Metagenomic Shotgun Sequencing of Endocervical, Vaginal, and Rectal Samples among Fijian Women with and without Chlamydia trachomatis Reveals Disparate Microbial Populations and Function across Anatomic Sites: a Pilot Study

ABSTRACT Chlamydia trachomatis is a sexually transmitted pathogen and a global public health concern. Little is known about the microbial composition and function across endocervical, vaginal, and rectal microbiomes in the context of C. trachomatis infection. We evaluated the microbiomes of 10 age-m...

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Main Authors: Sankhya Bommana, Gracie Richards, Mike Kama, Reshma Kodimerla, Kenan Jijakli, Timothy D. Read, Deborah Dean
Format: Article
Language:English
Published: American Society for Microbiology 2022-06-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.00105-22
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author Sankhya Bommana
Gracie Richards
Mike Kama
Reshma Kodimerla
Kenan Jijakli
Timothy D. Read
Deborah Dean
author_facet Sankhya Bommana
Gracie Richards
Mike Kama
Reshma Kodimerla
Kenan Jijakli
Timothy D. Read
Deborah Dean
author_sort Sankhya Bommana
collection DOAJ
description ABSTRACT Chlamydia trachomatis is a sexually transmitted pathogen and a global public health concern. Little is known about the microbial composition and function across endocervical, vaginal, and rectal microbiomes in the context of C. trachomatis infection. We evaluated the microbiomes of 10 age-matched high-risk Fijian women with and without C. trachomatis using metagenomic shotgun sequencing (MSS). Lactobacillus iners and Lactobacillus crispatus dominated the vagina and endocervix of uninfected women. Species often found in higher relative abundance in bacterial vaginosis (BV)—Mageeibacillus indolicus, Prevotella spp., Sneathia spp., Gardnerella vaginalis, and Veillonellaceae spp.—were dominant in C. trachomatis-infected women. This combination of BV pathogens was unique to Pacific Islanders compared to previously studied groups. The C. trachomatis-infected endocervix had a higher diversity of microbiota and microbial profiles that were somewhat different from those of the vagina. However, community state type III (CST-III) and CST-IV predominated, reflecting pathogenic microbiota regardless of C. trachomatis infection status. Rectal microbiomes were dominated by Prevotella and Bacteroides, although four women had unique microbiomes with Gardnerella, Akkermansia, Bifidobacterium, and Brachyspira. A high level of microbial similarity across microbiomes in two C. trachomatis-infected women suggested intragenitorectal transmission. A number of metabolic pathways in the endocervix, driven by BV pathogens and C. trachomatis to meet nutritional requirements for survival/growth, 5-fold higher than that in the vagina indicated that endocervical microbial functions are likely more diverse and complex than those in the vagina. Our novel findings provide the impetus for larger prospective studies to interrogate microbial/microbiome interactions that promote C. trachomatis infection and better define the unique genitorectal microbiomes of Pacific Islanders. IMPORTANCE Chlamydia trachomatis is the primary cause of bacterial sexually transmitted infections worldwide, with a disturbing increase in annual rates. While there is a plethora of data on healthy and pathogenic vaginal microbiomes—defining microbial profiles and associations with sexually transmitted infections (STIs)—far fewer studies have similarly examined the endocervix or rectum. Further, vulnerable populations, such as Pacific Islanders, remain underrepresented in research. We investigated the microbial composition, structure, and function of these anatomic microbiomes using metagenomic shotgun sequencing among a Fijian cohort. We found, primarily among C. trachomatis-infected women, unique microbial profiles in endocervical, vaginal, and rectal microbiomes with an increased diversity and more complex microbial pathways in endocervical than vaginal microbiomes. Similarities in microbiome composition across sites for some women suggested intragenitorectal transmission. These novel insights into genitorectal microbiomes and their purported function require prospective studies to better define Pacific Islander microbiomes and microbial/microbiome interactions that promote C. trachomatis infection.
