Microbial Ecology in States of Health and Disease Workshop Summary (2014) / Chapter Skim
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A11 Community ecology and the vaginal microbiome--Larry J. Forney and Jacques Ravel
A11 Community ecology and the vaginal microbiome--Larry J. Forney and Jacques Ravel
Pages 292-322
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From page 292... ...
To better define variation in the species composition of these communities we conducted a cross-sectional study in which the vaginal bacterial communities of 396 asymptomatic North American women that represented four ethnic groups (white, black, Hispanic, and Asian) were sampled and the species composition was characterized by pyrosequencing of barcoded 16S rRNA genes.
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From page 293... ...
It is envisioned that better knowledge of vaginal community dynamics and the mutualism between the host and indigenous bacterial communities will lead to the development of strategies to manage the vaginal ecosystem in a way that promotes health and minimizes the use of antibiotics. These efforts should take into account the temporal dynamics of vaginal communities and the potential problems that might arise from diagnostic and therapeutic strategies based on cross-sectional studies.
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From page 294... ...
The environmental pH of the vagina, traditionally considered to be around 4.0–4.5 in healthy women, is presumably determined by the organic acid contributions from both epithelial cells, resident LAB, and other anaerobic and strictly anaerobic bacteria (Linhares et al., 2010)
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. While numerous studies have been done to understand the vaginal microbiology of reproductive age women, far fewer studies have been done on the vaginal microbiota48 of premenarcheal, perimenopausal, and postmenopausal females.
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Below we summarize the results of studies done by our group using this approach and the insights to the structure, function, and dynamics of vaginal microbial communities that have been obtained. Results Vaginal Bacterial Community Composition and Structure We characterized the vaginal microbiota and vaginal pH of 396 asymptomatic, sexually active women that fairly equally represented four self-reported ethnic groups: Caucasian (N = 98)
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From page 297... ...
It highlights the diversity found in all vaginal bacterial communities, even those where the phylotypes abundance is highly skewed and dominated by a single phylotype, and identifies taxa with similar correlation profiles. The analysis revealed five major groups of microbial communities, which we named community state types (CST)
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(A) Complete linkage clustering of samples based the species composition and abundance of vaginal bacterial communities that defines community groups I to V
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, and this offered the oppor tunity to assess the relationship of ethnic background on vaginal bacterial community composition. The proportions of each CST varied among the four ethnic groups (Figures A11-2 and A11-3)
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. FIGURE A11-3 Contribution of ethnicity to each of the five vaginal community groups expressed as percentage.
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Studies done to tease out the influence of these various factors on vaginal community ecology will be important to understanding community stability, resistance, and resilience so that strategies can be developed to maintain human vaginal health and prevent disease. Vaginal Community Space The relationships among communities were visualized by principal component analysis and displayed in three-dimensional (3-D)
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Communities found on the edges joining two vertices are mixtures of the two Lactobacillus species that dominate the communities found at the corresponding vertices, with an equal proportion of each species at the midpoint of the edge. We refer to each location in this 3-D space as a community state, and one can consider the entire space to represent the plausible alternative community states, or vaginal bacterial community space.
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The pH and Nugent scores of each community are depicted in the 3-D community space on Figures A11-4B and A11-4C. The figures show a strong correlation between high pH and high Nugent scores.49 The lowest pH values were associated with community states dominated by L
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Importantly, it also suggests m that differences in vaginal bacterial community composition should be taken into account in the estimation of disease risks. This would constitute the first
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sequences per sample. Using the methods described above the bacterial communities sampled were classified into one of five community state types based on differences in species composition and their relative abundances (Figure A11-5)
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(B) Community state types resulting from clustering analysis wherein each sample was assigned to one of the five community state type (CST I, CST II, CST III, CST IV-A, and CST IV-B)
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(C) Profiles of community state types, Nugent scores, and menses for 32 women over a 16-week period.
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Thus, highly variable vaginal bacterial communities do not always have persistently high Nugent scores, so variation per se does not always equate with disease. These results suggest that neither variation in community composition, nor constantly high levels of apparent diversity (codominance)
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These communities were rather stable, exhibited fewer transitions between community states, and typically had low Nugent scores. In these women most transitions between community states were associated with menses (Figure A11-6)
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This is illustrated by the communities of subjects 14, 15, 16, 18, and 19 that appeared rather stable over time, while others such as 11 and 27 commonly shifted to different community types that were more often associated with higher Nugent scores. These differences might reflect genomic heterogeneity in the dominating Lactobacillus sp.
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. These illustrations show that while the vaginal community composition of many FIGURE A11-9 Temporal dynamics of vaginal bacterial communities in two women over 16 weeks.
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. Identifying Factors of Stability Disturbance In an effort to evaluate the dependence of stability of vaginal bacterial communities on the time in the menstrual cycle and other time-varying factors, we modeled the log Jensen-Shannon divergence rate of change over normalized menstrual cycles using a linear mixed effects model with a Fourier polynomial of the normalized menstrual time component adjusted for hormonal contraception, community type, sexual activities, lubricant use and douching (with the last three evaluated 1 day prior to sampling)
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The species that make up vaginal microbial communities vary between indi viduals as do the dynamics of these communities. The differences between individuals can be demonstrated by what has been learned about the vaginal microbiome wherein at least five bacterial community state types are common in healthy reproductive age women, and the frequencies of these types vary among women of different ethnic groups.
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From page 314... ...
, considerable variability exists within the definition of a "normal" vaginal microbiome. When surveyed cross-sectionally, it appears that several distinct "community state types" exist in normal, otherwise healthy women, each with a markedly different bacterial species composition and pH profile, and that the prevalence of each varies with ethnicity (Ravel et al., 2011)
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Ecological Dynamics of the Vaginal Microbiota The dynamics of vaginal communities were found to vary widely among women even among those that clustered in the same community class, and the communities of some women were shown to have low constancy and high levels of species turnover. These findings suggest that point estimates of community composition that arise from cross-sectional studies could be misleading for most women because they experience a distribution of community states over time I
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Community Stability: Resistance Versus Resilience Vaginal bacterial communities that differ in species composition are expected to differ in their resilience and resistance to environmental change, and this is manifest in the degree of stability that each exhibits over time. The resistance of a community is a measure of its ability to resist changes in response to a disturbance event, and it is measured by the amount of change the community can withstand without having an impact on community function (McCann, 2000)
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From page 317... ...
More robust communities, however, may be able to retain community structure and function, despite more frequent events of low to moderate intensity. Given this, we postulate that stability and resilience of vaginal bacterial communities is likely to vary widely since the species composition and structure of these communities differs among women and this variance in turn may account for differences in the susceptibility of individuals to urogenital infectious diseases.
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. While these studies have yielded valuable information in terms of species composition, they do not allow for any assessment of community stability, therefore painting an incomplete picture of vaginal microbial ecology.
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These might include other low molecular weight metabolites, including various short-chain fatty acids that are produced by strict anaerobes that inhabit the vagina. This is an appealing idea because vaginal bacterial species have coevolved with their hosts over time, and it seems likely that they collectively provide benefits to the host as part of a complex mutualistic relationship.
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2002. Exposure to chronic stress and ethnic differences in rates of bacterial vaginosis among pregnant women.
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2012. Temporal dynamics of the human vaginal microbiota.
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2008. The Human Vaginal Bacterial Biota and Bacterial Vaginosis.
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