Abstract

Microbial cells in the seabed are thought to persist by slow population turnover rates and extremely low energy requirements. External stimulations such as seafloor hydrocarbon seeps have been demonstrated to significantly boost microbial growth; however, the microbial community response has not been fully understood. Here we report a comparative metagenomic study of microbial response to natural hydrocarbon seeps in the Gulf of Mexico. Subsurface sediments (10–15 cm below seafloor) were collected from five natural seep sites and two reference sites. The resulting metagenome sequencing datasets were analyzed with both gene-based and genome-based approaches. 16S rRNA gene-based analyses suggest that the seep samples are distinct from the references by both 16S rRNA fractional content and phylogeny, with the former dominated by ANME-1 archaea (~50% of total) and Desulfobacterales, and the latter dominated by the Deltaproteobacteria, Planctomycetes, and Chloroflexi phyla. Sulfate-reducing bacteria (SRB) are present in both types of samples, with higher relative abundances in seep samples than the references. Genes for nitrogen fixation were predominantly found in the seep sites, whereas the reference sites showed a dominant signal for anaerobic ammonium oxidation (anammox). We recovered 49 metagenome-assembled genomes and assessed the microbial functional potentials in both types of samples. By this genome-based analysis, the seep samples were dominated by ANME-1 archaea and SRB, with the capacity for methane oxidation coupled to sulfate reduction, which is consistent with the 16S rRNA-gene based characterization. Although ANME-1 archaea and SRB are present in low relative abundances, genome bins from the reference sites are dominated by uncultured members of NC10 and anammox Scalindua, suggesting a prevalence of nitrogen transformations for energy in non-seep pelagic sediments. This study suggests that hydrocarbon seeps can greatly change the microbial community structure by stimulating nitrogen fixation, inherently shifting the nitrogen metabolism compared to those of the reference sediments.

Highlights

  • Abundant microbial cells are found in marine sediments beneath the ocean, accounting for 1/3rd to 1/20th of total microbial biomass on the planet[1]

  • At the site with visible bubble plume, D27 at the center of Seep-1 area, thermogenic gases were detected in the overlying seawater (139 ppm methane, 0.16 ppm ethane, and 0.049 ppm of propane). Based on these geochemical characterizations, we divided these samples into two groups: D27, D33, D24, D72 and D75 are within seep areas influenced by natural liquid and gaseous hydrocarbon seepages, while D21 and D30 serve as references without obvious seepage influences

  • Our study revealed the responses of subseafloor microbial communities to hydrocarbon seepage in deepwater Gulf of Mexico (GOM), by employing both gene- and genome-based analysis of metagenomes

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Summary

Introduction

Abundant microbial cells are found in marine sediments beneath the ocean, accounting for 1/3rd to 1/20th of total microbial biomass on the planet[1]. We focus on the subseafloor sediments to test the hypothesis that the seep-related communities persist at low metabolic rates in the deep sediments and are insensitive to hydrocarbon seepages, as had been previously suggested for GOM sediments[11]. We employ both gene- and genome-based approaches to characterize the microbial community composition and structure, overall metabolic functionality, and inter-dependencies by comparing the metagenomes from seep and reference environments. With our genomic and functional insights into the microbial communities inhabiting the two contrasting geochemical conditions, we see that in addition to microbial cycling of sulfate and methane, nitrogen cycling dynamics must be severely shifted between seep and reference sediments

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