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      Lactobacilli Dominance and Vaginal pH: Why Is the Human Vaginal Microbiome Unique?

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          Abstract

          The human vaginal microbiome is dominated by bacteria from the genus Lactobacillus, which create an acidic environment thought to protect women against sexually transmitted pathogens and opportunistic infections. Strikingly, lactobacilli dominance appears to be unique to humans; while the relative abundance of lactobacilli in the human vagina is typically >70%, in other mammals lactobacilli rarely comprise more than 1% of vaginal microbiota. Several hypotheses have been proposed to explain humans' unique vaginal microbiota, including humans' distinct reproductive physiology, high risk of STDs, and high risk of microbial complications linked to pregnancy and birth. Here, we test these hypotheses using comparative data on vaginal pH and the relative abundance of lactobacilli in 26 mammalian species and 50 studies ( N = 21 mammals for pH and 14 mammals for lactobacilli relative abundance). We found that non-human mammals, like humans, exhibit the lowest vaginal pH during the period of highest estrogen. However, the vaginal pH of non-human mammals is never as low as is typical for humans (median vaginal pH in humans = 4.5; range of pH across all 21 non-human mammals = 5.4–7.8). Contrary to disease and obstetric risk hypotheses, we found no significant relationship between vaginal pH or lactobacilli relative abundance and multiple metrics of STD or birth injury risk ( P-values ranged from 0.13 to 0.99). Given the lack of evidence for these hypotheses, we discuss two alternative explanations: the common function hypothesis and a novel hypothesis related to the diet of agricultural humans. Specifically, with regard to diet we propose that high levels of starch in human diets have led to increased levels of glycogen in the vaginal tract, which, in turn, promotes the proliferation of lactobacilli. If true, human diet may have paved the way for a novel, protective microbiome in human vaginal tracts. Overall, our results highlight the need for continuing research on non-human vaginal microbial communities and the importance of investigating both the physiological mechanisms and the broad evolutionary processes underlying human lactobacilli dominance.

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          Did the end-Cretaceous mass extinction event, by eliminating non-avian dinosaurs and most of the existing fauna, trigger the evolutionary radiation of present-day mammals? Here we construct, date and analyse a species-level phylogeny of nearly all extant Mammalia to bring a new perspective to this question. Our analyses of how extant lineages accumulated through time show that net per-lineage diversification rates barely changed across the Cretaceous/Tertiary boundary. Instead, these rates spiked significantly with the origins of the currently recognized placental superorders and orders approximately 93 million years ago, before falling and remaining low until accelerating again throughout the Eocene and Oligocene epochs. Our results show that the phylogenetic 'fuses' leading to the explosion of extant placental orders are not only very much longer than suspected previously, but also challenge the hypothesis that the end-Cretaceous mass extinction event had a major, direct influence on the diversification of today's mammals.
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              Temporal dynamics of the human vaginal microbiota.

              Elucidating the factors that impinge on the stability of bacterial communities in the vagina may help in predicting the risk of diseases that affect women's health. Here, we describe the temporal dynamics of the composition of vaginal bacterial communities in 32 reproductive-age women over a 16-week period. The analysis revealed the dynamics of five major classes of bacterial communities and showed that some communities change markedly over short time periods, whereas others are relatively stable. Modeling community stability using new quantitative measures indicates that deviation from stability correlates with time in the menstrual cycle, bacterial community composition, and sexual activity. The women studied are healthy; thus, it appears that neither variation in community composition per se nor higher levels of observed diversity (co-dominance) are necessarily indicative of dysbiosis.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                08 December 2016
                2016
                : 7
                : 1936
                Affiliations
                [1] 1Department of Biological Sciences, University of Notre Dame Notre Dame, IN, USA
                [2] 2Department of Biology, Geology and Environmental Science, University of Tennessee at Chattanooga Chattanooga, TN, USA
                [3] 3Department of Applied Ecology, North Carolina State University Raleigh, NC, USA
                [4] 4Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark, University of Copenhagen Copenhagen, Denmark
                [5] 5Institute of Primate Research, National Museums of Kenya Nairobi, Kenya
                Author notes

                Edited by: Robert Brucker, Rowland Institute at Harvard, USA

                Reviewed by: Elisabeth Margaretha Bik, uBiome, USA; Carl James Yeoman, Montana State University, USA

                *Correspondence: Elizabeth A. Miller emille18@ 123456nd.edu

                This article was submitted to Microbial Symbioses, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2016.01936
                5143676
                28008325
                aeaa4af3-2f17-4655-8b58-152237f252de
                Copyright © 2016 Miller, Beasley, Dunn and Archie.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 24 August 2016
                : 17 November 2016
                Page count
                Figures: 4, Tables: 3, Equations: 3, References: 112, Pages: 13, Words: 10619
                Funding
                Funded by: National Science Foundation 10.13039/100000001
                Award ID: DGE-1313583
                Award ID: IOS-1053461
                Award ID: MSP-1319293
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                vaginal microbiome,lactobacilli,ph,estrogen,mammals,evolution
                Microbiology & Virology
                vaginal microbiome, lactobacilli, ph, estrogen, mammals, evolution

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