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Longitudinal Profiling of the Macaque Vaginal Microbiome Reveals Similarities To bioRxiv preprint doi: https://doi.org/10.1101/2020.12.14.422805; this version posted December 15, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Longitudinal profiling of the macaque vaginal microbiome reveals similarities to 2 diverse human vaginal communities: implications for use as a pre-clinical model 3 for bacterial vaginosis. 4 5 Nicholas S. Rhoades1#, Sara M. Hendrickson2#, Danielle R. Gerken1, Kassandra 6 Martinez1, Ov D. Slayden3, Mark K. Slifka2*, Ilhem Messaoudi1* 7 8 1Department of Molecular biology and Biochemistry, University of California Irvine, Irvine, 9 CA, USA 10 2 Division of Neuroscience, Oregon National Primate Research Center, Beaverton OR, 11 USA 12 3Division of Reproductive & Developmental Sciences, Oregon National Primate 13 Research Center, Beaverton, OR, USA 14 USA 15 # These authors contributed equally to this work 16 17 * To whom correspondence should be addressed 18 Ilhem Messaoudi, PhD 19 Molecular Biology and Biochemistry 20 University of California Irvine 21 2400 Biological Sciences III 22 Irvine, CA 92697 23 Phone: 949-824-3078 24 Email: [email protected] 25 Or bioRxiv preprint doi: https://doi.org/10.1101/2020.12.14.422805; this version posted December 15, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 26 Mark Slifka, PhD 27 Division of Neuroscience 28 Oregon National Primate Research Center 29 Oregon Health & Science University 30 505 NW 185th Avenue 31 Beaverton, OR 97006 32 Phone: (503) 346-5483 33 Email: [email protected] 34 35 This PDF file includes: 36 Main Text 37 Table 1 38 Figures 1 to 5 39 Supplemental figures 1 to 4 40 Supplemental tables 1 to 2 41 bioRxiv preprint doi: https://doi.org/10.1101/2020.12.14.422805; this version posted December 15, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 42 ABSTRACT 43 The vaginal microbiota plays an important role in women’s reproductive and 44 urogenital health. Disturbances in this microbial community can lead to several adverse 45 outcomes including pelvic inflammatory disease, bacterial vaginosis (BV) as well as 46 increased susceptibility to sexually transmitted infections, miscarriage, and pre-term 47 births. It is now well accepted that while the microbiome of healthy women in the 48 developed world is dominated by Lactobacillus species, vaginal communities in 49 asymptomatic women, especially those in the developing world, can be comprised of a 50 diverse set of micro-organisms. The presence of a diverse vaginal microbiome has been 51 associated with increased susceptibility to HIV infection but their implications for 52 women’s health remain poorly understood. Rhesus macaques are an excellent 53 translational animal model due to significant physiological and genetic homology with 54 humans. In this study, we performed a longitudinal analysis of clinical and microbiome 55 data from 16 reproductive age female rhesus macaques. Many animals showed 56 hallmarks of BV, including Nugent scores above 7 and high vaginal pH. At both the 57 taxonomic and functional level, the rhesus macaque vaginal microbiome was most 58 similar to that of women who harbor a diverse vaginal community associated with 59 asymptomatic/symptomatic bacterial vaginosis. Specifically, rhesus macaque vaginal 60 microbiomes harbored a diverse set of anaerobic gram-negative bacteria, including; 61 Snethia, Prevotella, Porphyromonas, and Mobilluncus. Interestingly, some animals were 62 transiently colonized by Lactobacillus and some with Gardnerella. Our in-depth and 63 comprehensive analysis highlights the importance of the model to test interventions for 64 manipulating the vaginal microbiome. 65 bioRxiv preprint doi: https://doi.org/10.1101/2020.12.14.422805; this version posted December 15, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 66 IMPORTANCE 67 It is widely accepted that the “healthy” vaginal microbiome of the majority 68 of women in the developed world is dominated by Lactobacillus species. 