Abstract
Over the past decade several studies have reported that the gut microbiomes of mammals with similar dietary niches exhibit similar compositional and functional traits. However, these studies rely heavily on samples from captive individuals and often confound host phylogeny, gut morphology, and diet. To more explicitly test the influence of host dietary niche on the mammalian gut microbiome we use 16S rRNA gene amplicon sequencing and shotgun metagenomics to compare the gut microbiota of 18 species of wild non-human primates classified as either folivores or closely related non-folivores, evenly distributed throughout the primate order and representing a range of gut morphological specializations. While folivory results in some convergent microbial traits, collectively we show that the influence of host phylogeny on both gut microbial composition and function is much stronger than that of host dietary niche. This pattern does not result from differences in host geographic location or actual dietary intake at the time of sampling, but instead appears to result from differences in host physiology. These findings indicate that mammalian gut microbiome plasticity in response to dietary shifts over both the lifespan of an individual host and the evolutionary history of a given host species is constrained by host physiological evolution. Therefore, the gut microbiome cannot be considered separately from host physiology when describing host nutritional strategies and the emergence of host dietary niches.
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References
Delsuc F, Metcalf JL, Parfrey LW, Song SJ, Gonzalez A, Knight R. Convergence of gut microbiomes in myrmecophagous mammals. Mol Ecol. 2014;23:1301–17.
Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, et al. Evolution of mammals and their gut microbes. Science. 2008;320:1647–51.
Muegge BD, Kuczynski J, Knights D, Clemente JC, Gonzalez A, Fontana L, et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science. 2011;332:970–4.
David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–66.
Amato KR, Leigh SR, Kent A, Mackie RI, Yeoman CJ, Stumpf RM, et al. The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra). Microb Ecol. 2015;69:434–43.
Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science. 2011;334:105–8.
Kohl KD, Weiss RB, Cox J, Dale C, Dearing MD. Gut microbes of mammalian herbivores facilitate intake of plant toxins. Ecol Lett. 2014b;17:1238–46.
Scharf ME, Karl ZJ, Sethi A, Boucias DG. Multiple levels of synergistic collaboration in termite lignocellulose digestion. PLoS ONE. 2011;6:e21709.
Amato KR, Yeoman CJ, Kent A, Carbonero F, Righini N, Estrada AE, et al. Habitat degradation impacts primate gastrointestinal microbiomes. ISME J. 2013;7:1344–53.
Clayton JB, Vangay P, Huan H, Ward T, Hillmann BM, Al-Ghalith GA, et al. Captivity humanizes the primate microbiome. Proc Natl Acad Sci USA. 2016;113:10376–81.
Kohl KD, Skopec MM, Dearing MD. Captivity results in disparate loss of gut microbial diversity in closely related hosts. Conserv Physiol. 2014a;2:cou009.
Sanders JG, Beichman AC, Roman J, Scott JJ, Emerson D, McCarthy JJ, et al. Baleen whales host a unique gut microbiome with similarities to both carnivores and herbivores. Nat Commun. 2015;6:8285.
Moeller AH, Caro-Quintero A, Mjungu D, Georgiev AV, Lonsdorf EV, Muller MN, et al. Cospeciation of gut microbiota with hominids. Science. 2016;353:380–2.
Ochman H, Worobey M, Kuo CH, Ndjango JBN, Peeters M, Hahn BH, et al. Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol. 2010;8:e1000546.
Brooks AW, Kohl KD, Brucker RM, van Opstal EJ, Bordenstein SR. Phylosymbiosis: relationships and functional effects of microbial communities across host evolutionary history. PLoS Biol. 2016;14:e2000225.
Nishida A, Ochman H. Rates of gut microbiome divergence in mammals. Mol Ecol. 2018;27:1884–97.
Lambert JE. Primate nutritional ecology: feeding biology and diet at ecological and evolutionary scales. In: Campbell C, Fuentes A, MacKinnon KC, Panger M, Bearder SK, (eds). Primates in Perspective. Second edition. New York: Oxford University Press; 2011. p. 512–22. edn
Gomez A, Rothman JM, Petrzelkova KJ, Yeoman CJ, Vlckova K, Umana JD, et al. Temporal variation selects for diet-microbe co-metabolic traits in the gut of Gorilla spp. ISME J. 2016;10:514–26.
Thompson LR, Sanders JG, McDonald D, Amir A, Ladau J, Locey KJ, et al. A communal catalogue reveals Earth’s multiscale microbial diversity. Nat Biotech. 2017;551:457–63.
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;6:1621–4.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010b;7:335–6.
Kopylova E, Noe L, Touzet H. SortMeRNA: Fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics. 2012;28:3211–7.
Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics. 2010a;26:266–7.
Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–1.
DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72:5069–72.
Price MN, Dehal PS, Arkin AP. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE. 2010;5:e9490.
Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, et al. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods. 2013;10:57–59.
Amir A, McDonald D, Navas-Molina JA, Kopylova E, Morton JT, Xu ZZ, et al. Deblur rapidly resolves single-nucleotide community sequence patterns. mSystems. 2017;2:e00191–00116.
Mirarab S, Nguyen N, Warnow T. SEPP: SAT-enabled phylogenetic placement. Pac Symp Biocomput. 2012;247–58.
