mSystems 3, 1–12 (2018).
- Zhao G, Nyman M, Jönsson JÅ. Rapid determination of short-chain fatty acids in colonic contents and faeces of humans and rats by acidified water-extraction and direct-injection gas chromatography. Biomed. Chromatogr. 20, 674–682 (2006).
- McMurdie PJ, Holmes S. phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8, 1–11 (2013).
- Bates D, Mächler M, Bolker BM, Walker SC. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
- Richard E, Simpson SE, Medill SA, Mcloughlin PD. Interacting effects of age, density, and weather on survival and current reproduction for a large mammal. Ecol. Evol. 4, 3851–3860 (2014).
- Contasti AL, Tissier EJ, Johnstone JF, McLoughlin PD. Explaining spatial heterogeneity in population dynamics and genetics from spatial variation in resources for a large herbivore. PLoS One 7, 1–8 (2012).
- Regan CE, Medill SA, Poissant J, McLoughlin PD. Causes and consequences of an unusually male-biased adult sex ratio in an unmanaged feral horse population. J. Anim. Ecol. 89, 2909–2921 (2020).
- Thorsen J et al. Large-scale benchmarking reveals false discoveries and count transformation sensitivity in 16S rRNA gene amplicon data analysis methods used in microbiome studies. Microbiome 4, 1–14 (2016).
- Butler DG, Cullis BR, Gilmour AR, Gogel BG, Thompson R. ASReml-R Reference Manual Version 4.2. .
- Stothart MR et al. Bacterial dispersal and drift drive microbiome diversity patterns within a population of feral hindgut fermenters. Mol. Ecol. 30, 555–571 (2021).
- Taberlet P et al. Power and limitations of the chloroplast trnL (UAA) intron for plant DNA barcoding. Nucleic Acids Res. 35, 1–8 (2007).
- Callahan BJ et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).
- Poissant J et al. A repeatable and quantitative DNA metabarcoding assay to characterize mixed strongyle infections in horses. Int. J. Parasitol. 51, 183–192 (2021).
- Wang Q, Garrity GM, Tiedje JM, Cole JR. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ. Microbiol 73, 5261–5267 (2007).
Citations
This article has been cited 9 times.- Zhang C, Wang X, Wang L, Li P, Bao Y, Zhang Z, Jiang Z, Feng C, Chen L. Multi-omics reveals gut microbiota-mediated environmental adaptation in Mallards and domesticated Shaoxing ducks. Poult Sci 2026 Jan;105(1):106177.
- Schank N, Cottone A, Wulf M, Seiter K, Thomas B, Miller LMJ, Anderson SL, Sahyoun A, Abidi AH, Kassan M, Verma A. The Role of Short-Chain Fatty Acids (SCFAs) in Colic and Anti-Inflammatory Pathways in Horses. Animals (Basel) 2025 Dec 3;15(23).
- Daniels S, Martin S, Harris P, Moore-Colyer M. Using culture 'omics to explore the microbial structure and function in an equid in vitro digestion model. Sci Rep 2025 Dec 1;16(1):455.
- Li F, Kong X, Khan MZ, Wei L, Wei J, Zhu M, Liu G, Huang B, Wang C, Zhang Z. Gut microbiome regulation in equine animals: current understanding and future perspectives. Front Microbiol 2025;16:1602258.
- Łopucki R, Sajnaga E, Ożga K, Stępień-Pyśniak D, Jastrzębski A, Świątek M, Kloch M, Sadok I, Nasiadka P, Kjellander P, Klich D. Bacterial indicators of environmental stress in the gut microbiome of free-ranging European roe deer inhabiting agricultural landscapes. Sci Rep 2025 Aug 7;15(1):28876.
- Kamenova S, Albon SD, Loe LE, Irvine RJ, Langvatn R, Gusarova G, de Muinck EJ, Trosvik P. Arctic Greening Drives Changes in the Diet and Gut Microbiome of a Large Herbivore With Consequences for Body Mass. Ecol Evol 2025 Jul;15(7):e71731.
- Ghaddar BC, Blaser MJ, De S. Revisiting the cancer microbiome using PRISM. bioRxiv 2025 Jan 24;.
- Stothart MR, Lavergne S, McCaw L, Singh H, de Vega W, Amato K, Poissant J, Boonstra R. Population Dynamics and the Microbiome in a Wild Boreal Mammal: The Snowshoe Hare Cycle and Impacts of Diet, Season and Predation Risk. Mol Ecol 2025 Feb;34(3):e17629.
- Brandi LA, Nunes AT, Faleiros CA, Poleti MD, Oliveira ECM, Schmidt NT, Sousa RLM, Fukumasu H, Balieiro JCC, Brandi RA. Dietary Energy Sources Affect Cecal and Fecal Microbiota of Healthy Horses. Animals (Basel) 2024 Dec 3;14(23).
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