Abstract

Bacteria of the genus Sulfurimonas within the class Campylobacteria are predominant in global deep-sea hydrothermal environments and widespread in global oceans. However, only few bacteria of this group have been isolated, and their adaptations for these extreme environments remain poorly understood. Here, we report a novel mesophilic, hydrogen- and sulfur-oxidizing bacterium, strain NW10T, isolated from a deep-sea sulfide chimney of Northwest Indian Ocean.16S rRNA gene sequence analysis showed that strain NW10T was most closely related to the vent species Sulfurimonas paralvinellae GO25T with 95.8% similarity, but ANI and DDH values between two strains were only 19.20 and 24.70%, respectively, indicating that strain NW10 represents a novel species. Phenotypic characterization showed strain NW10T is an obligate chemolithoautotroph utilizing thiosulfate, sulfide, elemental sulfur, or molecular hydrogen as energy sources, and molecular oxygen, nitrate, or elemental sulfur as electron acceptors. Moreover, hydrogen supported a better growth than reduced sulfur compounds. During thiosulfate oxidation, the strain can produce extracellular sulfur of elemental α-S8 with an unknown mechanism. Polyphasic taxonomy results support that strain NW10T represents a novel species of the genus Sulfurimonas, and named as Sulfurimonas hydrogeniphila sp. nov. Genome analyses revealed its diverse energy metabolisms driving carbon fixation via rTCA cycling, including pathways of sulfur/hydrogen oxidation, coupled oxygen/sulfur respiration and denitrification. Comparative analysis of the 11 available genomes from Sulfurimonas species revealed that vent bacteria, compared to marine non-vent strains, possess unique genes encoding Type V Sqr, Group II, and Coo hydrogenase, and are selectively enriched in genes related to signal transduction and inorganic ion transporters. These phenotypic and genotypic features of vent Sulfurimonas may explain their thriving in hydrothermal environments and help to understand the ecological role of Sulfurimonas bacteria in hydrothermal ecosystems.

Highlights

  • Deep-sea hydrothermal vent is one of the most extreme environments on earth and provides unique and diverse habitats for various microorganisms (Zeng et al, 2020)

  • To obtain Chemolithoautotrophic Sulfur-Oxidizing Bacteria (CSOB) from a newly discovered hydrothermal vent on the Carlsberg Ridge, active vent chimney samples were ground on board and inoculated into sealed bottles filled with MMJHS medium with thiosulfate and hydrogen as the energy sources

  • Strain NW10T represents a novel species named as S. hydrogeniphila, which is abundant (≥1%) in nearly half of deep-sea hydrothermal vent environments globally

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Summary

Introduction

Deep-sea hydrothermal vent is one of the most extreme environments on earth and provides unique and diverse habitats for various microorganisms (Zeng et al, 2020). Biomass production is mainly energized by oxidation of reduced sulfur compounds and hydrogen driving carbon fixation via chemolithoautotrophic microorganisms, which constitute a dominant bacterial group in situ (Nakagawa and Takai, 2008). Among these chemolithoautotrophs, members of the genus Sulfurimonas (class Campylobacteria) represent one of the most widespread and preponderant mesophilic bacteria in global deep-sea hydrothermal environments. Bacteria of this genus play the important role in the biogeochemical cycles of hydrothermal vent systems

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