Original Article

The ISME Journal (2014) 8, 2431–2444; doi:10.1038/ismej.2014.90; published online 18 July 2014

Primate vaginal microbiomes exhibit species specificity without universal Lactobacillus dominance

Suleyman Yildirim1,6, Carl J Yeoman1,7, Sarath Chandra Janga1,8, Susan M Thomas1, Mengfei Ho1,2, Steven R Leigh1,3,9, Primate Microbiome Consortium5, Bryan A White1,4, Brenda A Wilson1,2 and Rebecca M Stumpf1,3

  1. 1The Institute for Genomic Biology, University of Illinois, Urbana, IL, USA
  2. 2Department of Microbiology, University of Illinois, Urbana, IL, USA
  3. 3Department of Anthropology, University of Illinois, Urbana, IL, USA
  4. 4Department of Animal Sciences, University of Illinois, Urbana, IL, USA

Correspondence: BA Wilson or RM Stumpf, Department of Microbiology, University of Illinois, Urbana, IL 61801, USADepartment of Anthropology, University of Illinois, 1206 W. Gregory Drive, Urbana, IL 61801, USA. E-mail: bawilson@life.illinois.edu or rstumpf@illinois.edu

5Primate Microbiome Consortium are listed before the references.

6Current address: Department of Medical Microbiology, Istanbul Medipol University School of Medicine, Beykoz, Istanbul 34810, Turkey.

7Current address: Department of Animal and Range Sciences, Montana State University, Bozeman, MT 59717, USA.

8Current address: School of Informatics and Computing, Indiana University-Purdue University Indianapolis, Indianapolis, IN 46202, USA.

9Current address: Department of Anthropology, University of Colorado–Boulder, Boulder, CO 80309, USA.

Received 14 November 2013; Revised 12 April 2014; Accepted 28 April 2014
Advance online publication 18 July 2014

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Abstract

Bacterial communities colonizing the reproductive tracts of primates (including humans) impact the health, survival and fitness of the host, and thereby the evolution of the host species. Despite their importance, we currently have a poor understanding of primate microbiomes. The composition and structure of microbial communities vary considerably depending on the host and environmental factors. We conducted comparative analyses of the primate vaginal microbiome using pyrosequencing of the 16S rRNA genes of a phylogenetically broad range of primates to test for factors affecting the diversity of primate vaginal ecosystems. The nine primate species included: humans (Homo sapiens), yellow baboons (Papio cynocephalus), olive baboons (Papio anubis), lemurs (Propithecus diadema), howler monkeys (Alouatta pigra), red colobus (Piliocolobus rufomitratus), vervets (Chlorocebus aethiops), mangabeys (Cercocebus atys) and chimpanzees (Pan troglodytes). Our results indicated that all primates exhibited host-specific vaginal microbiota and that humans were distinct from other primates in both microbiome composition and diversity. In contrast to the gut microbiome, the vaginal microbiome showed limited congruence with host phylogeny, and neither captivity nor diet elicited substantial effects on the vaginal microbiomes of primates. Permutational multivariate analysis of variance and Wilcoxon tests revealed correlations among vaginal microbiota and host species-specific socioecological factors, particularly related to sexuality, including: female promiscuity, baculum length, gestation time, mating group size and neonatal birth weight. The proportion of unclassified taxa observed in nonhuman primate samples increased with phylogenetic distance from humans, indicative of the existence of previously unrecognized microbial taxa. These findings contribute to our understanding of host–microbe variation and coevolution, microbial biogeography, and disease risk, and have important implications for the use of animal models in studies of human sexual and reproductive diseases.