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

Abstract

Deep sea cold seep sediments host abundant and diverse bacterial and archaeal populations that significantly influence biogeochemical cycles. While numerous studies have revealed the community structure and functional capabilities of cold seep microbiomes, little is known about their genetic heterogeneity within species. Here, we examined intraspecies diversity patterns of 39 abundant species identified in sediment layers down to 4.3 mbsf across six cold seep sites from around the world. These species were predicted to participate in methane oxidation and sulfate reduction, and based on their metabolic capabilities, grouped as aerobic methane-oxidizing bacteria (MOB), anaerobic methanotrophic archaea (ANME) and sulfate-reducing bacteria (SRB). These physiologically and phylogenetically diverse MOB, ANME and SRB display different degrees of intrapopulation sequence divergence and different evolutionary trajectories. Populations were in general characterized by low rates of homologous recombination and strong purifying selection with most of the nucleotide variation being synonymous. Functional genes related to methane (pmoAandmcrA) and sulfate (dsrA) metabolisms were found to be under strong purifying selection in the vast majority of species investigated, although examples of active positive selection were also observed. These genes differed in evolutionary trajectories across phylogenetic clades but are functionally conserved across cold seep sites. Intrapopulation diversification of MOB, ANME and SRB species as well as theirmcrAanddsrAgenes was observed to be depth-dependent and undergo divergent selection pressures throughout the sediment column. These results highlight the role of the interplay between ecological processes and the evolution of key bacteria and archaea in deep sea cold seep sediments and shed light on how microbial populations adapt in the subseafloor biosphere.

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

“…Viral genomes were clustered into 338 species-level viral operational taxonomic units (vOTUs) 38 , belonging to 83 viral clusters (VCs; roughly equivalent to an ICTV genus) utilizing whole genome gene-sharing profiles 39 ( Supplementary Figure 5 and Supplementary Table 6 ). Similar to observations in prokaryotic communities 1, 2, 40 , alpha and beta diversity analyses of 338 vOTUs suggest that sampling site, sediment depth in relation to redox conditions 28 , and the geological state of cold seeps (active or extinct) shape the structure of viral communities ( Supplementary Figure 6 and Supplementary Table 5 ).…”

“…F ST values between viral populations in relation to different sediment samples ranged from zero to 0.89 and were on-average 0.048, with 80% of pairwise fixation indices being zero ( Figure 4c ). These data reflect that cold seep viral populations are genetically conserved and homogeneous contrary to observations of their microbial hosts 1 , suggesting viruses and microbes might undergo different types of environmental selection.…”

“…A total of 2,678 bacterial and archaeal MAGs recovered from 68 previously sequenced cold seep sediments were used to serve as the host reference database 1 . Multiple host prediction strategies were used to link viral genomes to their microbial hosts following our previous method 7 complemented with iPHoP, an automated command-line pipeline for host predictions 72 ( Supplementary Figure 4 ).…”

“…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][26][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.…”