Pressure-Regulated Gene Expression and Enzymatic Activity of the Two Periplasmic Nitrate Reductases in the Deep-Sea Bacterium Shewanella piezotolerans WP3
Shewanella species are widely distributed in marine environments, from the shallow coasts to the deepest sea bottom. Most Shewanella species possess two isoforms of periplasmic nitrate reductases (NAP-α and NAP-β) and are able to generate energy through nitrate reduction. However, the contributions...
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Frontiers Media S.A.
2018-12-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2018.03173/full |
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| author | Xue-Gong Li Xue-Gong Li Wei-Jia Zhang Wei-Jia Zhang Xiang Xiao Xiang Xiao Hua-Hua Jian Ting Jiang Ting Jiang Hong-Zhi Tang Hong-Zhi Tang Xiao-Qing Qi Xiao-Qing Qi Long-Fei Wu Long-Fei Wu |
| author_facet | Xue-Gong Li Xue-Gong Li Wei-Jia Zhang Wei-Jia Zhang Xiang Xiao Xiang Xiao Hua-Hua Jian Ting Jiang Ting Jiang Hong-Zhi Tang Hong-Zhi Tang Xiao-Qing Qi Xiao-Qing Qi Long-Fei Wu Long-Fei Wu |
| author_sort | Xue-Gong Li |
| collection | DOAJ |
| description | Shewanella species are widely distributed in marine environments, from the shallow coasts to the deepest sea bottom. Most Shewanella species possess two isoforms of periplasmic nitrate reductases (NAP-α and NAP-β) and are able to generate energy through nitrate reduction. However, the contributions of the two NAP systems to bacterial deep-sea adaptation remain unclear. In this study, we found that the deep-sea denitrifier Shewanella piezotolerans WP3 was capable of performing nitrate respiration under high hydrostatic pressure (HHP) conditions. In the wild-type strain, NAP-β played a dominant role and was induced by both the substrate and an elevated pressure, whereas NAP-α was constitutively expressed at a relatively lower level. Genetic studies showed that each NAP system alone was sufficient to fully sustain nitrate-dependent growth and that both NAP systems exhibited substrate and pressure inducible expression patterns when the other set was absent. Biochemical assays further demonstrated that NAP-α had a higher tolerance to elevated pressure. Collectively, we report for the first time the distinct properties and contributions of the two NAP systems to nitrate reduction under different pressure conditions. The results will shed light on the mechanisms of bacterial HHP adaptation and nitrogen cycling in the deep-sea environment. |
| first_indexed | 2024-12-12T02:09:21Z |
| format | Article |
| id | doaj.art-20285a1bbe764c51a0edbe91dbb89075 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-12T02:09:21Z |
| publishDate | 2018-12-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-20285a1bbe764c51a0edbe91dbb890752022-12-22T00:41:56ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-12-01910.3389/fmicb.2018.03173430310Pressure-Regulated Gene Expression and Enzymatic Activity of the Two Periplasmic Nitrate Reductases in the Deep-Sea Bacterium Shewanella piezotolerans WP3Xue-Gong Li0Xue-Gong Li1Wei-Jia Zhang2Wei-Jia Zhang3Xiang Xiao4Xiang Xiao5Hua-Hua Jian6Ting Jiang7Ting Jiang8Hong-Zhi Tang9Hong-Zhi Tang10Xiao-Qing Qi11Xiao-Qing Qi12Long-Fei Wu13Long-Fei Wu14Laboratory of Deep Sea Microbial Cell Biology, Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya, ChinaInternational Associated Laboratory of Evolution and Development of Magnetotactic Multicellular Organisms, CNRS-Marseille/CAS, Sanya, ChinaLaboratory of Deep Sea Microbial Cell Biology, Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya, ChinaInternational Associated Laboratory of Evolution and Development of Magnetotactic Multicellular Organisms, CNRS-Marseille/CAS, Sanya, ChinaState Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, ChinaState Key Laboratory of Ocean Engineering, School of Naval Architecture, Ocean and Civil Engineering, Shanghai Jiao Tong University, Shanghai, ChinaState Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, ChinaLaboratory of Deep Sea Microbial Cell