Characterization of Sulfurimonas hydrogeniphila sp. nov., a Novel Bacterium Predominant in Deep-Sea Hydrothermal Vents and Comparative Genomic Analyses of the Genus Sulfurimonas

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...

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Main Authors: Shasha Wang, Lijing Jiang, Qitao Hu, Liang Cui, Bitong Zhu, Xiaoteng Fu, Qiliang Lai, Zongze Shao, Suping Yang
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.626705/full
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language English
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author Shasha Wang
Shasha Wang
Shasha Wang
Shasha Wang
Lijing Jiang
Lijing Jiang
Lijing Jiang
Qitao Hu
Qitao Hu
Qitao Hu
Liang Cui
Bitong Zhu
Xiaoteng Fu
Xiaoteng Fu
Xiaoteng Fu
Qiliang Lai
Qiliang Lai
Qiliang Lai
Zongze Shao
Zongze Shao
Zongze Shao
Zongze Shao
Suping Yang
spellingShingle Shasha Wang
Shasha Wang
Shasha Wang
Shasha Wang
Lijing Jiang
Lijing Jiang
Lijing Jiang
Qitao Hu
Qitao Hu
Qitao Hu
Liang Cui
Bitong Zhu
Xiaoteng Fu
Xiaoteng Fu
Xiaoteng Fu
Qiliang Lai
Qiliang Lai
Qiliang Lai
Zongze Shao
Zongze Shao
Zongze Shao
Zongze Shao
Suping Yang
Characterization of Sulfurimonas hydrogeniphila sp. nov., a Novel Bacterium Predominant in Deep-Sea Hydrothermal Vents and Comparative Genomic Analyses of the Genus Sulfurimonas
Frontiers in Microbiology
Sulfurimonas hydrogeniphila
hydrogen oxidation
sulfur oxidation
hydrothermal vent
environmental adaptation
author_facet Shasha Wang
Shasha Wang
Shasha Wang
Shasha Wang
Lijing Jiang
Lijing Jiang
Lijing Jiang
Qitao Hu
Qitao Hu
Qitao Hu
Liang Cui
Bitong Zhu
Xiaoteng Fu
Xiaoteng Fu
Xiaoteng Fu
Qiliang Lai
Qiliang Lai
Qiliang Lai
Zongze Shao
Zongze Shao
Zongze Shao
Zongze Shao
Suping Yang
author_sort Shasha Wang
title Characterization of Sulfurimonas hydrogeniphila sp. nov., a Novel Bacterium Predominant in Deep-Sea Hydrothermal Vents and Comparative Genomic Analyses of the Genus Sulfurimonas
title_short Characterization of Sulfurimonas hydrogeniphila sp. nov., a Novel Bacterium Predominant in Deep-Sea Hydrothermal Vents and Comparative Genomic Analyses of the Genus Sulfurimonas
title_full Characterization of Sulfurimonas hydrogeniphila sp. nov., a Novel Bacterium Predominant in Deep-Sea Hydrothermal Vents and Comparative Genomic Analyses of the Genus Sulfurimonas
title_fullStr Characterization of Sulfurimonas hydrogeniphila sp. nov., a Novel Bacterium Predominant in Deep-Sea Hydrothermal Vents and Comparative Genomic Analyses of the Genus Sulfurimonas
title_full_unstemmed Characterization of Sulfurimonas hydrogeniphila sp. nov., a Novel Bacterium Predominant in Deep-Sea Hydrothermal Vents and Comparative Genomic Analyses of the Genus Sulfurimonas
title_sort characterization of sulfurimonas hydrogeniphila sp. nov., a novel bacterium predominant in deep-sea hydrothermal vents and comparative genomic analyses of the genus sulfurimonas
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2021-02-01
description 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.
topic Sulfurimonas hydrogeniphila
hydrogen oxidation
sulfur oxidation
hydrothermal vent
environmental adaptation
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.626705/full
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spelling doaj-40fa17eeed2047658d9dca89117d7dce2021-02-26T06:06:36ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-02-011210.3389/fmicb.2021.626705626705Characterization of Sulfurimonas hydrogeniphila sp. nov., a Novel Bacterium Predominant in Deep-Sea Hydrothermal Vents and Comparative Genomic Analyses of the Genus SulfurimonasShasha Wang0Shasha Wang1Shasha Wang2Shasha Wang3Lijing Jiang4Lijing Jiang5Lijing Jiang6Qitao Hu7Qitao Hu8Qitao Hu9Liang Cui10Bitong Zhu11Xiaoteng Fu12Xiaoteng Fu13Xiaoteng Fu14Qiliang Lai15Qiliang Lai16Qiliang Lai17Zongze Shao18Zongze Shao19Zongze Shao20Zongze Shao21Suping Yang22Department of Bioengineering and Biotechnology, Huaqiao University, Xiamen, ChinaKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaState Key Laboratory Breeding Base of Marine Genetic Resources, Xiamen, ChinaFujian Key Laboratory of Marine Genetic Resources, Xiamen, ChinaKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaState Key Laboratory Breeding Base of Marine Genetic Resources, Xiamen, ChinaFujian Key Laboratory of Marine Genetic Resources, Xiamen, ChinaKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaState Key Laboratory Breeding Base of Marine Genetic Resources, Xiamen, ChinaFujian Key Laboratory of Marine Genetic Resources, Xiamen, ChinaDepartment of Bioengineering and Biotechnology, Huaqiao University, Xiamen, ChinaDepartment of Bioengineering and Biotechnology, Huaqiao University, Xiamen, ChinaKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaState Key Laboratory Breeding Base of Marine Genetic Resources, Xiamen, ChinaFujian Key Laboratory of Marine Genetic Resources, Xiamen, ChinaKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaState Key Laboratory Breeding Base of Marine Genetic Resources, Xiamen, ChinaFujian Key Laboratory of Marine Genetic Resources, Xiamen, ChinaKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaState Key Laboratory Breeding Base of Marine Genetic Resources, Xiamen, ChinaFujian Key Laboratory of Marine Genetic Resources, Xiamen, ChinaSouthern Marine Science and Engineering Guangdong Laboratory, Zhuhai, ChinaDepartment of Bioengineering and Biotechnology, Huaqiao University, Xiamen, ChinaBacteria 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.https://www.frontiersin.org/articles/10.3389/fmicb.2021.626705/fullSulfurimonas hydrogeniphilahydrogen oxidationsulfur oxidationhydrothermal ventenvironmental adaptation