Genomic insights into the alphaproteobacterium Georhizobium sp. MAB10 revealed a pathway of Mn(II) oxidation-coupled anoxygenic photoautotrophy: a novel understanding of the biotic process in deep-sea ferromanganese nodule formation
ABSTRACT Under light conditions, Mn(II) facilitates the photoautotrophic growth of Georhizobium sp. MAB10, a strain derived from deep-sea ferromanganese nodules, along with the generation of dark Mn oxides (β-MnO2). This study investigated the genetic basis of Mn(II) oxidation-coupled anoxygenic pho...
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American Society for Microbiology
2025-01-01
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| Online Access: | https://journals.asm.org/doi/10.1128/mbio.02675-24 |
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| author | Xiuli Xu Litao Zhang Fuhang Song Guoliang Zhang Linlin Ma Na Yang |
| author_facet | Xiuli Xu Litao Zhang Fuhang Song Guoliang Zhang Linlin Ma Na Yang |
| author_sort | Xiuli Xu |
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| description | ABSTRACT Under light conditions, Mn(II) facilitates the photoautotrophic growth of Georhizobium sp. MAB10, a strain derived from deep-sea ferromanganese nodules, along with the generation of dark Mn oxides (β-MnO2). This study investigated the genetic basis of Mn(II) oxidation-coupled anoxygenic photoautotrophy using genome sequencing and biochemical assays of strain MAB10. Preliminary results indicated the presence of genes encoding a functional pheophytin-quinone-type photosynthetic reaction center and a putative key enzyme for Mn(II) oxidation, namely FtsP/CotA-like multicopper oxidase GE001273. Under light conditions, Mn(II) significantly reduced the respiration rate and elevated the intracellular NADH/NADtotal ratio. This suggested that Mn(II)-derived electrons entered the cyclic photophosphorylation, partially replacing the oxidative phosphorylation for ATP production and enhancing the electron flow to complex I for NADH generation. In vitro enzymatic studies confirmed that GE001273 was a catalyst for Mn(II) oxidation in the outer membrane. Comprehensive genomic analyses of respiration and carbon and nitrogen metabolism revealed the high ecophysiological flexibility of strain MAB10 during Mn(II) oxidation-coupled anoxygenic photoautotrophy in deep-sea habitats. These analyses provided insights into bacterial Mn(II) oxidation-coupled anoxygenic photoautotrophy during microorganism-mediated deep-sea ferromanganese nodule formation.IMPORTANCEMicroorganisms are believed to participate in the biotic process of deep-sea ferromanganese nodule formation [Mn(II) oxidation]. Despite the multitude of studies and reviews focusing on the details of Mn(II) oxidation catalyzed by diverse heterotrophs, the mechanistic roles of manganese chemolithotrophs from ferromanganese nodules remain unclear. We demonstrate that strain Georhizobium sp. MAB10 can utilize Mn(II)-derived electrons for photoautotrophic growth, with concomitant generation of dark β-MnO2 type Mn oxides under near-infrared light condition. This study uses genomic and biochemical assays to explore the genetic basis of Mn(II) oxidation-coupled anoxygenic photoautotrophy. The comprehensive analyses of respiration and carbon and nitrogen metabolism further elucidated the high ecophysiological flexibility of strain MAB10 in deep-sea habits. These findings expand our understanding of the role of chemolithotrophs in deep-sea ferromanganese nodule formation and justify further investigations into the molecular basis for Mn(II) oxidation-coupled anoxygenic photoautotrophy. |
| format | Article |
| id | doaj-art-f8c1b295c1b940cdaf8d611f15859975 |
| institution | Kabale University |
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| language | English |
| publishDate | 2025-01-01 |
| publisher | American Society for Microbiology |
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| spelling | doaj-art-f8c1b295c1b940cdaf8d611f158599752025-01-08T14:00:38ZengAmerican Society for MicrobiologymBio2150-75112025-01-0116110.1128/mbio.02675-24Genomic insights into the alphaproteobacterium Georhizobium sp. MAB10 revealed a pathway of Mn(II) oxidation-coupled anoxygenic photoautotrophy: a novel understanding of the biotic process in deep-sea ferromanganese nodule formationXiuli Xu0Litao Zhang1Fuhang Song2Guoliang Zhang3Linlin Ma4Na Yang5Key Laboratory of Polar Geology and Marine Mineral Resources (China University of Geosciences, Beijing), Ministry of Education; Hainan Institute of China University of Geosciences (Beijing); School of Ocean Sciences, China University of Geosciences, Beijing, P. R. ChinaCAS Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, P. R. ChinaKey Laboratory of Geriatric Nutrition and Health, Ministry of Education of China, School of Light Industry Science and Engineering, Beijing Technology and Business University, Beijing, P. R. ChinaCenter of Deep Sea Research, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, P. R. ChinaInstitute for Biomedicine and Glycomics, School of Environment and Science, Griffith