Directed shift of vaginal microbiota induced by vaginal application of sucrose gel in rhesus macaques

Hu, Kaitao; Zheng, Jinxin; Yu, Ziming; Chen, Zhong; Cheng, Hang; Pan, Weiguang; Yang, Wenjing; Wang, Hongyan; Deng, Qi; Zeng, Zhongming

doi:10.1016/j.ijid.2014.12.040

Cited by 16 publications

(21 citation statements)

References 17 publications

(13 reference statements)

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“…In addition to these shared functions, the core genome of L. crispatus also includes the enzymes necessary to ferment lactose, galactose, fructose, and sucrose. A previous study showed that the application of a sucrose gel can select for L. crispatus in the Rhesus macaque vagina (62), lending credence to this result. Furthermore, fructose can be found in high abundance in male ejaculate (63).…”

Section: Discussionsupporting

confidence: 55%

Genomic Comparisons of Lactobacillus crispatus and Lactobacillus iners Reveal Potential Ecological Drivers of Community Composition in the Vagina

Mendes‐Soares

Forney

2016

Appl Environ Microbiol

113

115

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Lactobacillus crispatus and Lactobacillus iners are common inhabitants of the healthy human vagina. These two species are closely related and are thought to perform similar ecological functions in the vaginal environment. Temporal data on the vaginal microbiome have shown that nontransient instances of cooccurrence are uncommon, while transitions from an L. iners-dominated community to one dominated by L. crispatus, and vice versa, occur often. This suggests that there is substantial overlap in the fundamental niches of these species. Given this apparent niche overlap, it is unclear how they have been maintained as common inhabitants of the human vagina. In this study, we characterized and compared the genomes of L. iners and L. crispatus to gain insight into possible mechanisms driving the maintenance of this species diversity. Our results highlight differences in the genomes of these two species that may facilitate the partitioning of their shared niche space. Many of the identified differences may impact the protective benefits provided to the host by these two species. IMPORTANCEThe microbial communities that inhabit the human vagina play a critical role in the maintenance of vaginal health through the production of lactic acid and lowering the environmental pH. This precludes the growth of nonindigenous organisms and protects against infectious disease. The two most common types of vaginal communities are dominated by either Lactobacillus iners or Lactobacillus crispatus, while some communities alternate between the two over time. We combined ecological theory with state-of-the-art genome analyses to characterize how these two species might partition their shared niche space in the vagina. We show that the genomes of L. iners and L. crispatus differ in many respects, several of which may drive differences in their competitive abilities in the vagina. Our results provide insight into factors that drive the complicated temporal dynamics of the vaginal microbiome and demonstrate how closely related microbial species partition shared fundamental niche space. The microbial communities that inhabit the vaginas of healthy reproductive age women commonly contain high proportions of Lactobacillus species (1). Studies have shown that these communities can be divided into five different types, four of which are dominated by either Lactobacillus iners, Lactobacillus crispatus, Lactobacillus gasseri, or Lactobacillus jensenii (2). These four species are closely related and are thought to perform similar ecological functions in the vaginal environment (namely, the production of lactic acid) (3, 4). Instances of cooccurrence among these species are rare, and temporal data have demonstrated that shifts in the dominant Lactobacillus are common (5), suggesting that the species compete for shared niche space in the vagina. Ecological theory predicts that multiple species cannot occupy the same niche indefinitely, as one will eventually outcompete the others (6). Therefore, it is unclear how the four Lactobacillus spec...

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Section: Discussionsupporting

confidence: 55%

Genomic Comparisons of Lactobacillus crispatus and Lactobacillus iners Reveal Potential Ecological Drivers of Community Composition in the Vagina

Mendes‐Soares

Forney

2016

Appl Environ Microbiol

113

115

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“…Detailed analysis of the pigtail macaque vaginal microbiome has been reported resulting in preferred use of this species in microbicide studies . RM and particularly CM vaginal environments have received comparatively less attention, even though both species are used extensively for the testing of vaccine efficacy, including protection from repeated vaginal challenges . Moreover, the ability to colonize macaques with Lactobacilli to mimic a healthy human vaginal environment has not systematically been attempted.…”

Section: Discussionmentioning

confidence: 99%

Comparison of the vaginal environment in rhesus and cynomolgus macaques pre‐ and post‐lactobacillus colonization

Daggett

Zhao

Connor-Stroud

et al. 2017

J of Medical Primatology

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Background Rhesus and cynomologus macaques are valuable animal models for the study of Human Immunodeficiency Virus (HIV) prevention strategies. However, for such studies focused on the vaginal route of infection, differences in vaginal environment may have deterministic impact on the outcome of such prevention, providing the rationale for this study. Methods We tested the vaginal environment of rhesus and cynomolgus macaques longitudinally to characterize the normal microflora based on Nugent scores and pH. This evaluation was extended after colonization of the vaginal space with Lactobacilli in an effort to recreate NHP models representing the healthy human vaginal environment. Results and Conclusion Nugent scores and pH differed significantly between species, though data from both species were suggestive of stable bacterial vaginosis. Colonization with Lactobacilli was successful in both species leading to lower Nugent score and pH, though rhesus macaques appeared better able to sustain Lactobacillus spp over time.

