Longitudinal Assessment of Pigtailed Macaque Lower Genital Tract Microbiota by Pyrosequencing Reveals Dissimilarity to the Genital Microbiota of Healthy Humans

Abstract

Vaginal bacterial communities play an important role in human health and have been shown to influence HIV infection. Pigtailed macaques (Macaca nemestrina) are used as an animal model of HIV vaginal infection of women. Since the bacterial microbiota could influence retrovirus infection of pigtailed macaques, the genital microbiota in 10 cycling macaques was determined by pyrosequencing. The microbiota of all macaques was polymicrobial with a median of 13 distinct genera. Strikingly, the genera Sneathia and Fusobacterium, both in the phylum Fusobacteria, accounted for 18.9% and 13.3% of sequences while the next most frequent were Prevotella (5.6%), Porphyromonas (4.1%), Atopobium (3.6%), and Parvimonas (2.6%). Sequences corresponding to Lactobacillus comprised only 2.2% of sequences on average and were essentially all L. amylovorus. Longitudinal sampling of the 10 macaques over an 8-week period, which spanned at least one full ovulatory cycle, showed a generally stable presence of the major types of bacteria with some exceptions. These studies show that the microbiota of the pigtailed macaques is substantially dissimilar to that found in most healthy humans, where the genital microbiota is usually dominated by Lactobacillus sp. The polymicrobial makeup of the macaque bacterial populations, the paucity of lactobacilli, and the specific types of bacteria present suggest that the pigtailed macaque microbiota could influence vaginal retrovirus infection.

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

“…Women with BV also exhibited compositional similarities to healthy baboons and macaques, including moderately high relative abundances of Gardnerella, Mobiluncus, Sneathia , and Prevotella (e.g., Miller et al, in review; Spear et al, 2010, 2012; Uchihashi et al, 2015; Onderdonk et al, 2016). However, of the five macaque and baboon species in our data set, all but the olive baboon had significantly higher vaginal pH than BV women (ANOVA: F (5, 14) = 12.84, P = 8.12e-05; Figure 1), which suggests that similar microbial composition may not always translate into similar ecological functions and consequences (e.g., Mirmonsef et al, 2012).…”

“…To date, most comparative studies in mammals find that hosts with similar lifestyles and evolutionary histories harbor similar microbiomes at a given body site, both in the bacterial taxa they contain and the functions they provide to hosts (Ley et al, 2008a; Delsuc et al, 2014). One important exception to this pattern is the vaginal microbiome, where humans exhibit striking differences in community composition compared to other mammals (Spear et al, 2012; Swartz et al, 2014; Yildirim et al, 2014). Specifically, the human vaginal microbiome is dominated by Lactobacillus spp., which typically comprise >70% of resident bacteria in women, compared to <1% in other mammals.…”

Ovarian cycling and reproductive state shape the vaginal microbiota in wild baboons

“…To date, the majority of research on the vaginal microbiome of non-human primates has used captive animals (e.g., [6, 39, 41–43, 78]). Recently, several authors have called for greater use of wild subjects in studies of the microbiome, in part because of strong effects of captivity on host-associated microbial communities [79–81].…”

Live-Attenuated Lentivirus Immunization Modulates Innate Immunity and Inflammation while Protecting Rhesus Macaques from Vaginal Simian Immunodeficiency Virus Challenge

“…Although we did not attempt to determine the cause of the cervicitis found in some animals, the vaginal flora of captive rhesus and pigtail macaques is unique to each animal, and all animals are colonized with a large variety of bacterial vaginosis-type organisms (68,69). In women, bacterial vaginosis is a source of genital inflammation that is associated with HIV acquisition (6,65,(71)(72)(73).…”