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spelling doaj.art-77027f61f1f94645bab76b2f046683872022-12-22T00:17:51ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-06-0110310.1128/spectrum.00105-22Metagenomic Shotgun Sequencing of Endocervical, Vaginal, and Rectal Samples among Fijian Women with and without Chlamydia trachomatis Reveals Disparate Microbial Populations and Function across Anatomic Sites: a Pilot StudySankhya Bommana0Gracie Richards1Mike Kama2Reshma Kodimerla3Kenan Jijakli4Timothy D. Read5Deborah Dean6Department of Pediatrics, University of California San Francisco, Oakland, California, USADepartment of Pediatrics, University of California San Francisco, Oakland, California, USAMinistry of Health and Medical Services, Suva, FijiDepartment of Pediatrics, University of California San Francisco, Oakland, California, USADepartment of Medicine, Emory University School of Medicine, Atlanta, Georgia, USADepartment of Medicine, Emory University School of Medicine, Atlanta, Georgia, USADepartment of Pediatrics, University of California San Francisco, Oakland, California, USAABSTRACT Chlamydia trachomatis is a sexually transmitted pathogen and a global public health concern. Little is known about the microbial composition and function across endocervical, vaginal, and rectal microbiomes in the context of C. trachomatis infection. We evaluated the microbiomes of 10 age-matched high-risk Fijian women with and without C. trachomatis using metagenomic shotgun sequencing (MSS). Lactobacillus iners and Lactobacillus crispatus dominated the vagina and endocervix of uninfected women. Species often found in higher relative abundance in bacterial vaginosis (BV)—Mageeibacillus indolicus, Prevotella spp., Sneathia spp., Gardnerella vaginalis, and Veillonellaceae spp.—were dominant in C. trachomatis-infected women. This combination of BV pathogens was unique to Pacific Islanders compared to previously studied groups. The C. trachomatis-infected endocervix had a higher diversity of microbiota and microbial profiles that were somewhat different from those of the vagina. However, community state type III (CST-III) and CST-IV predominated, reflecting pathogenic microbiota regardless of C. trachomatis infection status. Rectal microbiomes were dominated by Prevotella and Bacteroides, although four women had unique microbiomes with Gardnerella, Akkermansia, Bifidobacterium, and Brachyspira. A high level of microbial similarity across microbiomes in two C. trachomatis-infected women suggested intragenitorectal transmission. A number of metabolic pathways in the endocervix, driven by BV pathogens and C. trachomatis to meet nutritional requirements for survival/growth, 5-fold higher than that in the vagina indicated that endocervical microbial functions are likely more diverse and complex than those in the vagina. Our novel findings provide the impetus for larger prospective studies to interrogate microbial/microbiome interactions that promote C. trachomatis infection and better define the unique genitorectal microbiomes of Pacific Islanders. IMPORTANCE Chlamydia trachomatis is the primary cause of bacterial sexually transmitted infections worldwide, with a disturbing increase in annual rates. While there is a plethora of data on healthy and pathogenic vaginal microbiomes—defining microbial profiles and associations with sexually transmitted infections (STIs)—far fewer studies have similarly examined the endocervix or rectum. Further, vulnerable populations, such as Pacific Islanders, remain underrepresented in research. We investigated the microbial composition, structure, and function of these anatomic microbiomes using metagenomic shotgun sequencing among a Fijian cohort. We found, primarily among C. trachomatis-infected women, unique microbial profiles in endocervical, vaginal, and rectal microbiomes with an increased diversity and more complex microbial pathways in endocervical than vaginal microbiomes. Similarities in microbiome composition across sites for some women suggested intragenitorectal transmission. These novel insights into genitorectal microbiomes and their purported function require prospective studies to better define Pacific Islander microbiomes and microbial/microbiome interactions that promote C. trachomatis infection.https://journals.asm.org/doi/10.1128/spectrum.00105-22Chlamydia trachomatisendocervical microbiomemetabolomicsmetagenomic shotgun sequencingrectal microbiomesexually transmitted infections
spellingShingle Sankhya Bommana
Gracie Richards
Mike Kama
Reshma Kodimerla
Kenan Jijakli
Timothy D. Read
Deborah Dean
Metagenomic Shotgun Sequencing of Endocervical, Vaginal, and Rectal Samples among Fijian Women with and without Chlamydia trachomatis Reveals Disparate Microbial Populations and Function across Anatomic Sites: a Pilot Study
Microbiology Spectrum
Chlamydia trachomatis
endocervical microbiome
metabolomics
metagenomic shotgun sequencing
rectal microbiome
sexually transmitted infections
title Metagenomic Shotgun Sequencing of Endocervical, Vaginal, and Rectal Samples among Fijian Women with and without Chlamydia trachomatis Reveals Disparate Microbial Populations and Function across Anatomic Sites: a Pilot Study
title_full Metagenomic Shotgun Sequencing of Endocervical, Vaginal, and Rectal Samples among Fijian Women with and without Chlamydia trachomatis Reveals Disparate Microbial Populations and Function across Anatomic Sites: a Pilot Study
title_fullStr Metagenomic Shotgun Sequencing of Endocervical, Vaginal, and Rectal Samples among Fijian Women with and without Chlamydia trachomatis Reveals Disparate Microbial Populations and Function across Anatomic Sites: a Pilot Study
title_full_unstemmed Metagenomic Shotgun Sequencing of Endocervical, Vaginal, and Rectal Samples among Fijian Women with and without Chlamydia trachomatis Reveals Disparate Microbial Populations and Function across Anatomic Sites: a Pilot Study
title_short Metagenomic Shotgun Sequencing of Endocervical, Vaginal, and Rectal Samples among Fijian Women with and without Chlamydia trachomatis Reveals Disparate Microbial Populations and Function across Anatomic Sites: a Pilot Study
title_sort metagenomic shotgun sequencing of endocervical vaginal and rectal samples among fijian women with and without chlamydia trachomatis reveals disparate microbial populations and function across anatomic sites a pilot study
topic Chlamydia trachomatis
endocervical microbiome
metabolomics
metagenomic shotgun sequencing
rectal microbiome
sexually transmitted infections
url https://journals.asm.org/doi/10.1128/spectrum.00105-22
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