Atribacteria from the Subseafloor Sedimentary Biosphere Disperse to the Hydrosphere through Submarine Mud Volcanoes.

Tatsuhiko Hoshino,Kei Okamura,Tomohiro Toki,Fumio Inagaki,Hideaki Machiyama,Akira Ijiri,Juichiro Ashi,Yuki Morono

doi:10.3389/fmicb.2017.01135

Abstract

Submarine mud volcanoes (SMVs) are formed by muddy sediments and breccias extruded to the seafloor from a source in the deep subseafloor and are characterized by the discharge of methane and other hydrocarbon gasses and deep-sourced fluids into the overlying seawater. Although SMVs act as a natural pipeline connecting the Earth’s surface and subsurface biospheres, the dispersal of deep-biosphere microorganisms and their ecological roles remain largely unknown. In this study, we investigated the microbial communities in sediment and overlying seawater at two SMVs located on the Ryukyu Trench off Tanegashima Island, southern Japan. The microbial communities in mud volcano sediments were generally distinct from those in the overlying seawaters and in the well-stratified Pacific margin sediments collected at the Peru Margin, the Juan de Fuca Ridge flank off Oregon, and offshore of Shimokita Peninsula, northeastern Japan. Nevertheless, in-depth analysis of different taxonomic groups at the sub-species level revealed that the taxon affiliated with Atribacteria, heterotrophic anaerobic bacteria that typically occur in organic-rich anoxic subseafloor sediments, were commonly found not only in SMV sediments but also in the overlying seawater. We designed a new oligonucleotide probe for detecting Atribacteria using the catalyzed reporter deposition-fluorescence in situ hybridization (CARD-FISH). CARD-FISH, digital PCR and sequencing analysis of 16S rRNA genes consistently showed that Atribacteria are abundant in the methane plumes of the two SMVs (0.58 and 1.5 × 104 cells/mL, respectively) but not in surrounding waters, suggesting that microbial cells in subseafloor sediments are dispersed as “deep-biosphere seeds” into the ocean. These findings may have important implications for the microbial transmigration between the deep subseafloor biosphere and the hydrosphere.

Highlights

The subseafloor environment is one of the largest biospheres on Earth, with an estimated total abundance of microorganisms of about 2.9 × 1029 cells, which is equivalent to half of the microbial cells worldwide in the oceans (Kallmeyer et al, 2012)
One of the common predominant microbial taxa frequently found in the marine sediment is Atribacteria including members of JS1 and OP9 which are recently revealed to be monophyletic by phylogenomic analyses of single-cell amplified genome (Nobu et al, 2016)
The depth profiles of sulfate and methane indicate that the sulfate–methane transition zone (SMTZ) was located at around 1 mbsf at both submarine mud volcanoes (SMVs)

Summary

Introduction

The subseafloor environment is one of the largest biospheres on Earth, with an estimated total abundance of microorganisms of about 2.9 × 1029 cells, which is equivalent to half of the microbial cells worldwide in the oceans (Kallmeyer et al, 2012). One of the common predominant microbial taxa frequently found in the marine sediment is Atribacteria including members of JS1 and OP9 which are recently revealed to be monophyletic by phylogenomic analyses of single-cell amplified genome (Nobu et al, 2016). Atribacteria are especially predominant in anaerobic, organic carbon replete, and methane-rich marine sediment. Representatives of this phylum have not been cultivated as yet, several recent studies of single-cell amplified genomes consistently suggested anaerobic heterotrophic metabolism (Carr et al, 2015; Nobu et al, 2016). Atribacteira would control methane production in anaerobic marine sediment by primary or secondary fermentation producing fermentation products as acetate or CO2, that can be used as substrates for methanogen (Carr et al, 2015; Nobu et al, 2016)

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Discussion

Conclusion