Resource landscape shapes the composition and stability of the human vaginal microbiota
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Abstract
The vaginal microbiota is associated with the health of women and newborns alike. Despite its comparatively simple composition relative to other human microbiota systems, the mechanisms underpinning the dynamics and stability of vaginal microbial communities remain elusive. A crucial, yet so far underexplored, aspect of vaginal microbiota ecology is the role played by nutritional resources. Glycogen and its derivatives, produced by vaginal epithelia, are accessible to all bacterial constituents of the microbiota. Concurrently, free sialic acid and fucose offer supplementary nutritional resources to bacterial strains capable of cleaving them from glycans, which are structurally integral to mucus. Notably, bacteria adept at sialic acid exploitation are often correlated with adverse clinical outcomes and are frequently implicated in bacterial vaginosis (BV). In this study, we introduce a novel mathematical model tailored to human vaginal microbiota dynamics to explore the interactions between bacteria and their respective nutritional landscape. Our resource-based model examines the impact of the relative availability of glycogen derivatives (accessible to all bacterial species) and sialic acid (exclusive to some BV-associated bacteria) on the composition of the vaginal microbiota. Our findings elucidate that the success of BV-associated bacteria is intricately linked to their exclusive access to specific nutritional resources. This private access fortifies communities dominated by BV-associated bacteria, rendering them resilient to compositional transitions. We empirically corroborate our model prediction with longitudinal clinical data on microbiota composition and previously unpublished metabolomic profiles obtained from a North American cohort. The insights gleaned from this study shed light on potential pathways for BV prevention and treatment.
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Theoretical ecology can have practical implications – actually, it is one of its most fundamental purposes, as a theory is useful only if it helps understand reality and lends itself to empirical tests or applications. While many classics in theoretical ecology have been inspired by the observation of “macroorganisms”, the same theories have repeatedly and consistently embraced empirics in the world of microorganisms, starting with Gause’s experimental works on Volterra’s theory (Gause, 1934). The recent surge of interest towards microbiota and the involvement of such microorganism communities in their host’s functions has, however, shifted the position of microorganisms from “simple organisms useful to test theories” to that of “important critters deserving theories” (Coyte et al., 2015, Shapira, 2016, Koskella et al., 2017).
As …
Theoretical ecology can have practical implications – actually, it is one of its most fundamental purposes, as a theory is useful only if it helps understand reality and lends itself to empirical tests or applications. While many classics in theoretical ecology have been inspired by the observation of “macroorganisms”, the same theories have repeatedly and consistently embraced empirics in the world of microorganisms, starting with Gause’s experimental works on Volterra’s theory (Gause, 1934). The recent surge of interest towards microbiota and the involvement of such microorganism communities in their host’s functions has, however, shifted the position of microorganisms from “simple organisms useful to test theories” to that of “important critters deserving theories” (Coyte et al., 2015, Shapira, 2016, Koskella et al., 2017).
As vaginal bacterial community composition affects the occurrence of bacterial vaginosis in humans, Kamiya et al. (2025) have endeavoured to understand the determinants of bacterial dominance within this microbiome. Various studies, on competitive (Wale et al., 2017), parasitic (Griffiths et al., 2014) and mutualistic (Weese et al., 2015) microbes suggest that resource acquisition is key to understand microbial community dynamics, on both ecological and evolutionary timescales. Some well-known examples of bacterial communities evolving as a result of competition for resources include the evolution of private vs. common siderophores when iron is the limiting nutrient (Niehus et al., 2017). Based on in vitro observations reported in the literature, Kamiya et al. (2025) have thus based their model of bacterial type abundances on the exploitation of shared (glycogen) and private resources (sialoglycans). With the addition of a last assumption regarding direct negative interactions between bacterial types due to change in pH, they have uncovered three different regimes within the parameter space of the model, with the two regimes of dominance of normal and dysbiotic bacteria separated by a zone of alternative stable states (hysteresis) – a situation of historical contingency reminiscent of other microbial communities, such as those found in pitcher plant microbiota (Bittleston et al., 2020). They have thus determined conditions under which the vaginal microbiota community becomes surely dysbiotic, surely healthy, or can be in one or the other state depending on initial conditions and perturbations. Comparing their predictions with original data on vaginal community types shows that model predictions are generally correct, and thus lends credence to the hypothesis that vaginal microbiota community dynamics is strongly determined by resource ratio and community assembly history.
This study is remarkable and merits reading for several reasons. From a purely formal point of view, it is remarkable because it breaks the invisible barrier that ecologists often erect between theoretical and empirical works. With both a model and its positive confrontation with existing data, the proposed hypothesis is more than just a construction of the mind. From a more thematic viewpoint, this study highlights a prospective path towards both treatment and prevention of bacterial vaginosis, with an important caveat stemming from the intrinsic tendency of the model to display hysteresis: prevention will always be easier. And finally, from a more conceptual standpoint, this paper underlines yet another route by which bacteria can become competitively dominant ecosystem engineers in their environment, namely by facilitating the production of private resources and antagonizing other bacteria controlling ecosystem parameters such as pH. For any ecologist or evolutionary biologist interested in keeping up with good theoretical ideas, their neat empirical confirmations and potential applications, I strongly recommend the reading of this study.
References
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