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“…A more recent article utilizing DNA‐based sequencing reported that only 4 of 11 rhesus macaques had Lactobacillus sequences (Spear et al, ). Another study employing 16S rRNA sequencing found that Lactobacillus represented less than 2% of sequences in the vaginal specimens from 16 rhesus monkeys (Hu et al, ). These results are in marked contrast to the healthy profile for women, in whom Lactobacilli are typically the dominant taxa (Ravel et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…Some researchers have taken advantage of this bacterial attribute of the monkey reproductive tract to investigate clinical treatments for changing the commensal bacteria (Scorpio, Ruben, Liao, Hildreth, & Fletcher, ). Even in female rhesus monkeys, topical introduction of a sucrose gel vaginally for just 5 days markedly increased Lactobacilli , and decreased Porphyromonas, Sneathia , and Mobiluncus , and changed the acidity of their CVF (Hu et al, ). It has also been possible to colonize the reproductive tract of rhesus monkeys with recombinant Lactobacillus jensenii expressing an antiviral protein, which afforded protection against retroviral infection (Lagenaur et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…The Nugent score is a traditional test used in gynecological practice to diagnose BV, and is based on a Gram stain scoring system (Nugent, Krohn, & Hillier, ). Prior assessments of female monkeys indicated that their specimens often receive high scores (Doyle, Young, Jang, & Hillier, ; Hu et al, ). The aim was to determine the prevalence of this condition in an established breeding colony of rhesus monkeys, and to address the hypothesis that it might be associated with elevated cytokine levels indicative of inflammation.…”

Section: Introductionmentioning

confidence: 99%

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Low Lactobacilli abundance and polymicrobial diversity in the lower reproductive tract of female rhesus monkeys do not compromise their reproductive success

Amaral

Lubach

Kapoor

et al. 2017

American J Primatol

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The lower reproductive tract of nonhuman primates is colonized with a diverse microbiota, resembling bacterial vaginosis (BV), a gynecological condition associated with negative reproductive outcomes in women. Our 4 aims were to: 1) assess the prevalence of low Lactobacilli and a BV-like profile in female rhesus monkeys, 2) quantify cytokines in their cervicovaginal fluid (CVF), 3) examine the composition and structure of their mucosal microbiota with culture-independent sequencing methods, and 4) evaluate the potential influence on reproductive success. CVF specimens were obtained from 27 female rhesus monkeys for Gram's staining, and to determine acidity (pH), and quantify proinflammatory cytokines. Based on Nugent's classification, 40% had a score of 7 or higher, which would be indicative of BV in women. Nugent scores were significantly correlated with the pH of the CVF. Interleukin-1β was present at high concentrations, but not further elevated by high Nugent scores. Vaginal swabs were obtained from 8 additional females to determine microbial diversity by rRNA gene amplicon sequencing. At the phylum level, the Firmicutes/Bacteroidetes ratio was low. The relative abundance of Lactobacilli was also low (between 3–17%), and 11 other genera were present at >1%. However, neither the microbial diversity in the community structure, nor high Nugent scores, was associated with reduced fecundity. Female monkeys provide an opportunity to understand how reproductive success can be sustained in the presence of a diverse polymicrobial community in the reproductive tract.

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Directed shift of vaginal microbiota induced by vaginal application of sucrose gel in rhesus macaques

Abstract: Rhesus macaques can be used as animal models of bacterial vaginosis to develop drugs and test treatment efficacy. Furthermore, the topical application of sucrose gel induced the shifting of vaginal flora of rhesus macaques from a BV kind of flora to a lactobacilli-dominating flora.

Cited by 16 publications

References 17 publications

Genomic Comparisons of Lactobacillus crispatus and Lactobacillus iners Reveal Potential Ecological Drivers of Community Composition in the Vagina

Genomic Comparisons of Lactobacillus crispatus and Lactobacillus iners Reveal Potential Ecological Drivers of Community Composition in the Vagina

Comparison of the vaginal environment in rhesus and cynomolgus macaques pre‐ and post‐lactobacillus colonization

Low Lactobacilli abundance and polymicrobial diversity in the lower reproductive tract of female rhesus monkeys do not compromise their reproductive success

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