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Quantification, Isolation and Characterization of Bifidobacterium from the Vaginal Microbiomes of Reproductive Aged Women

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Quantification, Isolation and Characterization of Bifidobacterium from the Vaginal Microbiomes of Reproductive Aged Women Accepted Manuscript Quantification, isolation and characterization of Bifidobacterium from the vaginal microbiomes of reproductive aged women Aline C. Freitas, Janet E. Hill PII: S1075-9964(17)30112-9 DOI: 10.1016/j.anaerobe.2017.05.012 Reference: YANAE 1743 To appear in: Anaerobe Received Date: 22 March 2017 Revised Date: 23 April 2017 Accepted Date: 22 May 2017 Please cite this article as: Freitas AC, Hill JE, Quantification, isolation and characterization of Bifidobacterium from the vaginal microbiomes of reproductive aged women, Anaerobe (2017), doi: 10.1016/j.anaerobe.2017.05.012. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. ACCEPTED MANUSCRIPT 1 Quantification, isolation and characterization of Bifidobacterium 2 from the vaginal microbiomes of reproductive aged women 3 4 Aline C. Freitas, Janet E. Hill * 5 6 Department of Veterinary Microbiology, University of Saskatchewan, Saskatoon, SK, 7 S7N 5B4, Canada 8 9 E-mail adresses: 10 ACF: [email protected] 11 JEH: [email protected] MANUSCRIPT 12 13 *To whom correspondence should be addressed: 14 Department of Veterinary Microbiology 15 University of Saskatchewan 16 52 Campus Drive 17 Saskatoon,ACCEPTED SK S7N 5B4 18 CANADA 1 ACCEPTED MANUSCRIPT 19 Abstract 20 The vaginal microbiome plays an important role in women’s reproductive health. 21 Imbalances in this microbiota, such as the poorly defined condition of bacterial vaginosis, 22 are associated with increased susceptibility to sexually transmitted infections and 23 negative reproductive outcomes. Currently, a “healthy” vaginal microbiota in 24 reproductive aged women is understood to be dominated by Lactobacillus , although 25 “atypical” microbiomes, such as Bifidobacterium-dominated profiles, have been 26 described. Despite these observations, vaginal bifidobacteria remain relatively poorly 27 characterized, and questions remain regarding their actual abundance in the microbiome. 28 In this study, we used quantitative PCR to confirm the relative abundance of 29 Bifidobacterium in the vaginal microbiomes of healthy reproductive aged women (n=42), 30 previously determined by deep sequencing. We also isolated and phenotypically 31 characterized vaginal bifidobacteria (n=40) in theMANUSCRIPT context of features thought to promote 32 reproductive health. Most isolates were identified as B. breve or B. longum based on 33 cpn 60 barcode sequencing. Fermentation patterns of vaginal bifidobacteria did not differ 34 substantially from corresponding type strains of gut or oral origin. Lactic acid was 35 produced by all vaginal isolates, with B. longum strains producing the highest levels, but 36 only 32% of isolates produced hydrogen peroxide. Most vaginal bifidobacteria were also 37 able to tolerate high levels of lactic acid (100 mM) and low pH (4.5 or 3.9), conditions 38 typical of vaginalACCEPTED fluid of healthy women. Most isolates were resistant to metronidazole 39 but susceptible to clindamycin, the two most common antibiotics used to treat vaginal 40 dysbiosis. These findings demonstrate that Bifidobacterium is the dominant member of 41 some vaginal microbiomes and suggest that bifidobacteria have the potential to be as 2 ACCEPTED MANUSCRIPT 42 protective as lactobacilli according to the current understanding of a healthy vaginal 43 microbiome. 44 45 Keywords: Bifidobacterium , vaginal microbiome, fermentation pattern, hydrogen 46 peroxide, lactic acid, antibiotic 47 48 MANUSCRIPT ACCEPTED 3 ACCEPTED MANUSCRIPT 49 1. Introduction 50 Bifidobacteria were first described by Tissier in 1899, who isolated a bacterium 51 from breast-fed infant feces and named it Bacillus bifidus [1]. In 1924, Orla-Jensen 52 proposed the genus Bifidobacterium as a separate taxon for these organisms [2], which 53 currently includes more than 30 species [3]. Bifidobacteria are Gram-positive, anaerobic, 54 non-motile, non-spore forming rod-shaped bacteria, with varied branching. They belong 55 to the Bifidobacteriaceae family and have high genomic G+C content (55-67 mol%) [3]. 