Gut microbiomes of wild great apes fluctuate seasonally in response to diet

Nature Communications

Volumn 9, Issue 1, 2018, Pages

  Hicks, Allison L ^a   Lee, Kerry Jo ^a   Couto Rodriguez, Mara ^a   Patel, Juber ^a   Sinha, Rohini ^a   Guo, Cheng ^a   Olson, Sarah H ^b   Seimon, Anton ^c   Seimon, Tracie A ^a,b   Ondzie, Alain U ^b   Karesh, William B ^b,d   Reed, Patricia ^b   Cameron, Kenneth N ^b   Lipkin, W Ian ^a,e,f   Williams, Brent L ^a,e,f  

^a Columbia University ^*  (United States)

^b WILDLIFE CONSERVATION SOCIETY   (United States)

^c APPALACHIAN STATE UNIVERSITY   (United States)

^d ECOHEALTH ALLIANCE   (United States)

^e Department of Medicine   (United States)

^f New York Presbyterian Columbia University Medical Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCAN; RAIN; RNA 16S;

ADAPTATION; DIET; DIGESTIVE SYSTEM; LOWLAND ENVIRONMENT; MICROORGANISM; NICHE; PRIMATE; PROKARYOTE; SEASONALITY; WILD POPULATION;

APE; ARTICLE; CERCOPITHECIDAE; CHIMPANZEE; CONTROLLED STUDY; DIET; FRUGIVORY; GORILLA GORILLA GORILLA; INTESTINE FLORA; METABOLISM; METAGENOMICS; NONHUMAN; RNA SEQUENCE; SEASONAL VARIATION; SYMPATRY; ANIMAL; ANIMAL FOOD; COMPARATIVE STUDY; FECES; FEMALE; GENETICS; GORILLA GORILLA; HERBIVORY; HUMAN; MALE; MICROBIOLOGY; PAN TROGLODYTES; SEASON; SPECIES DIFFERENCE; VETERINARY MEDICINE;

CERCOPITHECIDAE; GORILLA GORILLA GORILLA; HOMINIDAE; PAN; PRIMATES;

ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; CERCOPITHECIDAE; DIET; FECES; FEMALE; GASTROINTESTINAL MICROBIOME; GORILLA GORILLA; HERBIVORY; HUMANS; MALE; METABOLIC NETWORKS AND PATHWAYS; PAN TROGLODYTES; RNA, RIBOSOMAL, 16S; SEASONS; SPECIES SPECIFICITY;

EID: 85046530729     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-018-04204-w     Document Type: Article

References (80)

