Characterization of two novel chemolithoautotrophic bacteria of Sulfurovum from marine coastal environments and further comparative genomic analyses revealed species differentiation among deep-sea hydrothermal vent and non-vent origins
Bacteria of the genus Sulfurovum within the class Campylobacteria are widespread in global oceans and are predominant in sulfide-rich environments. However, little is known about their adaptation to such harsh environments owing to their resistance to cultivation. In this study, we obtained three pu...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-08-01
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| Series: | Frontiers in Marine Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmars.2023.1222526/full |
| _version_ | 1797744827396259840 |
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| author | Jun Wang Jun Wang Jun Wang Jun Wang Qiang Zheng Shasha Wang Shasha Wang Shasha Wang Jialing Zeng Qing Yuan Qing Yuan Qing Yuan Yangsheng Zhong Yangsheng Zhong Yangsheng Zhong Lijing Jiang Lijing Jiang Lijing Jiang Lijing Jiang Zongze Shao Zongze Shao Zongze Shao Zongze Shao |
| author_facet | Jun Wang Jun Wang Jun Wang Jun Wang Qiang Zheng Shasha Wang Shasha Wang Shasha Wang Jialing Zeng Qing Yuan Qing Yuan Qing Yuan Yangsheng Zhong Yangsheng Zhong Yangsheng Zhong Lijing Jiang Lijing Jiang Lijing Jiang Lijing Jiang Zongze Shao Zongze Shao Zongze Shao Zongze Shao |
| author_sort | Jun Wang |
| collection | DOAJ |
| description | Bacteria of the genus Sulfurovum within the class Campylobacteria are widespread in global oceans and are predominant in sulfide-rich environments. However, little is known about their adaptation to such harsh environments owing to their resistance to cultivation. In this study, we obtained three pure cultures of this genus from marine coastal environments and compared them with those obtained from the deep sea. Phylogenetic analysis of 16S rRNA gene sequences indicated that they represent two novel species of the genus, sharing 95.9%–96.1% sequence similarities to Sulfurovum aggregans Monchim33T. Based on the polyphasic classification results, the type strains XTW-4T and zt1-1T were proposed to represent two new species: Sulfurovum xiamenensis sp. nov. and Sulfurovum zhangzhouensis sp. nov., respectively. These coastal isolates were also obligate chemoautotrophs featuring molecular hydrogen as an electron donor and molecular oxygen, thiosulfate, or elemental sulfur as the sole electron acceptor. Comparative genomic analyses based on 11 Sulfurovum species further revealed a clear differentiation between hydrothermal vent and non-vent origins. The non-vent Sulfurovum can use thiosulfate as an electron acceptor but lacks denitrification pathways, whereas the vent bacteria can respire nitrate through complete denitrification pathways. Moreover, the non-vent Sulfurovum contained a nitrogen fixation pathway, implying their adaptation to nitrogen source-deficit niches. In addition, non-vent Sulfurovum species adapted to a higher oxygen concentration via multiple antioxidative defense mechanisms. These phenotypic and genotypic features help us to understand the ecological role of Sulfurovum bacteria in marine ecosystems. |
| first_indexed | 2024-03-12T15:14:50Z |
| format | Article |
| id | doaj.art-3eaa59720c8b43539b42a6386e2c8b90 |
| institution | Directory Open Access Journal |
| issn | 2296-7745 |
| language | English |
| last_indexed | 2024-03-12T15:14:50Z |
| publishDate | 2023-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Marine Science |
| spelling | doaj.art-3eaa59720c8b43539b42a6386e2c8b902023-08-11T15:03:12ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452023-08-011010.3389/fmars.2023.12225261222526Characterization of two novel chemolithoautotrophic bacteria of Sulfurovum from marine coastal environments and further comparative genomic analyses revealed species differentiation among deep-sea hydrothermal vent and non-vent originsJun Wang0Jun Wang1Jun Wang2Jun Wang3Qiang Zheng4Shasha Wang5Shasha Wang6Shasha Wang7Jialing Zeng8Qing Yuan9Qing Yuan10Qing Yuan11Yangsheng Zhong12Yangsheng Zhong13Yangsheng Zhong14Lijing Jiang15Lijing Jiang16Lijing Jiang17Lijing Jiang18Zongze Shao19Zongze Shao20Zongze Shao21Zongze Shao22Key Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources of China, Xiamen, ChinaState Key Laboratory for Marine Environmental Science, Institute of Marine Microbes and Ecospheres, College of Ocean and Earth Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory Breeding Base of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaKey Laboratory of Marine Genetic Resources of Fujian Province, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaState Key Laboratory for Marine Environmental Science, Institute of Marine Microbes and Ecospheres, College of Ocean and Earth Sciences, Xiamen University, Xiamen, ChinaKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources of China, Xiamen, ChinaState Key Laboratory Breeding Base of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaKey Laboratory of Marine Genetic Resources of Fujian Province, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaState Key Laboratory for Marine Environmental Science, Institute of Marine Microbes and Ecospheres, College of Ocean and Earth Sciences, Xiamen University, Xiamen, ChinaKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources of China, Xiamen, ChinaState Key Laboratory Breeding Base of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaKey