title: Destabilization of the gut microbiome marks the end-stage of simian immunodeficiency virus infection in wild chimpanzees.
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. © 2015 Wiley Periodicals, Inc.
authors.affiliation: Department of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.|Department of Microbiology, University of Pennsylvania, Philadelphia, Pennsylvania.
authors.forename: Hannah J
authors.initials: HJ
authors.lastname: Barbian
authors.affiliation: Department of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.|Department of Microbiology, University of Pennsylvania, Philadelphia, Pennsylvania.
authors.forename: Yingying
authors.initials: Y
authors.lastname: Li
authors.affiliation: Department of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
authors.forename: Miguel
authors.initials: M
authors.lastname: Ramirez
authors.affiliation: Department of Biological Sciences, University of the Sciences, Philadelphia, Pennsylvania.
authors.forename: Zachary
authors.initials: Z
authors.lastname: Klase
authors.affiliation: Gombe Stream Research Center, Kigoma, Tanzania.
authors.forename: Iddi
authors.initials: I
authors.lastname: Lipende
authors.affiliation: Gombe Stream Research Center, Kigoma, Tanzania.
authors.forename: Deus
authors.initials: D
authors.lastname: Mjungu
authors.affiliation: Department of Integrative Biology, University of California, Berkeley, California.|Miller Institute for Basic Research, University of California, Berkeley, California.
authors.forename: Andrew H
authors.initials: AH
authors.lastname: Moeller
authors.affiliation: Department of Anthropology, University of Minnesota, Minneapolis, Minnesota.|Department of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, Minnesota.
authors.forename: Michael L
authors.initials: ML
authors.lastname: Wilson
authors.affiliation: Department of Evolutionary Anthropology, Duke University, Durham, North Carolina.
authors.forename: Anne E
authors.initials: AE
authors.lastname: Pusey
authors.affiliation: Department of Psychology, Franklin and Marshall College, Lancaster, Pennsylvania.
authors.forename: Elizabeth V
authors.initials: EV
authors.lastname: Lonsdorf
authors.affiliation: Department of Microbiology, University of Pennsylvania, Philadelphia, Pennsylvania.
authors.forename: Frederic D
authors.initials: FD
authors.lastname: Bushman
authors.affiliation: Department of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.|Department of Microbiology, University of Pennsylvania, Philadelphia, Pennsylvania.
authors.forename: Beatrice H
authors.initials: BH
authors.lastname: Hahn
mesh_terms: D000261:Adenoviruses, Simian / Q000235:genetics; D000818:Animals; D018420:Ape Diseases / Q000382:microbiology* / Q000821:virology; D001419:Bacteria / Q000145:classification* / Q000235:genetics; D004267:DNA Viruses / Q000235:genetics; D005243:Feces / Q000382:microbiology / Q000821:virology; D005260:Female; D000069196:Gastrointestinal Microbiome; D008297:Male; D054892:Metagenome; D002679:Pan troglodytes; D012336:RNA, Ribosomal, 16S; D016097:Simian Acquired Immunodeficiency Syndrome / Q000382:microbiology* / Q000473:pathology; D015302:Simian Immunodeficiency Virus; D013636:Tanzania
chemical_list: D012336:RNA, Ribosomal, 16S
keywords: AIDS enteropathy; SIVcpz; chimpanzees; dysbiosis; fecal virome; gut microbiome