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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Format: | Article |
Language: | English |
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Frontiers Media S.A.
2021-02-01
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Series: | Frontiers in Microbiology |
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Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2021.626705/full |
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record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
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 |
work_keys_str_mv |
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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 |