Destabilization of the gut microbiome marks the end-stage of simian immunodeficiency virus infection in wild chimpanzees

Hannah J. Barbian, Yingying Li, Miguel Ramirez, Zachary Klase, Iddi Lipende, Deus Mjungu, Andrew H. Moeller, Michael L. Wilson, Anne E. Pusey, Elizabeth V. Lonsdorf, Frederic D. Bushman, Beatrice H. Hahn

Research output: Contribution to journalArticlepeer-review

18 Scopus citations

Abstract

Enteric dysbiosis is a characteristic feature of progressive human immunodeficiency virus type 1 (HIV-1) infection but has not been observed in simian immunodeficiency virus (SIVmac)-infected macaques, including in animals with end-stage disease. This has raised questions concerning the mechanisms underlying the HIV-1 associated enteropathy, with factors other than virus infection, such as lifestyle and antibiotic use, implicated as playing possible causal roles. Simian immunodeficiency virus of chimpanzees (SIVcpz) is also associated with increased mortality in wild-living communities, and like HIV-1 and SIVmac, can cause CD4+ T cell depletion and immunodeficiency in infected individuals. Given the central role of the intestinal microbiome in mammalian health, we asked whether gut microbial constituents could be identified that are indicative of SIVcpz status and/or disease progression. Here, we characterized the gut microbiome of SIVcpz-infected and -uninfected chimpanzees in Gombe National Park, Tanzania. Subjecting a small number of fecal samples (N = 9) to metagenomic (shotgun) sequencing, we found bacteria of the family Prevotellaceae to be enriched in SIVcpz-infected chimpanzees. However, 16S rRNA gene sequencing of a larger number of samples (N = 123) failed to show significant differences in both the composition and diversity (alpha and beta) of gut bacterial communities between infected (N = 24) and uninfected (N = 26) chimpanzees. Similarly, chimpanzee stool-associated circular virus (Chi-SCV) and chimpanzee adenovirus (ChAdV) identified by metagenomic sequencing were neither more prevalent nor more abundant in SIVcpz-infected individuals. However, fecal samples collected from SIVcpz-infected chimpanzees within 5 months before their AIDS-related death exhibited significant compositional changes in their gut bacteriome. These data indicate that SIVcpz-infected chimpanzees retain a stable gut microbiome throughout much of their natural infection course, with a significant destabilization of bacterial (but not viral) communities observed only in individuals with known immunodeficiency within the last several months before their death. Am. J. Primatol. 80:e22515, 2018.

Original languageEnglish (US)
Article numbere22515
JournalAmerican journal of primatology
Volume80
Issue number1
DOIs
StatePublished - Jan 2018

Bibliographical note

Funding Information:
Contract grant sponsor: National Institutes of Health; contract grant numbers: R01 AI50529, R01 AI58715, P30 AI045008, T32 AI 055400; contract grant sponsor: National Science Foundation; contract grant number: IOS-LTREB-1052693; contract grant sponsor: Jane Goodall Institute.

Funding Information:
We thank the Jane Goodall Institute field staff at the Gombe Stream Research Centre for collecting behavioral and observational health data as well as fecal samples from wild-living chimpanzees; Jacque Young, Christel Chehoud, and Paul Sharp for expert advice; Andrew Smith, Andrew Caffro, Eric Ruff, and Aubrey Bailey for technical assistance; Shivani Sethi for artwork and manuscript preparation; the Tanzania Commission for Science and Technology (COSTECH), the Tanzania Wildlife Research Institute (TAWIRI), and the Tanzania National Parks Association (TANAPA) for their support and permission to conduct research in Gombe. This work was supported by grants from the National Institutes of Health (R01 AI50529, R01 AI58715; P30 AI 045008), the National Science Foundation (IOS-LTREB-1052693), and the Jane Goodall Institute. HJB was funded by a training grant in Emerging Infectious Diseases (T32 AI 055400).

Keywords

  • AIDS enteropathy
  • SIVcpz
  • chimpanzees
  • dysbiosis
  • fecal virome
  • gut microbiome

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