1. Smits, S. A. et al. Seasonal cycling in the gut microbiome of the Hadza huntergatherers of Tanzania. Science 357, 802-806 (2017).
2. Doran-Sheehy, D., Mongo, P., Lodwick, J. &Conklin-Brittain, N. L. Male and female western gorilla diet: preferred foods, use of fallback resources, and implications for ape versus old world monkey foraging strategies. Am. J. Phys. Anthropol. 140, 727-738 (2009).
3. Gomez, A. et al. Temporal variation selects for diet-microbe co-metabolic traits in the gut of Gorilla spp. ISME J. 10, 514-526 (2015).
4. Rothman, J. M., Dierenfeld, E. S., Hintz, H. F. &Pell, A. N. Nutritional quality of gorilla diets: consequences of age, sex, and season. Oecologia 155, 111-122 (2008).
5. Gomez, A. et al. Gut microbiome composition and metabolomic profiles of wild western lowland gorillas (Gorilla gorilla gorilla) reflect host ecology. Mol. Ecol. 24, 2551-2565 (2015).
6. Arumugam, M. et al. Enterotypes of the human gut microbiome. Nature 473, 174-180 (2011).
7. Lim, M. Y. et al. Stability of gut enterotypes in Korean monozygotic twins and their association with biomarkers and diet. Sci. Rep. 4, 7348 (2014).
8. Wu, G. D. et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 334, 105-108 (2011).
9. Zhang, J. et al. Mongolians core gut microbiota and its correlation with seasonal dietary changes. Sci. Rep. 4, 5001 (2014).
10. Costea, P. I. et al. Enterotypes in the landscape of gut microbial community composition. Nat. Microbiol. 3, 8-16 (2018).
11. Vieira-Silva, S. et al. Species-function relationships shape ecological properties of the human gut microbiome. Nat. Microbiol. 1, 16088 (2016).
12. Li, J. et al. A metagenomic approach to dissect the genetic composition of enterotypes in Han Chinese and two Muslim groups. Syst. Appl. Microbiol. 41, 1-12 (2017).
13. Moeller, A. H. et al. Chimpanzees and humans harbour compositionally similar gut enterotypes. Nat. Commun. 3, 1179 (2012).
14. Moeller, A. H. et al. Stability of the gorilla microbiome despite simian immunodeficiency virus infection. Mol. Ecol. 24, 690-697 (2015).
15. Ren, T., Grieneisen, L. E., Alberts, S. C., Archie, E. A. &Wu, M. Development, diet and dynamism: longitudinal and cross-sectional predictors of gut microbial communities in wild baboons. Environ. Microbiol. 18, 1312-1325 (2016).
16. Wang, J. et al. Dietary history contributes to enterotype-like clustering and functional metagenomic content in the intestinal microbiome of wild mice. Proc. Natl Acad. Sci. USA 111, E2703-E2710 (2014).
17. Walter, J., Martinez, I. &Rose, D. J. Holobiont nutrition: considering the role of the gastrointestinal microbiota in the health benefits of whole grains. Gut Microbes 4, 340-346 (2013).
18. Zhou, Y. et al. Exploration of bacterial community classes in major human habitats. Genome Biol. 15, R66 (2014).
19. Ley, R. E. et al. Evolution of mammals and their gut microbes. Science 320, 1647-1651 (2008).
20. Yildirim, S. et al. Characterization of the fecal microbiome from non-human wild primates reveals species specific microbial communities. PLoS ONE 5, e13963 (2010).
21. Moeller, A. H. et al. Rapid changes in the gut microbiome during human evolution. Proc. Natl Acad. Sci. USA 111, 16431-16435 (2014).
22. Knights, D. et al. Rethinking "enterotypes". Cell Host Microbe. 16, 433-437 (2014).
23. Jeffery, I. B., Claesson, M. J., O'Toole, P. W. &Shanahan, F. Categorization of the gut microbiota: enterotypes or gradients? Nat. Rev. Microbiol. 10, 591-592 (2012).
24. Roager, H. M., Licht, T. R., Poulsen, S. K., Larsen, T. M. &Bahl, M. I. Microbial enterotypes, inferred by the prevotella-to-bacteroides ratio, remained stable during a 6-month randomized controlled diet intervention with the new nordic diet. Appl. Environ. Microbiol. 80, 1142-1149 (2014).
25. Segata, N. et al. Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60 (2011).
26. Rousvel, S. et al. Comparison between vegetation and rainfall of bioclimatic ecoregions in Central Africa. Atmosphere 4, 411-427 (2013).
