Original Article

The ISME Journal (2016) 10, 514–526; doi:10.1038/ismej.2015.146; published online 28 August 2015

There is a Corrigendum (19 January 2016) associated with this article.

Temporal variation selects for diet–microbe co-metabolic traits in the gut of Gorilla spp

Andres Gomez1,2, Jessica M Rothman3,4, Klara Petrzelkova5,6,7, Carl J Yeoman8, Klara Vlckova9, Juan D Umaña1, Monica Carr1, David Modry6,9,10, Angelique Todd11, Manolito Torralba12, Karen E Nelson12, Rebecca M Stumpf1,13, Brenda A Wilson1,14, Ran Blekhman15,16, Bryan A White1,2 and Steven R Leigh1,13,17

  1. 1Department of Animal Sciences, Institute for Genomic Biology, University of Illinois at Urbana–Champaign, Champaign, IL, USA
  2. 2Department of Animal Sciences, University of Illinois at Urbana–Champaign, Champaign, IL, USA
  3. 3Department of Anthropology, Hunter College of CUNY, New York, NY, USA
  4. 4New York Consortium in Evolutionary Primatology (NYCEP), New York, NY, USA
  5. 5Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Brno, Czech Republic
  6. 6Biology Centre, Institute of Parasitology, Academy of Sciences of the Czech Republic, Ceske Budejovice, Czech Republic
  7. 7Liberec Zoo, Liberec, Czech Republic
  8. 8Department of Animal and Range Sciences, Montana State University, Bozeman, MT, USA
  9. 9Department of Pathology and Parasitology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences Brno, Czech Republic
  10. 10CEITEC, Central European Institute for Technology, Brno, Czech Republic
  11. 11World Wildlife Fund, Dzanga-Sangha Protected Areas, Bayanga, Central African Republic
  12. 12J. Craig Venter Institute, Rockville, MD, USA
  13. 13Department of Anthropology, University of Illinois at Urbana–Champaign, Champaign, IL, USA
  14. 14Department of Microbiology, University of Illinois at Urbana–Champaign, Champaign, IL, USA
  15. 15Department of Genetics, Cell Biology and Development, University of Minnesota Twin Cities, St Paul, MN, USA
  16. 16Department of Ecology, Evolution and Behavior, University of Minnesota Twin Cities, St Paul, MN, USA
  17. 17Department of Anthropology, University of Colorado, Boulder, CO, USA

Correspondence: A Gomez, Department of Genetics, Cell Biology and Development and Department of Ecology, Evolution and Behavior, University of Minnesota Twin Cities, St Paul 55108, USA. E-mail: gomeza@umn.edu

Received 4 February 2015; Revised 7 July 2015; Accepted 14 July 2015
Advance online publication 28 August 2015

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Abstract

Although the critical role that our gastrointestinal microbes play in host physiology is now well established, we know little about the factors that influenced the evolution of primate gut microbiomes. To further understand current gut microbiome configurations and diet–microbe co-metabolic fingerprints in primates, from an evolutionary perspective, we characterized fecal bacterial communities and metabolomic profiles in 228 fecal samples of lowland and mountain gorillas (G. g. gorilla and G. b. beringei, respectively), our closest evolutionary relatives after chimpanzees. Our results demonstrate that the gut microbiomes and metabolomes of these two species exhibit significantly different patterns. This is supported by increased abundance of metabolites and bacterial taxa associated with fiber metabolism in mountain gorillas, and enrichment of markers associated with simple sugar, lipid and sterol turnover in the lowland species. However, longitudinal sampling shows that both species’ microbiomes and metabolomes converge when hosts face similar dietary constraints, associated with low fruit availability in their habitats. By showing differences and convergence of diet–microbe co-metabolic fingerprints in two geographically isolated primate species, under specific dietary stimuli, we suggest that dietary constraints triggered during their adaptive radiation were potential factors behind the species-specific microbiome patterns observed in primates today.