The unique microbial diversity, community composition and networks of Pacific Islander endocervical and vaginal microbiomes in the presence or absence ofChlamydia trachomatisinfection using metagenomic shotgun sequencing

Abstract

AbstractBackgroundPacific Islanders are a vulnerable population with a high prevalence ofChlamydia trachomatis(Ct) sexually transmitted infections (STIs) and remain underrepresented in research. Here, 258 vaginal and 92 paired endocervical samples from women of diverse ethnicities in Fiji were evaluated using metagenomics to characterize microbial relative abundance, composition and networks including associations withNeisseria gonorrhoeae, human papilloma virus (HPV),Mycoplasma genitalium,Candidaand bacterial vaginosis (BV).ResultsPacific Islander ethnicities and age <25 years were significantly associated withCtinfection. Using VALENCIA, a sub-community state type (subCST) classifier, 93 (36.04%) vaginal and 38 (41.30%) endocervical microbiomes did not match reference subCSTs. Four unique subCSTs were developed to better classify Pacific Islander microbiomes: IV-D0, dominated byGardnerella vaginalis; IV-D1, high/moderateG. vaginalisrelative abundance withPrevotellaspp.; IV-D2, high/moderateG. vaginaliswithLactobacillus iners; and IV-E, moderatePrevotellaspp. Ctpositive endocervical and paired vaginal microbiomes were significantly more likely to have differential species relative abundance (81.58%) thanCtnegative pairs (35.84%; AOR: 7.93; 95% CI: 2.93-21.93;P<0.0001). A significantly higher alpha diversity was found for iTaukei ethnicity, all subCST-IV types, BV, andCtfor vaginal microbiomes. For endocervical microbiomes, higher diversity was significant for subCST-IV-A, subCST-IV-D1, and subCST-IV-E, and high-risk HPV types. Overall, there was a significantly higher diversity for the endocervix in paired microbiomes. Vaginal microbiomes showed significant divergence in community composition as above and forCandida.Endocervical composition varied significantly by subCST type andCtstatus. Gut and BV-associated bacterial clusters were present inCtpositive and negative paired endocervical and vaginal microbiome networks but were smaller with fewer bacterial and noLactobacillusspp. interactions inCt-infected endocervical networks whereG. vaginalisgenerated polymicrobial biofilms along withCtlikely influence pathogenicity.ConclusionsFijian endocervical and vaginal microbiomes represent divergent microbial abundance and compositions, especially for Pacific Islander ethnicities, with distinct subCSTs compared to other global populations. The higher microbial diversity of the endocervix with prevalentG. vaginalis,L. inersandPrevotellaspp. suggest that these microbiomes/networks may predispose to and/or promote chlamydial and HPV pathogenesis. Prospective studies are needed to further define causal associations to develop successful interventions.