56 Bifidobacteria are known to colonize the human vagina, oral cavity and, more 57 abundantly, the gastrointestinal tract (GIT) [4]. Several studies have shown their 58 influence on human physiology and nutrition [5–9]. In newborns, bifidobacteria play an 59 important role as one of the primary colonizers of the GIT, representing 60 to 91% of 60 fecal bacteria in breast-fed infants [10,11]. This proportion decreases with age and it may 61 represent less than 10% of the adult fecal microbioMANUSCRIPTta [12,13]. Bifidobacteria provide 62 protection from pathogens in the GIT through the production of bacteriocins [7], 63 inhibition of pathogen adhesion [5], and modulation of the immune system [14,15]. Due 64 to these health-promoting effects, bifidobacteria have been extensively studied as 65 probiotics [8,16–18]. 66 Early microbial colonization is an essential process in the maturation of the 67 immune system [19]. This initial colonization may be affected by many factors, such as 68 the mode of ACCEPTEDdelivery (vaginal or caesarean section), feeding type (breast-fed or formula- 69 fed), exposure to antibiotics and hygiene [20]. However, the relative contributions of 70 maternal microbiota (gut, breast milk, vaginal) and environmental sources to the 71 bifidobacteria population of the neonatal gut remain unresolved. 4 ACCEPTED MANUSCRIPT 72 While Bifidobacterium spp. present in the gut are well described, vaginal 73 bifidobacteria remain relatively poorly characterized, and it is not known if vaginal 74 adaptation has resulted in distinct phenotypic features that distinguish them from gut 75 populations. Although a healthy vaginal microbiota is defined as Lactobacillus - 76 dominated, several studies have identified vaginal Bifidobacterium -dominated profiles in 77 5-10% of healthy, reproductive aged women [21–24]. Furthermore, vaginal bifidobacteria 78 are reported to produce lactic acid and hydrogen peroxide; attributes of vaginal 79 lactobacilli credited with maintaining homeostasis in the vaginal microbiome [25]. 80 Culture-independent techniques are useful tools in microbiome characterization, 81 but methods based on amplification and sequencing of 16S rRNA genes, have been 82 reported to underrepresent Bifidobacterium in microbial communities [26]. The 83 abundance of Bifidobacterium in the vaginal microbiota may also be underestimated due 84 to the similarity of their 16S rRNA sequencesMANUSCRIPT to those of Gardnerella vaginalis. G. 85 vaginalis is also a member of the Bifidobacteriaceae family and is a commonly detected 86 microorganism associated with bacterial vaginosis (BV) [27]. The use of the cpn 60 87 “universal target” (UT) region as a barcode for microbiome profiling results in better 88 resolution of closely related species, including those within Bifidobacteriaceae [28], and 89 cpn 60 based human fecal microbiome profiles have been shown to more accurately 90 represent Bifidobacterium content than a 16S rRNA based approach [26]. Previous 91 studies of the vaginal microbiome [21] or synthetic mixtures of vaginal organisms [29] 92 have demonstratedACCEPTED a strong correlation between cpn 60 sequence read abundance and 93 organism abundance determined by quantitative PCR. However, regardless of the target 94 used, relative abundance of specific organisms within complex communities may not be 5 ACCEPTED MANUSCRIPT 95 represented accurately by methods that rely on polymerase chain reaction (PCR) 96 amplification and its inherent biases. 97 Considering the lack of information about Bifidobacterium spp. of vaginal origin, 98 their importance as a potential source for the neonatal gut microbiome, and their potential 99 health-promoting effects in the vagina, a better understanding of the properties of vaginal 100 bifidobacteria is needed. In this study, our main objectives were: 1) to apply species- 101 specific quantitative PCR to confirm the relative abundance of Bifidobacterium in the 102 vaginal microbiomes of reproductive aged women previously determined based on cpn 60 103 barcode sequencing, and 2) to characterize vaginal Bifidobacterium isolates based on 104 carbohydrate fermentation patterns, hydrogen peroxide production, lactic acid 105 production, resistance to low pH and lactic acid, and susceptibility to antibiotics. 106 MANUSCRIPT 107 2. Material and Methods 108 2.1 Samples and microbiome profiles 109 Vaginal microbiome profiles from 492 healthy women were previously published 110 by our research group [30,31]. Profiles were created by PCR amplification and deep 111 sequencing of the cpn 60 UT region. Total bacterial load in each sample was also 112 estimated as part of these studies using a SYBR Green assay based on the amplification 113 of the V3 region of the 16S rRNA gene. The remaining vaginal swabs and DNA extracts 114 from these studies,ACCEPTED archived at -80 ˚C, were available for use in the current study. 6 ACCEPTED MANUSCRIPT 115 2.2 Bifidobacterium quantitative PCR assays 116 Sequences with similarity to Bifidobacterium breve, Bifidobacterium dentium and 117 Alloscardovia omnicolens (Bifidobacteriaceae family) that
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