Biology, Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya, ChinaUniversity of Chinese Academy of Sciences, Beijing, ChinaLaboratory of Deep Sea Microbial Cell Biology, Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya, ChinaUniversity of Chinese Academy of Sciences, Beijing, ChinaLaboratory of Deep Sea Microbial Cell Biology, Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya, ChinaInternational Associated Laboratory of Evolution and Development of Magnetotactic Multicellular Organisms, CNRS-Marseille/CAS, Sanya, ChinaInternational Associated Laboratory of Evolution and Development of Magnetotactic Multicellular Organisms, CNRS-Marseille/CAS, Sanya, ChinaAix Marseille Université, CNRS, LCB, Marseille, FranceShewanella species are widely distributed in marine environments, from the shallow coasts to the deepest sea bottom. Most Shewanella species possess two isoforms of periplasmic nitrate reductases (NAP-α and NAP-β) and are able to generate energy through nitrate reduction. However, the contributions of the two NAP systems to bacterial deep-sea adaptation remain unclear. In this study, we found that the deep-sea denitrifier Shewanella piezotolerans WP3 was capable of performing nitrate respiration under high hydrostatic pressure (HHP) conditions. In the wild-type strain, NAP-β played a dominant role and was induced by both the substrate and an elevated pressure, whereas NAP-α was constitutively expressed at a relatively lower level. Genetic studies showed that each NAP system alone was sufficient to fully sustain nitrate-dependent growth and that both NAP systems exhibited substrate and pressure inducible expression patterns when the other set was absent. Biochemical assays further demonstrated that NAP-α had a higher tolerance to elevated pressure. Collectively, we report for the first time the distinct properties and contributions of the two NAP systems to nitrate reduction under different pressure conditions. The results will shed light on the mechanisms of bacterial HHP adaptation and nitrogen cycling in the deep-sea environment.https://www.frontiersin.org/article/10.3389/fmicb.2018.03173/fullShewanella piezotolerans WP3nitrate reductionperiplasmic nitrate reductase (NAP)high hydrostatic pressurepiezotolerance |
| spellingShingle | Xue-Gong Li Xue-Gong Li Wei-Jia Zhang Wei-Jia Zhang Xiang Xiao Xiang Xiao Hua-Hua Jian Ting Jiang Ting Jiang Hong-Zhi Tang Hong-Zhi Tang Xiao-Qing Qi Xiao-Qing Qi Long-Fei Wu Long-Fei Wu Pressure-Regulated Gene Expression and Enzymatic Activity of the Two Periplasmic Nitrate Reductases in the Deep-Sea Bacterium Shewanella piezotolerans WP3 Frontiers in Microbiology Shewanella piezotolerans WP3 nitrate reduction periplasmic nitrate reductase (NAP) high hydrostatic pressure piezotolerance |
| title | Pressure-Regulated Gene Expression and Enzymatic Activity of the Two Periplasmic Nitrate Reductases in the Deep-Sea Bacterium Shewanella piezotolerans WP3 |
| title_full | Pressure-Regulated Gene Expression and Enzymatic Activity of the Two Periplasmic Nitrate Reductases in the Deep-Sea Bacterium Shewanella piezotolerans WP3 |
| title_fullStr | Pressure-Regulated Gene Expression and Enzymatic Activity of the Two Periplasmic Nitrate Reductases in the Deep-Sea Bacterium Shewanella piezotolerans WP3 |
| title_full_unstemmed | Pressure-Regulated Gene Expression and Enzymatic Activity of the Two Periplasmic Nitrate Reductases in the Deep-Sea Bacterium Shewanella piezotolerans WP3 |
| title_short | Pressure-Regulated Gene Expression and Enzymatic Activity of the Two Periplasmic Nitrate Reductases in the Deep-Sea Bacterium Shewanella piezotolerans WP3 |
| title_sort | pressure regulated gene expression and enzymatic activity of the two periplasmic nitrate reductases in the deep sea bacterium shewanella piezotolerans wp3 |
| topic | Shewanella piezotolerans WP3 nitrate reduction periplasmic nitrate reductase (NAP) high hydrostatic pressure piezotolerance |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2018.03173/full |
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