Abstract

Methane seeps are among the most productive habitats along continental margins, as anaerobic methane-oxidizing euryarchaeaota and sulfur-metabolizing deltaproteobacteria form the biological base of a dynamic deep-sea ecosystem. The degree of methane seepage therefore represents one important variable in ecosystem dynamics, and the recent discovery of carbonate-hosted endolithic methanotrophy exposes another potentially discriminating factor: physical substrate type. Methanotrophic microbial communities have been detected within diverse seep-associated habitats, including unlithified sediments, protolithic carbonate nodules, and lithified carbonate slabs and chemoherms of distinct mineralogies. However, a systematic assessment of the diversity and community structure associated with these different habitats has been lacking. In this study, microbial aggregate analysis, microbial abundance quantification, mineralogical identification, and archaeal and bacterial 16S rRNA gene clone libraries were used to deconvolve the relationships between seepage activity, substrate type, and microbial community structure. We report prevalent methane-oxidizing archaeal lineages in both active and low-activity seep settings, and a strong community dependence on both seepage activity and substrate type. Statistical treatments of relative taxa abundances indicate that archaeal community structure is more dependent on the degree of methane seepage than physical substrate type; bacterial assemblages appear to be more strongly influenced by the type of colonization substrate than seepage activity. These findings provide a window into the determinants of community structure and function, improving our understanding of potential elemental cycling at seep sites.

Highlights

  • The seafloor is a dynamic and varied environment whose biological communities are dependent upon organic detritus from surface waters and/or chemically reduced fluids emitted from the subseafloor

  • MINERALOGY OF AUTHIGENIC CARBONATES IN THE SEEP ENVIRONMENT X-ray diffraction analysis (XRD) analysis of the 12 samples considered in this study supports four broad categories of mineralogical identification (Figure S1): sediments containing a dominant siliciclastic component identified as quartz (AS-3730, AS-5119, LS-3433, LS-5164, OS-3487, OS-3582); quartz, aragonite, and calcite mixtures (AN-3730N, AN-5119N, LC-5189); aragonitic carbonate rocks (AC-3439, LC-3662); and a dolomitic carbonate (AC-5120)

  • The analysis of mineralogy, microbial abundance, and archaeal and bacterial community structure across a range of habitats within and surrounding marine methane seeps reveals several key findings with implications for microbial ecology and seep development beyond what has been previously reported for marine sediment habitats

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Summary

Introduction

The seafloor is a dynamic and varied environment whose biological communities are dependent upon organic detritus from surface waters and/or chemically reduced fluids emitted from the subseafloor. As the full extent of benthic microbial activity comes into focus, clarifying the identities, distribution, and metabolic roles of constituent organisms in sediments, and endolithic and deeper-seated habitats across a spectrum of energetic regimes, has emerged as a priority. Methane seeps are among the most productive habitats on the sub-photic zone seafloor. In these regions, reduced, methane-rich fluids come into contact with oxidized seawater, fueling chemosynthetic communities such as anaerobic methanotrophic archaea (ANME)/Deltaproteobacteria consortia that mediate the sulfate-coupled anaerobic oxidation of methane (AOM). The metabolic byproducts of methanotrophy support micro- and macrofaunal communities in the seep food web, including sulfide-oxidizing bacteria (Beggiatoa, Thioploca), chemosynthetic clams (Vesicomya), mussels (Bathymodiolus), tube worms (Siboglinidae), and ampharetid polychaetes that serve as visual manifestations of CH4 seepage on the seafloor www.frontiersin.org

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