Abstract
The female reproductive tract (FRT) microbiome plays a vital role in maintaining vaginal health. Viruses are key regulators of other microbial ecosystems, but little is known about how the FRT viruses (virome), particularly bacteriophages that comprise the phageome, impact FRT health and dysbiosis. We hypothesize that bacterial vaginosis (BV) is associated with altered FRT phageome diversity, transkingdom interplay, and bacteriophage discriminate taxa. Here, we conducted a retrospective, longitudinal analysis of vaginal swabs collected from 54 BV-positive and 46 BV-negative South African women. Bacteriome analysis revealed samples clustered into five distinct bacterial community groups (CGs), and further, bacterial alpha diversity was significantly associated with BV. Virome analysis on a subset of baseline samples showed FRT bacteriophages clustering into novel viral state types (VSTs), a viral community clustering system based on virome composition and abundance. Distinct BV bacteriophage signatures included increased alpha diversity along with discriminant Bacillus, Burkholderia, and Escherichia bacteriophages. Bacteriophage-bacteria transkingdom associations were also identified between Bacillus and Burkholderia viruses and BV-associated bacteria, providing key insights for future studies elucidating the transkingdom interactions driving BV-associated microbiome perturbations. In this cohort, bacteriophage-bacterial associations suggest complex interactions, which may play a role in the establishment and maintenance of BV.
Highlights
The female reproductive tract (FRT) houses a compositionally dynamic environment where the host participates in an intricate interplay with a microbiome composed of bacteria and archaea, fungi, viruses, and occasional protozoal parasites [1,2]
50 human immunodeficiency virus (HIV)-positive and 50 HIV-negative young, sexually active South African women ages 16–21 were recruited in Cape Town, South Africa between October 2012 and October
Bacteriophages have been studied at other mucosal sites in humans, including the gut [61], this is the first description of bacteriophage community groupings, which may be unique to the FRT environment due to the distinctive bacterial communities present
Summary
The female reproductive tract (FRT) houses a compositionally dynamic environment where the host participates in an intricate interplay with a microbiome composed of bacteria and archaea (bacteriome), fungi (fungome), viruses (virome), and occasional protozoal parasites [1,2]. At least five different bacterial community groupings have been described within the FRT, distinguishable by the dominance of Lactobacillus species or the presence of more diverse anaerobes [7,8]. Lactobacillus-dominant FRT bacteriomes, especially L. crispatus, protect against vaginal disease through several mechanisms, including by competitive exclusion of pathogenic bacteria for space and nutrients, promoting an acidic vaginal environment via production of lactic acid, and maintaining a low inflammatory state [10,11,12]. BV, the most common cause of vaginal discharge in reproductive age women, is a symptomatic clinical condition characterized by a shift in the FRT microbiota away from a low inflammatory, Lactobacillusdominant bacteriome to a more diverse community including facultative anaerobes.
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