27. Morgan, D. &Sanz, C. in Feeding Ecology in Apes and Other Primates 97-122 (Cambridge University Press, New York, 2006).
28. Nishihara, T. Feeding Ecology of Western Lowland Gorillas in the Nouabale-Ndoki National Park, Congo. Primates 36, 151-168 (1995).
29. Doran-Sheehy, D. M., Greer, D., Mongo, P. &Schwindt, D. Impact of ecological and social factors on ranging in western gorillas. Am. J. Primatol. 64, 207-222 (2004).
30. Poulsen, J. R., Clark, C. J. &Smith, T. B. Seasonal variation in the feeding ecology of the grey-cheeked mangabey (Lophocebus albigena) in Cameroon. Am. J. Primatol. 54, 91-105 (2001).
31. Head, J. S., Boesch, C., Makaga, L. &Robbins, M. M. Sympatric chimpanzees (Pan troglodytes troglodytes) and Gorillas (Gorilla gorilla gorilla) in Loango National Park, Gabon: dietary composition, seasonality, and intersite comparisons. Int. J. Primatol. 32, 755-775 (2011).
32. Tutin, C. E. G., Fernandez, M., Rogers, M. E., Williamson, E. A. &Mcgrew, W. C. Foraging profiles of sympatric lowland gorillas and chimpanzees in the lope reserve, gabon. Philos. T. Roy. Soc. B 334, 179-186 (1991).
33. Kuhad, R. C., Singh, A. &Eriksson, K. E. Microorganisms and enzymes involved in the degradation of plant fiber cell walls. Adv. Biochem. Eng. Biotechnol. 57, 45-125 (1997).
34. Koropatkin, N. M., Cameron, E. A. &Martens, E. C. How glycan metabolism shapes the human gut microbiota. Nat. Rev. Microbiol. 10, 323-335 (2012).
35. Desai, M. S. et al. A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell 167, 1339-1353 (2016). e1321.
36. Borrel, G. et al. Unique characteristics of the pyrrolysine system in the 7th order of methanogens: implications for the evolution of a genetic code expansion cassette. Archaea 2014, 374146 (2014).
37. Raymann, K., Moeller, A. H., Goodman, A. L. &Ochman, H. Unexplored archaeal diversity in the great Ape gut microbiome. mSphere 2, e00026-17 (2017).
38. Hoffmann, C. et al. Archaea and fungi of the human gut microbiome: correlations with diet and bacterial residents. PLoS ONE 8, e66019 (2013).
39. Srivathsan, A., Ang, A., Vogler, A. P. &Meier, R. Fecal metagenomics for the simultaneous assessment of diet, parasites, and population genetics of an understudied primate. Front. Zool. 13, 17 (2016).
40. Rogers, M. E. et al. Western gorilla diet: a synthesis from six sites. Am. J. Primatol. 64, 173-192 (2004).
41. Lemmens, R., Louppe, D. &Oteng-Amoako, A. Timbers 2, (PROTA Foundation, Wageningen, Netherlands, 2012).
42. Petre, C. A. et al. Quantity and spatial distribution of seeds dispersed by a western lowland gorilla population in south-east Cameroon. J. Trop. Ecol. 31, 201-212 (2015).
43. Gorvitovskaia, A., Holmes, S. P. &Huse, S. M. Interpreting prevotella and bacteroides as biomarkers of diet and lifestyle. Microbiome 4, 15 (2016).
44. Schnorr, S. L. et al. Gut microbiome of the Hadza hunter-gatherers. Nat. Commun. 5, 3654 (2014).
45. Yatsunenko, T. et al. Human gut microbiome viewed across age and geography. Nature 486, 222-227 (2012).
46. Zeder, M. A. Domestication and early agriculture in the mediterranean basin: origins, diffusion, and impact. Proc. Natl Acad. Sci. USA 105, 11597-11604 (2008).
47. Milton, K. Diet and primate evolution. Sci. Am. 269, 86-93 (1993).
48. Flint, H. J. The rumen microbial ecosystem-some recent developments. Trends Microbiol. 5, 483-488 (1997).
49. Gomez, A. et al. Gut microbiome of coexisting baaka pygmies and bantu reflects gradients of traditional subsistence patterns. Cell Rep. 14, 2142-2153 (2016).
50. Obregon-Tito, A. J. et al. Subsistence strategies in traditional societies distinguish gut microbiomes. Nat. Commun. 6, 6505 (2015).
51. Anton, S. C., Potts, R. &Aiello, L. C. Human evolution. Evolution of early Homo: an integrated biological perspective. Science 345, 1236828 (2014).
