The Transcriptome of Bathymodiolus azoricus Gill Reveals Expression of Genes from Endosymbionts and Free-Living Deep-Sea Bacteria

Conceição Egas,Miguel Pinheiro,Raul Bettencourt,Cristina Barroso,Paula Gomes

doi:10.3390/md10081765

Abstract

Deep-sea environments are largely unexplored habitats where a surprising number of species may be found in large communities, thriving regardless of the darkness, extreme cold, and high pressure. Their unique geochemical features result in reducing environments rich in methane and sulfides, sustaining complex chemosynthetic ecosystems that represent one of the most surprising findings in oceans in the last 40 years. The deep-sea Lucky Strike hydrothermal vent field, located in the Mid Atlantic Ridge, is home to large vent mussel communities where Bathymodiolus azoricus represents the dominant faunal biomass, owing its survival to symbiotic associations with methylotrophic or methanotrophic and thiotrophic bacteria. The recent transcriptome sequencing and analysis of gill tissues from B. azoricus revealed a number of genes of bacterial origin, hereby analyzed to provide a functional insight into the gill microbial community. The transcripts supported a metabolically active microbiome and a variety of mechanisms and pathways, evidencing also the sulfur and methane metabolisms. Taxonomic affiliation of transcripts and 16S rRNA community profiling revealed a microbial community dominated by thiotrophic and methanotrophic endosymbionts of B. azoricus and the presence of a Sulfurovum-like epsilonbacterium.

Highlights

Life in extreme marine environments is highly diverse, as illustrated by deep-sea hydrothermal vents
The mussel Bathymodiolus azoricus is the dominant animal at Mid-Atlantic Ridge deep-sea hydrothermal vents, owing its high biomass to the functional dependence on its symbiotic association with both sulfur-oxidizing and methanotrophic bacteria [2,3,6,7]
Search analysis of DeepSeaVent, the B. azoricus gill tissue transcriptome database, revealed the presence of genes matching bacteria phylotypes among the mussel gill transcripts [17]. To understand if these transcripts could represent a bacterial fingerprint in the mussel gill tissues, we searched for transcripts with a BLASTx hit matching the superkingdom Bacteria, and retrieved 3522 contigs [17]

Summary

Introduction

Life in extreme marine environments is highly diverse, as illustrated by deep-sea hydrothermal vents. Much of the survival success of the invertebrates thriving in these environments relies on the establishment of symbiotic associations with chemoautotrophic bacteria, from which they receive most of their nutrition, whereas the bacteria likely benefit from a protected and stable physical and chemical environment, favorable for carbon fixation [4] Such symbioses are commonly found among various invertebrate phyla, in bivalve mollusks inhabiting hydrothermal vents, cold seeps, and other suboxic sediments [5], and are structurally supported by specialized organs or tissues harboring methanotrophic, thiotrophic or both bacteria. The mussel Bathymodiolus azoricus is the dominant animal at Mid-Atlantic Ridge deep-sea hydrothermal vents, owing its high biomass to the functional dependence on its symbiotic association with both sulfur-oxidizing and methanotrophic bacteria [2,3,6,7] Such a dual symbiosis is hosted in the bacteriocytes, and may provide the bulk of the host’s nutritional carbon requirement [6,8]. Such mixotrophy provides substantial nutritional advantage to the mussel, allowing it to obtain energy from both sulfide and methane at the vent sites, and from particulate organic matter [10]

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