Laboratory of Marine Genetic Resources of Fujian Province, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources of China, Xiamen, ChinaState Key Laboratory Breeding Base of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaKey Laboratory of Marine Genetic Resources of Fujian Province, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources of China, Xiamen, ChinaState Key Laboratory Breeding Base of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaKey Laboratory of Marine Genetic Resources of Fujian Province, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaSchool of Marine Biology, Xiamen Ocean Vocational College, Xiamen, ChinaKey Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources of China, Xiamen, ChinaState Key Laboratory for Marine Environmental Science, Institute of Marine Microbes and Ecospheres, College of Ocean and Earth Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory Breeding Base of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaKey Laboratory of Marine Genetic Resources of Fujian Province, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaBacteria of the genus Sulfurovum within the class Campylobacteria are widespread in global oceans and are predominant in sulfide-rich environments. However, little is known about their adaptation to such harsh environments owing to their resistance to cultivation. In this study, we obtained three pure cultures of this genus from marine coastal environments and compared them with those obtained from the deep sea. Phylogenetic analysis of 16S rRNA gene sequences indicated that they represent two novel species of the genus, sharing 95.9%–96.1% sequence similarities to Sulfurovum aggregans Monchim33T. Based on the polyphasic classification results, the type strains XTW-4T and zt1-1T were proposed to represent two new species: Sulfurovum xiamenensis sp. nov. and Sulfurovum zhangzhouensis sp. nov., respectively. These coastal isolates were also obligate chemoautotrophs featuring molecular hydrogen as an electron donor and molecular oxygen, thiosulfate, or elemental sulfur as the sole electron acceptor. Comparative genomic analyses based on 11 Sulfurovum species further revealed a clear differentiation between hydrothermal vent and non-vent origins. The non-vent Sulfurovum can use thiosulfate as an electron acceptor but lacks denitrification pathways, whereas the vent bacteria can respire nitrate through complete denitrification pathways. Moreover, the non-vent Sulfurovum contained a nitrogen fixation pathway, implying their adaptation to nitrogen source-deficit niches. In addition, non-vent Sulfurovum species adapted to a higher oxygen concentration via multiple antioxidative defense mechanisms. These phenotypic and genotypic features help us to understand the ecological role of Sulfurovum bacteria in marine ecosystems.https://www.frontiersin.org/articles/10.3389/fmars.2023.1222526/fullSulfurovum xiamenensisSulfurovum zhangzhouensisnitrogen fixationcoastal environmenthydrothermal ventenvironmental adaptation |
| spellingShingle | Jun Wang Jun Wang Jun Wang Jun Wang Qiang Zheng Shasha Wang Shasha Wang Shasha Wang Jialing Zeng Qing Yuan Qing Yuan Qing Yuan Yangsheng Zhong Yangsheng Zhong Yangsheng Zhong Lijing Jiang Lijing Jiang Lijing Jiang Lijing Jiang Zongze Shao Zongze Shao Zongze Shao Zongze Shao Characterization of two novel chemolithoautotrophic bacteria of Sulfurovum from marine coastal environments and further comparative genomic analyses revealed species differentiation among deep-sea hydrothermal vent and non-vent origins Frontiers in Marine Science Sulfurovum xiamenensis Sulfurovum zhangzhouensis nitrogen fixation coastal environment hydrothermal vent environmental adaptation |
| title | Characterization of two novel chemolithoautotrophic bacteria of Sulfurovum from marine coastal environments and further comparative genomic analyses revealed species differentiation among deep-sea hydrothermal vent and non-vent origins |
| title_full | Characterization of two novel chemolithoautotrophic bacteria of Sulfurovum from marine coastal environments and further comparative genomic analyses revealed species differentiation among deep-sea hydrothermal vent and non-vent origins |
| title_fullStr | Characterization of two novel chemolithoautotrophic bacteria of Sulfurovum from marine coastal environments and further comparative genomic analyses revealed species differentiation among deep-sea hydrothermal vent and non-vent origins |
| title_full_unstemmed | Characterization of two novel chemolithoautotrophic bacteria of Sulfurovum from marine coastal environments and further comparative genomic analyses revealed species differentiation among deep-sea hydrothermal vent and non-vent origins |
| title_short | Characterization of two novel chemolithoautotrophic bacteria of Sulfurovum from marine coastal environments and further comparative genomic analyses revealed species differentiation among deep-sea hydrothermal vent and non-vent origins |
| title_sort | characterization of two novel chemolithoautotrophic bacteria of sulfurovum from marine coastal environments and further comparative genomic analyses revealed species differentiation among deep sea hydrothermal vent and non vent origins |
| topic | Sulfurovum xiamenensis Sulfurovum zhangzhouensis nitrogen fixation coastal environment hydrothermal vent environmental adaptation |
| url | https://www.frontiersin.org/articles/10.3389/fmars.2023.1222526/full |
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