Lactation and menstruation shift the vaginal microbiota in captive rhesus monkeys to be more similar to the male urethral microbiota

Abstract

The vaginal microbiota of nonhuman primates differs substantially from humans in terms of Lactobacillus abundance, overall taxonomic diversity, and vaginal pH. Given these differences, it remains unclear in what way the nonhuman primate genital microbiota protects against pathogens, in particular sexually transmitted infections. Considering the effect that microbiota variations can have on disease acquisition and outcome, we examined endogenous and exogenous factors that influence the urogenital microbiota of male and female captive rhesus monkeys. The male urethral (n = 37) and vaginal (n = 194) microbiota of 11 breeding groups were examined in a cross-sectional study. During lactation and menstruation, the vaginal microbiota becomes significantly more diverse and more similar to the microbes observed in the male urethra. Group association and cage-mate (sexual partners) relationships were additionally associated with significant differences in the urogenital microbiota. Our results demonstrate that microbiota considerations are necessary in order to make informed selection of nonhuman primates as translational animal models.

Intestinal microbial diversity in female rhesus (Macaca mulatta) at different physiological periods

“…These changes are accompanied by changes in the microbiota, especially in the vagina and intestines ( Chen et al, 2017 ). A study of breastfeeding rhesus monkeys vaginal microbes during menstruation found that hormonal status affected the changes in microbiota ( Hallmaier-Wacker et al, 2019 ). It is generally believed that autoimmune diseases are the result of complex interactions between genetic and environmental factors.…”

“…Studies comparing the individual intestinal flora in mice showed that metabolic changes such as hyperglycemia, insulin resistance, and weight gain are related to changes in the composition of intestinal flora during pregnancy ( Curtis et al, 2012 ). Likewise, studies reported that the bacterial community of captive rhesus monkeys becomes more diversified with significantly different bacterial compositions during lactation and menstrual periods ( Hallmaier-Wacker et al, 2019 ). At present, there are rare reports about the changes in intestinal microbes during the menstrual cycle.…”

Microbiome Studies in Non-human Primates

“…It remains unclear what biological factors contribute to Lactobacillus dominance and whether the cervicovaginal microbiome can be durably modulated by therapeutic intervention [ 85 ]. Hallmaier-Wacker et al found that menstruation is associated with a significant increase in alpha diversity and shift in beta-diversity among the rhesus vaginal microbiome [ 82 ]. Although vaginal community composition varies widely between individual macaques, Nugeyre et al identified taxa that cycled with progesterone levels within individual cynomolgus macaques and similarly, Rhoades et al observed that clinical markers of bacterial vaginosis differed significantly by menstrual status in rhesus macaques, as in women [ 80 •, 81 , 84 , 86 ].…”

Metagenomics in One Health — from standardization to targeted application

“…pallidum) and simian immunodeficiency virus (SIV) (Marra et al, 1992). In Chapter B3, our data show that endocrine-regulated processes (lactation/menstruation), cage-mate (sexual partners) relationships and group associations can significantly impact the urogenital microbiota (Hallmaier-Wacker et al, 2019a). Since these differences likely influence biomedical experiments, we urge for increased awareness of microbiota considerations of translational animal models.…”

“…These findings have implications not only for disease ecology but also for the use of translational animal models (Kostic et al, 2013). In Chapter B3, we examined the genital microbiota of male and female rhesus monkeys (Hallmaier-Wacker et al, 2019a). Rhesus monkeys are commonly used translational animal models for infectious diseases, including sexually transmitted infections (Haus et al, 2014;Spear et al, 2010).…”