Evolutionary ecology of microbial populations inhabiting deep sea sediments associated with cold seeps

Abstract

Deep sea cold seep sediments host abundant and diverse microbial populations that significantly influence biogeochemical cycles. While numerous studies have revealed their community structure and functional capabilities, little is known about genetic heterogeneity within species. Here, we examine intraspecies diversity patterns of 39 abundant species identified in sediment layers down to 430 cm below the sea floor across six cold seep sites. These populations are grouped as aerobic methane-oxidizing bacteria, anaerobic methanotrophic archaea and sulfate-reducing bacteria. Different evolutionary trajectories are observed at the genomic level among these physiologically and phylogenetically diverse populations, with generally low rates of homologous recombination and strong purifying selection. Functional genes related to methane (pmoA and mcrA) and sulfate (dsrA) metabolisms are under strong purifying selection in most species investigated. These genes differ in evolutionary trajectories across phylogenetic clades but are functionally conserved across sites. Intrapopulation diversification of genomes and their mcrA and dsrA genes is depth-dependent and subject to different selection pressure throughout the sediment column redox zones at different sites. These results highlight the interplay between ecological processes and the evolution of key bacteria and archaea in deep sea cold seep extreme environments, shedding light on microbial adaptation in the subseafloor biosphere.

A first report on prokaryotic diversity in northwestern Arafura deep-sea sediments, Indonesia

“…This finding is substantiated by the previous report on archaea diversity studies across the depth above 2000 m in The South China Sea 34 . These depth-dependent differences in microbial taxa may impact their involvement in biogeochemical cycles (e.g., nitrogen, sulfur, and carbon) 35 . This highlights the significant role of deep ocean (> 1000 m) microbes in biogeochemical cycles, prompting further exploration of their advanced functional properties and key genes using techniques such as shotgun metagenomics 36 .…”

Population genetic analyses of longitudinal vaginal microbiome reveal racioethnic evolutionary dynamics and prevailing positive selection ofLactobacillusadhesins

“…Recent studies have observed that most microbial genes generally have low pN/pS and inferred a broad purifying selection of microbial genes in the gut and marine microbiome 18,26,79 . Genes undergoing positive selection are rare in theory, yet they usually play important roles in organismal evolution.…”

“…Recent microbiome studies have increasingly focused on microbiome intraspecific analyses 18–20 . Several SNP-based tools have been developed and applied to metagenomic data from multiple sources, including the gut, vagina, and natural environment 21–26 . Recent studies of the vaginal microbiome have investigated strain diversity, persistence, and vertical inheritance 20,27–29 .…”

Viruses in deep-sea cold seep sediments harbor diverse survival mechanisms and remain genetically conserved within species

“…Cold seeps are deep-sea environments where hydrocarbon fluids and gas seepage occur at the continental margins worldwide. The continuous seepage of gaseous and liquid hydrocarbons boosts local biodiversity and microbial activity, featuring prevalent archaeal anaerobic methanotrophs (ANME) and sulfate-reducing bacteria (SRB) [ 1 , 2 ]. Compared to the rich knowledge of cold seep bacterial and archaeal communities, viruses remain largely underexplored in spite of their significant roles in impacting microbes and corresponding biogeochemical cycles [ 3 , 4 ].…”

“…The principles governing the viral evolution likely differ depending on environmental conditions, such as host dynamics, physicochemical properties, and population sizes [ 25 – 27 ]. Examining 39 abundant microbial species identified in sediment layers below the sea floor and across six cold seep sites, we previously reported that their evolutionary trajectories were depth-dependent and differed across phylogenetic clades [ 1 ]. However, it remains to be answered if cold-seep viruses are undergoing similar evolutionary patterns and selection pressures.…”