52. Brockman, D. &van Schaik, C. Seasonality in Primates: Studies of Living and Extinct Human and Non-human Primates. (Cambridge University Press, New York, 2005).
53. Brucker, R. M. &Bordenstein, S. R. The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus Nasonia. Science 341, 667-669 (2013).
54. Zilber-Rosenberg, I. &Rosenberg, E. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev. 32, 723-735 (2008).
55. Amato, K. R. et al. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J. 7, 1344-1353 (2013).
56. Bermejo, M. et al. Ebola outbreak killed 5000 gorillas. Science 314, 1564 (2006).
57. Rwego, I. B., Isabirye-Basuta, G., Gillespie, T. R. &Goldberg, T. L. Gastrointestinal bacterial transmission among humans, mountain gorillas, and livestock in Bwindi Impenetrable National Park, Uganda. Conserv. Biol. 22, 1600-1607 (2008).
58. Lilly, A., Mehlman, P. &Doran, D. Intestinal parasites in gorillas, chimpanzees, and humans at mondika research site, Dzanga-Ndoki National Park, Central African Republic. Int. J. Primatol. 23, 555-573 (2002).
59. Parnell, R. Information From Animal Tracks and Trail. (Wildlife Conservation Society, New York, 2000).
60. Wroblewski, E. E. et al. Male dominance rank and reproductive success in chimpanzees, Pan troglodytes schweinfurthii. Anim. Behav. 77, 873-885 (2009).
61. Kocher, T. D. et al. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc. Natl Acad. Sci. USA 86, 6196-6200 (1989).
62. Keele, B. F. et al. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313, 523-526 (2006).
63. Valiere, N. GIMLET: a computer program for analysing genetic individual identification data. Mol. Ecol. Notes 2, 377-379 (2002).
64. Villesen, P. &Fredsted, T. Fast and non-invasive PCR sexing of primates: apes, Old World monkeys, New World monkeys and Strepsirrhines. Bmc. Ecol. 6, 8 (2006).
65. The Human Microbiome Project Consortium. A framework for human microbiome research. Nature 486, 215-221 (2012).
66. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461 (2010).
67. Lozupone, C. A. et al. Meta-analyses of studies of the human microbiota. Genome Res. 23, 1704-1714 (2013).
68. Mackenzie, B. W., Waite, D. W. &Taylor, M. W. Evaluating variation in human gut microbiota profiles due to DNA extraction method and intersubject differences. Front. Microbiol. 6, 130 (2015).
69. Rintala, A. et al. Gut microbiota analysis results are highly dependent on the 16S rRNA gene target region, whereas the impact of dna extraction is minor. J. Biomol. Tech. 28, 19-30 (2017).
70. Langmead, B. &Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359 (2012).
71. Schmieder, R. &Edwards, R. Quality control and preprocessing of metagenomic datasets. Bioinformatics 27, 863-864 (2011).
72. Truong, D. T. et al. MetaPhlAn2 for enhanced metagenomic taxonomic profiling. Nat. Methods 12, 902-903 (2015).
73. Srivathsan, A., Sha, J. C., Vogler, A. P. &Meier, R. Comparing the effectiveness of metagenomics and metabarcoding for diet analysis of a leaf-feeding monkey (Pygathrix nemaeus). Mol. Ecol. Resour. 15, 250-261 (2015).
74. Westfall, P. H. &Krishen, A. Optimally weighted, fixed sequence and gatekeeper multiple testing procedures. J. Stat. Plan. Infer. 99, 25-40 (2001).
75. Dmitrienko, A., Offen, W. W. &Westfall, P. H. Gatekeeping strategies for clinical trials that do not require all primary effects to be significant. Stat. Med. 22, 2387-2400 (2003).
76. Koren, O. et al. A guide to enterotypes across the human body: meta-analysis of microbial community structures in human microbiome datasets. PLoS Comput. Biol. 9, e1002863 (2013).
77. Dray, S. &Dufour, A. B. The ade4 package: Implementing the duality diagram for ecologists. J. Stat. Softw. 22, 1-20 (2007).
78. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).
79. Kumar, S., Stecher, G. &Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870-1874 (2016).
80. Letunic, I. &Bork, P. Interactive tree of life (iTOL)v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 44, W242-W245 (2016).