Identification of rhesus macaque genital microbiota by 16S pyrosequencing shows similarities to human bacterial vaginosis: implications for use as an animal model for HIV vaginal infection

Abstract

The composition of the lower genital tract microbiota in women is believed to affect the risk of sexually acquiring HIV. Since macaque genital microbiota could similarly impact vaginal infection with SIV we identified microbiota in 11 rhesus macaques using multitag pyrosequencing of the 16S rRNA gene. The microbiota was polymicrobial with a median of nine distinct bacterial taxa per macaque (range 3-16 taxa, each constituting 1% or more of the sequences). Taxa frequently found included Peptoniphilus, Sneathia, Porphyromonas, Mobiluncus, Atopobacter, Dialister, Thioreductor, Prevotella, and Streptococcus, many of which are also frequently found in women with bacterial vaginosis. Lactobacillus sequences (mostly L. johnsonii) were found in only four macaques but were not predominant in any (median of 0% of sequences, range 0-39%). All macaques were resampled 6 months after the first time point to determine the stability of the microbiota. The microbiota remained polymicrobial with a median of 10 taxa (range 6-18). Microbial patterns remained similar for six of the macaques, changed substantially in two, and had a mixed pattern in three. Significant sialidase enzyme activity, a marker of bacteria vaginosis in women, was detected in genital fluid from 9/11 and 8/11 macaques from the first and second time points, respectively. These results show that the macaque lower genital microbiota resembled a bacteria vaginosis-type microbiota in women and suggest that the microbiota of macaques in captivity promote rather than protect against vaginal infection with SIV. These results also suggest macaques could be used as an animal model to study some aspects of bacterial vaginosis.

FIG. 1.

Frequencies of Bacterial Taxa Identified in 11 Macaques

FIG. 1.

Frequencies of Bacterial Taxa Identified in 11 Macaques

FIG. 2.

Predominant Bacterial Sequences in Macaques

FIG. 3.

Macaque Genital Fluid pH over 14 Months

FIG. 4.

Sialidase activity in macaque CVL samples. Genital fluid from 11 macaques, sampled at two different times, was tested for sialidase activity. Sialidase activity in CVL obtained from 13 women with no bacterial vaginosis (Normal) and 30 women with bacterial vaginosis (BV) is also shown for comparison. CVL was collected from women using 10 ml of saline. BV in the women was determined using Nugent gram stain values 7–10 while normal was 0–3.