Abstract

BackgroundThe most widespread bacteria in oxic zones of carbonate chimneys at the serpentinite-hosted Lost City hydrothermal field, Mid-Atlantic Ridge, belong to the Thiomicrospira group of sulfur-oxidizing chemolithoautotrophs. It is unclear why Thiomicrospira-like organisms thrive in these chimneys considering that Lost City hydrothermal fluids are notably lacking in hydrogen sulfide and carbon dioxide.Methodology/Principal FindingsHere we describe metagenomic sequences obtained from a Lost City carbonate chimney that are highly similar to the genome of Thiomicrospira crunogena XCL-2, an isolate from a basalt-hosted hydrothermal vent in the Pacific Ocean. Even though T. crunogena and Lost City Thiomicrospira inhabit different types of hydrothermal systems in different oceans, their genomic contents are highly similar. For example, sequences encoding the sulfur oxidation and carbon fixation pathways (including a carbon concentration mechanism) of T. crunogena are also present in the Lost City metagenome. Comparative genomic analyses also revealed substantial genomic changes that must have occurred since the divergence of the two lineages, including large genomic rearrangements, gene fusion events, a prophage insertion, and transposase activity.Conclusions/SignificanceOur results show significant genomic similarity between Thiomicrospira organisms inhabiting different kinds of hydrothermal systems in different oceans, suggesting that these organisms are widespread and highly adaptable. These data also indicate genomic processes potentially associated with the adaptation of these lineages into strikingly different habitats.

Highlights

  • Microbial oxidation of sulfur is the basis of most ecosystems at seafloor hydrothermal environments

  • Almost all of the large contigs contained open reading frames with significant sequence similarity to a Thiomicrospira crunogena XCL-2 protein, indicating that Thiomicrospira-related sequences comprise a high proportion of the metagenomic assembly (Figure 2)

  • Despite inhabiting different types of hydrothermal systems in different oceans, both Thiomicrospira representatives share genes encoding functions that appear to be crucial for thriving in Lost City carbonate chimneys: the ability to aerobically oxidize reduced sulfur species and to concentrate CO2 intracellularly

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Summary

Introduction

Microbial oxidation of sulfur is the basis of most ecosystems at seafloor hydrothermal environments. At the serpentinite-hosted Lost City hydrothermal field in the Atlantic Ocean, H2S concentrations are lower [2], ranging between 0.05–2.8 mmol/kg in end-member hydrothermal fluids [3]. Megafaunal biomass is much lower at Lost City compared to most basalt-hosted systems, and the relative lack of H2S is the most likely cause [2]. The most widespread bacteria in oxic zones of carbonate chimneys at the serpentinite-hosted Lost City hydrothermal field, Mid-Atlantic Ridge, belong to the Thiomicrospira group of sulfur-oxidizing chemolithoautotrophs. It is unclear why Thiomicrospira-like organisms thrive in these chimneys considering that Lost City hydrothermal fluids are notably lacking in hydrogen sulfide and carbon dioxide

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