Vazquez-Baeza Y, Pirrung M, Gonzalez A, Knight R. Emperor: a tool for visualizing high-throughput microbial community data. Gigascience. 2013;2:16.
Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol. 2005;71:8228–35.
Faith DP. Conservation evaluation and phylogenetic diversity. Biol Conserv. 1992;61:1–10.
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60.
Morton JT, Sanders J, Quinn RA, McDonald D, Gonzalez A, Vazquez-Baeza Y, et al. Balance trees reveal microbial niche differentiation. mSystems. 2017;2:e00162–00116.
Friedman J, Alm EJ. Inferring correlation networks from genomic survey data. PLoS Comput Biol. 2012;8:e1002687.
Egozcue JJ, Pawlowsky-Glahn V. Groups of parts and their balances in compositional data analysis. Math Geol. 2005;37:795.
Amato KR, Martinez-Mota R, Righini N, Raguet-Schofield ML, Corcione FP, Marini E, et al. Phylogenetic and ecological factors impact the gut microbiota of Neotropical primate species. Oecologia. 2016a;180:717–33.
Amato KR, Metcalf JL, Song SJ, Hale VL, Clayton JB, Ackermann G, et al. Using the gut microbiota as a novel tool for examining colobine primate GI health. Glob Ecol Conserv. 2016b;7:225–37.
Sanders JG, Powell S, Kronauer DJC, Vasconcelos HL, Fredrickson ME, Pierce NE. Stability and phylgenetic correlation in gut microbiota: lessons from ants and apes. Mol Ecol. 2014;23:1268–83.
Hommola K, Smith JE, Qiu Y, Gilks WR. A permutation test of host-parasite co-speciation. Mol Biol Evol. 2009;26:1457–68.
Koster J, Rahmann S. Snakemake- a scalable bioinformatics workflow engine. Bioinformatics. 2012;28:2520–2.
Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–7.
Yin Y, Mao X, Yang JC, Chen X, Mao F, Xu Y. dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 2012;40:W445–451.
Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014;42:D490–D495.
Cantarel BL, Lombard V, Henrissat B. Complex carbohydrate utilization by the healthy human microbiome. PLoS ONE. 2012;7:e28742.
Davenport ER, Sanders JG, Song SJ, Amato KR, Clark AG, Knight R. The human microbiome in evolution. BMC Biol. 2017;15:127.
Groussin M, Mazel F, Sanders JG, Smillie CS, Lavergne S, Thuiller W, et al. Unraveling the processes shaping mammalian gut microbiomes over evolutionary time. Nat Commun. 2017;8:14319.
Perelman P, Johnson WE, Roos C, Seuanez HN, Horvath JE, Moreira MAM, et al. A molecular phylogeny of living primates. PLoS Genet. 2011;7:e1001342.
National Research Council. Nutrient Requirements of Nonhuman Primates: Second Revised Edition, Second edn. Washington, D.C: The National Academies Press; 2003.
Dill-McFarland KA, Weimer PJ, Pauli JN, Peery MZ, Suen G. Diet specialization selects for an unusual and simplified gut microbiota in two- and three-toed sloths. Environ Microbiol. 2016;18:1391–402.
Nelson TM, Rogers TL, Carlini AR, Brown MV. Diet and phylogeny shape the gut microbiota of Antarctic seals: a comparison of wild and captive animals. Environ Microbiol. 2012;15:1132–45.
Smits SA, Leach J, Sonnenburg ED, Gonzalez CG, Lichtman JS, Reid G, et al. Seasonal cycling in the gut microbiome of the Hadza hunter-gatherers of Tanzania. Science. 2017;357:802–6.
Sonnenburg ED, Smits SA, Tikhonov M, Higginbottom SK, Wingreen NS, Sonnenburg JL. Diet-induced extinctions in the gut microbiota compound over generations. Nature. 2016;529:212–5.
Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon HA. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med. 2009;1:6ra14.
Williams CL, Willard S, Kouba A, Sparks D, Holmes W, Falcone J, et al. Dietary shifts affect the gastrointestinal microflora of the giant panda (Ailuropoda melanoleuca). J Anim Physiol Anim Nutr. 2012;97:577–85.
Zhang J, Guo Z, Lim AAQ, Zheng Y, Koh EY, Ho D, et al. Mongolians core gut microbiota and its correlation with seasonal dietary changes. Sci Rep. 2014;4:5001.
Acknowledgements
This project was funded by the NSF (HOMINID, grant #0935347), the Earth Microbiome Project (W.M. Keck Foundation DT061413), and the John Templeton Foundation (Grant ID 44000, Convergent Evolution of the Vertebrate Microbiome). Field collection of samples was funded through a variety of individual grants awarded to the co-authors and collaborators listed in Table S1. The authors are grateful for the support with logistics and permits provided by the US government, as well as the governments and local agencies associated with each nation listed in Table S1, as well as countless field assistants at these locations. Raw sequence data generated by 16S rRNA amplicon sequencing and shotgun metagenomics are located in EBI under accession ERP104379.
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Amato, K.R., G. Sanders, J., Song, S.J. et al. Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes. ISME J 13, 576–587 (2019). https://doi.org/10.1038/s41396-018-0175-0
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DOI: https://doi.org/10.1038/s41396-018-0175-0
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