Vaginal microbiomes show ethnic evolutionary dynamics and positive selection of Lactobacillus adhesins driven by a long-term niche-specific process
Xin Wei,
Ming-Shian Tsai,
Liang Liang,
Liuyiqi Jiang,
Chia-Jui Hung,
Laura Jelliffe-Pawlowski,
Larry Rand,
Michael Snyder,
Chao Jiang
Affiliations
Xin Wei
MOE Key Laboratory of Biosystems Homeostasis & Protection, and Zhejiang Provincial Key Laboratory of Cancer Molecular Cell Biology, Life Sciences Institute, Zhejiang University, Hangzhou, Zhejiang 310030, China; State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang 310009, China
Ming-Shian Tsai
Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA
Liang Liang
Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA
Liuyiqi Jiang
MOE Key Laboratory of Biosystems Homeostasis & Protection, and Zhejiang Provincial Key Laboratory of Cancer Molecular Cell Biology, Life Sciences Institute, Zhejiang University, Hangzhou, Zhejiang 310030, China
Chia-Jui Hung
Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA; Department of Biomedical Informatics, Stanford University School of Medicine, Stanford, CA 94305, USA
Laura Jelliffe-Pawlowski
Department of Epidemiology and Biostatistics, School of Medicine, University of California, San Francisco, San Francisco, CA 94158, USA
Larry Rand
Department of Obstetrics, Gynecology & Reproductive Sciences, School of Medicine, University of California, San Francisco, San Francisco, CA 94158, USA; Corresponding author
Michael Snyder
Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA; Corresponding author
Chao Jiang
MOE Key Laboratory of Biosystems Homeostasis & Protection, and Zhejiang Provincial Key Laboratory of Cancer Molecular Cell Biology, Life Sciences Institute, Zhejiang University, Hangzhou, Zhejiang 310030, China; State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang 310009, China; Corresponding author
Summary: The vaginal microbiome’s composition varies among ethnicities. However, the evolutionary landscape of the vaginal microbiome in the multi-ethnic context remains understudied. We perform a systematic evolutionary analysis of 351 vaginal microbiome samples from 35 multi-ethnic pregnant women, in addition to two validation cohorts, totaling 462 samples from 90 women. Microbiome alpha diversity and community state dynamics show strong ethnic signatures. Lactobacillaceae have a higher ratio of non-synonymous to synonymous polymorphism and lower nucleotide diversity than non-Lactobacillaceae in all ethnicities, with a large repertoire of positively selected genes, including the mucin-binding and cell wall anchor genes. These evolutionary dynamics are driven by the long-term evolutionary process unique to the human vaginal niche. Finally, we propose an evolutionary model reflecting the environmental niches of microbes. Our study reveals the extensive ethnic signatures in vaginal microbial ecology and evolution, highlighting the importance of studying the host-microbiome ecosystem from an evolutionary perspective.
