Genomic and Transcriptomic Resolution of Organic Matter Utilization Among Deep-Sea Bacteria in Guaymas Basin Hydrothermal Plumes.

Meng Li,Gregory J Dick,Sunit Jain

doi:10.3389/fmicb.2016.01125

Abstract

Microbial chemosynthesis within deep-sea hydrothermal vent plumes is a regionally important source of organic carbon to the deep ocean. Although chemolithoautotrophs within hydrothermal plumes have attracted much attention, a gap remains in understanding the fate of organic carbon produced via chemosynthesis. In the present study, we conducted shotgun metagenomic and metatranscriptomic sequencing on samples from deep-sea hydrothermal vent plumes and surrounding background seawaters at Guaymas Basin (GB) in the Gulf of California. De novo assembly of metagenomic reads and binning by tetranucleotide signatures using emergent self-organizing maps (ESOM) revealed 66 partial and nearly complete bacterial genomes. These bacterial genomes belong to 10 different phyla: Actinobacteria, Bacteroidetes, Chloroflexi, Deferribacteres, Firmicutes, Gemmatimonadetes, Nitrospirae, Planctomycetes, Proteobacteria, Verrucomicrobia. Although several major transcriptionally active bacterial groups (Methylococcaceae, Methylomicrobium, SUP05, and SAR324) displayed methanotrophic and chemolithoautotrophic metabolisms, most other bacterial groups contain genes encoding extracellular peptidases and carbohydrate metabolizing enzymes with significantly higher transcripts in the plume than in background, indicating they are involved in degrading organic carbon derived from hydrothermal chemosynthesis. Among the most abundant and active heterotrophic bacteria in deep-sea hydrothermal plumes are Planctomycetes, which accounted for seven genomes with distinct functional and transcriptional activities. The Gemmatimonadetes and Verrucomicrobia also had abundant transcripts involved in organic carbon utilization. These results extend our knowledge of heterotrophic metabolism of bacterial communities in deep-sea hydrothermal plumes.

Highlights

Deep-sea hydrothermal vents are typically distributed along the mid-ocean ridges throughout the world’s oceans, where hot and chemically reduced hydrothermal vent fluids mix with cold and oxidizing seawater, forming hydrothermal plumes that rise 100s of meters off the seafloor and disperse 100s of kilometers from their sources
Metagenomic assembly and binning by tetranucleotide frequencies coupled with coverage and GC content resulted in a total of 74 bacterial genomes (Figure 1; Supplementary Table S2)
For remaining genomes (28 genomes), we used phylogeny of ribosomal protein S3 (Supplementary Figure S1) and the binning of reference genomes to confirm their taxonomic identities (Castelle et al, 2013; Hug et al, 2013). These results indicated that the 66 genomes belong to 10 different bacterial phyla, including Actinobacteria, Bacteroidetes, Chloroflexi, Deferribacteres, Firmicutes, Gemmatimonadetes, Nitrospirae, Planctomycetes, Proteobacteria (Alphaproteobacteria, six genomes; Betaproteobacteria, one genome; Deltaproteobacteria, five genomes; Gammaproteobacteria, 20 genomes), and Verrucomicrobia

Summary

Introduction

Deep-sea hydrothermal vents are typically distributed along the mid-ocean ridges throughout the world’s oceans, where hot and chemically reduced hydrothermal vent fluids mix with cold and oxidizing seawater, forming hydrothermal plumes that rise 100s of meters off the seafloor and disperse 100s of kilometers from their sources The hydrothermal inputs, such as H2S, H2, CH4, NH3, Mn2+ and Fe2+, serve as energy sources that support microbial chemosynthesis (Winn et al, 1986; Deangelis et al, 1993). Two recent studies presented metagenomic and metatranscriptomic evidence that widespread archaea (Li et al, 2015) and Alteromonas bacteria (Baker et al, 2013) play roles in scavenging a variety of organic compounds in the deep sea Another recent study inferred a microbial food web in which chemoautotrophy supports and heterotrophy in hydrothermal plumes at the Mid-Cayman Rise (Bennett et al, 2013). The broader role of bacteria in processing organic carbon in deepsea hydrothermal plumes, both in terms of specific groups and pathways, remains unclear (Dick et al, 2013)

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