University, Brisbane, AustraliaCAS Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, P. R. ChinaABSTRACT Under light conditions, Mn(II) facilitates the photoautotrophic growth of Georhizobium sp. MAB10, a strain derived from deep-sea ferromanganese nodules, along with the generation of dark Mn oxides (β-MnO2). This study investigated the genetic basis of Mn(II) oxidation-coupled anoxygenic photoautotrophy using genome sequencing and biochemical assays of strain MAB10. Preliminary results indicated the presence of genes encoding a functional pheophytin-quinone-type photosynthetic reaction center and a putative key enzyme for Mn(II) oxidation, namely FtsP/CotA-like multicopper oxidase GE001273. Under light conditions, Mn(II) significantly reduced the respiration rate and elevated the intracellular NADH/NADtotal ratio. This suggested that Mn(II)-derived electrons entered the cyclic photophosphorylation, partially replacing the oxidative phosphorylation for ATP production and enhancing the electron flow to complex I for NADH generation. In vitro enzymatic studies confirmed that GE001273 was a catalyst for Mn(II) oxidation in the outer membrane. Comprehensive genomic analyses of respiration and carbon and nitrogen metabolism revealed the high ecophysiological flexibility of strain MAB10 during Mn(II) oxidation-coupled anoxygenic photoautotrophy in deep-sea habitats. These analyses provided insights into bacterial Mn(II) oxidation-coupled anoxygenic photoautotrophy during microorganism-mediated deep-sea ferromanganese nodule formation.IMPORTANCEMicroorganisms are believed to participate in the biotic process of deep-sea ferromanganese nodule formation [Mn(II) oxidation]. Despite the multitude of studies and reviews focusing on the details of Mn(II) oxidation catalyzed by diverse heterotrophs, the mechanistic roles of manganese chemolithotrophs from ferromanganese nodules remain unclear. We demonstrate that strain Georhizobium sp. MAB10 can utilize Mn(II)-derived electrons for photoautotrophic growth, with concomitant generation of dark β-MnO2 type Mn oxides under near-infrared light condition. This study uses genomic and biochemical assays to explore the genetic basis of Mn(II) oxidation-coupled anoxygenic photoautotrophy. The comprehensive analyses of respiration and carbon and nitrogen metabolism further elucidated the high ecophysiological flexibility of strain MAB10 in deep-sea habits. These findings expand our understanding of the role of chemolithotrophs in deep-sea ferromanganese nodule formation and justify further investigations into the molecular basis for Mn(II) oxidation-coupled anoxygenic photoautotrophy.https://journals.asm.org/doi/10.1128/mbio.02675-24Georhizobium sp. MAB10Mn(II) oxidation-coupled anoxygenic photoautotrophyphotosynthetic reaction center IImulticopper oxidasegenomedeep-sea ferromanganese nodules |
| spellingShingle | Xiuli Xu Litao Zhang Fuhang Song Guoliang Zhang Linlin Ma Na Yang Genomic insights into the alphaproteobacterium Georhizobium sp. MAB10 revealed a pathway of Mn(II) oxidation-coupled anoxygenic photoautotrophy: a novel understanding of the biotic process in deep-sea ferromanganese nodule formation mBio Georhizobium sp. MAB10 Mn(II) oxidation-coupled anoxygenic photoautotrophy photosynthetic reaction center II multicopper oxidase genome deep-sea ferromanganese nodules |
| title | Genomic insights into the alphaproteobacterium Georhizobium sp. MAB10 revealed a pathway of Mn(II) oxidation-coupled anoxygenic photoautotrophy: a novel understanding of the biotic process in deep-sea ferromanganese nodule formation |
| title_full | Genomic insights into the alphaproteobacterium Georhizobium sp. MAB10 revealed a pathway of Mn(II) oxidation-coupled anoxygenic photoautotrophy: a novel understanding of the biotic process in deep-sea ferromanganese nodule formation |
| title_fullStr | Genomic insights into the alphaproteobacterium Georhizobium sp. MAB10 revealed a pathway of Mn(II) oxidation-coupled anoxygenic photoautotrophy: a novel understanding of the biotic process in deep-sea ferromanganese nodule formation |
| title_full_unstemmed | Genomic insights into the alphaproteobacterium Georhizobium sp. MAB10 revealed a pathway of Mn(II) oxidation-coupled anoxygenic photoautotrophy: a novel understanding of the biotic process in deep-sea ferromanganese nodule formation |
| title_short | Genomic insights into the alphaproteobacterium Georhizobium sp. MAB10 revealed a pathway of Mn(II) oxidation-coupled anoxygenic photoautotrophy: a novel understanding of the biotic process in deep-sea ferromanganese nodule formation |
| title_sort | genomic insights into the alphaproteobacterium georhizobium sp mab10 revealed a pathway of mn ii oxidation coupled anoxygenic photoautotrophy a novel understanding of the biotic process in deep sea ferromanganese nodule formation |
| topic | Georhizobium sp. MAB10 Mn(II) oxidation-coupled anoxygenic photoautotrophy photosynthetic reaction center II multicopper oxidase genome deep-sea ferromanganese nodules |
| url | https://journals.asm.org/doi/10.1128/mbio.02675-24 |
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