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

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.

Copulatory and Postcopulatory Sexual Selection in Primates

“…As far as we know, all primates ejaculate intravaginally so that buffering of vaginal pH by semen might constitute a general phenomenon for the order as a whole. Some caution is advisable, however, as it transpires that human vaginal pH is exceptionally low, averaging 4.5, as compared to pH values of 7.6 (Macaca nemestrina), 5.0-5.6 (Papio anubis), 5.5 (P. cynocephalus) and 6.5 (A. geoffroyi) at around the time of the oestrogen peak [Miller et al, 2016]. Nonetheless, in the last of the species listed (the black-handed spider monkey, A. geoffroyi), Hernández-López et al [2008] have demonstrated positive effects of the presence of a seminal coagulum upon vaginal pH (increased to 7.0) and the migration of fast linearly moving sperm into the uterus following intravaginal artificial insemination procedures.…”

Biological properties and production of bacteriocins‐like‐inhibitory substances by Lactobacillus sp. strains from human vagina

“…) and they are present in concentrations of 10 7 –10 8 CFU per gram of vaginal fluid, where glycogen is considered the maximum source of fermentable carbohydrates although the presence of the enzyme alpha‐amylase is necessary to break down glycogen into a form usable by lactobacilli strains which cannot directly metabolize glycogen (Miller et al . ; Fuochi et al . ).…”

Bacterial Vaginosis and Sexually Transmitted Diseases: Relationship and Management

“…An understanding of the diversity of the vaginal microbial environment during states of health and disease is essential for the identification of risk factors for disease and the development of appropriate treatment [26].…”

“…These lactobacilli process glycogen and it breaks down products to produce lactic acid, leading to an exceptional low vaginal pH of < 4.5 [26].…”

“…In addition to these mechanistic hypothesis, two evolutionary explanation have been proposed, the first, referred to as the "disease risk hypothesis," proposes that humans have higher STDs risk than nonhuman mammals because species with promiscuous mating strategies are [26].…”