69 However, in the developing world, a majority of women are colonized by diverse 70 microbial communities, typically associated with bacterial vaginosis, but remain 71 asymptomatic. Many questions remain about the drivers of this disparity and 72 potential interventions to alter the vaginal microbiome. Rhesus macaques 73 provide an excellent translational model due to significant physiological and 74 genetic homology with humans. In this study, we performed a longitudinal 75 analysis of clinical and microbiome data from a large cohort of reproductive age 76 rhesus macaques. At the taxonomic, genomic, and functional level, the rhesus 77 macaque vaginal microbiome was most similar to that of humans who harbor a 78 diverse vaginal community associated with asymptomatic/symptomatic bacterial 79 vaginosis. Our in-depth and comprehensive analysis highlights the utility of 80 macaques to test interventions for manipulating the vaginal microbiome. 81 82 83 84 85 bioRxiv preprint doi: https://doi.org/10.1101/2020.12.14.422805; this version posted December 15, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 86 INTRODUCTION 87 The vaginal microbial community modulates several critical physiological 88 functions and protect the host from infection with pathogenic organisms. The “healthy” 89 vaginal microbiome (VM) in women in the developed world is typically dominated by 90 Lactobacillus species, with L. crispatis, L. iners, L. johnsonii, and L. gasseri. These 91 microbes are considered keystone microbes that rarely co-occur in individuals (1, 2). 92 Lactobacilli inhibit the growth of other vaginal microbes via the production of lactic acid 93 through fermentation which decreases the pH of the vaginal environment (pH 3.5-5.5) 94 inhibiting the growth of other microbes (3). Lactobacillus species also competitively 95 exclude genitourinary pathogens thereby preventing infection. Disruptions of this 96 community have significant implications for women’s health (4-6). However, 97 approximately ~20% of women in the developed world and ~50% in the developing 98 world harbor a diverse VM with reduced abundance or absence of Lactobacilli and a 99 high abundance of taxa such as Gardnerella, Prevotella, Snethia, and Mobiluncus (1, 4). 100 This diverse community is often associated with a heightened inflammatory state, 101 increased susceptibility to sexually transmitted diseases notably HIV, and the 102 development of bacterial vaginosis (BV) (7). 103 BV is an inflammatory disorder and the most common vaginal infection in the US 104 affecting ~ 30% of women ages 15-44 (8). However, the prevalence of BV can vary 105 widely based on geographic location and racial background (8). BV is caused by 106 bacterial overgrowth, disruption of the commensal microbial community, and a pro- 107 inflammatory environment (9). While typically asymptomatic, BV can result in discomfort 108 and more importantly increased susceptibility to sexually transmitted diseases, preterm 109 birth, and pelvic inflammatory disease (6, 10, 11). The antibiotics Metronidazole and/or bioRxiv preprint doi: https://doi.org/10.1101/2020.12.14.422805; this version posted December 15, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 110 Clindamycin are the current standard treatment for BV. However, BV recurs in ~50% of 111 women within 12 months of antibiotic treatment (12). Additionally, the production of 112 biofilms and the development of other antimicrobial resistance mechanisms will most 113 likely reduce the effectiveness of antibiotics treatments over time (13, 14). Recently, VM 114 transplants have been shown to be effective in the treatment of intractable BV (15). 115 However, microbiome transfer procedures have recently come under scrutiny due to 116 safety concerns (16, 17). 117 Another potential intervention is the use of pre-biotics to shift a microbial 118 community to a more “beneficial” state. Pre-biotics are molecules and/or nutrients that 119 are metabolically accessible to microbes with the goal of enriching for beneficial 120 microbes and/or depleting undesired microbes. An example of such an intervention is 121 the consumption or supplementation of dietary fiber to enrich the gut microbiome in 122 beneficial short-chain fatty acid-producing microbes (18, 19). The use of pre-biotics has 123 also been proposed as a cheap and easily accessible alternative to antibiotic treatment 124 for BV (20, 21). Of interest is the intravaginal application of di- or polysaccharides that 125 are preferentially metabolized and fermented by Lactobacillus to produce lactic acid and 126 hydrogen peroxide, thereby generating a low pH vaginal environment and inhibiting the 127 growth of BV-associated bacteria. Clinical trials are currently underway to test the use of 128 intravaginal Lactose (NTC03878511), Glucose (NCT03357666), and Glycogen 129 (NCT02042287) to treat BV symptoms. Sucrose in particular has shown potential for 130
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