Anoxygenic phototrophic arsenite oxidation by a Rhodobacter strain
Microbially mediated arsenic redox transformations are key for arsenic speciation and mobility in rice paddies. Whereas anaerobic anoxygenic photosynthesis coupled to arsenite (As(III)) oxidation has been widely examined in arsenic‐replete ecosystems, it remains unknown whether this light‐dependent...
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Published in | Environmental microbiology Vol. 25; no. 8; pp. 1538 - 1548 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
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Hoboken, USA
John Wiley & Sons, Inc
01.08.2023
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Abstract | Microbially mediated arsenic redox transformations are key for arsenic speciation and mobility in rice paddies. Whereas anaerobic anoxygenic photosynthesis coupled to arsenite (As(III)) oxidation has been widely examined in arsenic‐replete ecosystems, it remains unknown whether this light‐dependent process exists in paddy soils. Here, we isolated a phototrophic purple bacteria, Rhodobacter strain CZR27, from an arsenic‐contaminated paddy soil and demonstrated its capacity to oxidize As(III) to arsenate (As(V)) using malate as a carbon source photosynthetically. Genome sequencing revealed an As(III)‐oxidizing gene cluster (aioXSRBA) encoding an As(III) oxidase. Functional analyses showed that As(III) oxidation under anoxic phototrophic conditions correlated with transcription of the large subunit of the As(III) oxidase aioA gene. Furthermore, the non‐As(III) oxidizer Rhodobacter capsulatus SB1003 heterologously expressing aioBA from strain CZR27 was able to oxidize As(III), indicating that aioBA was responsible for the observed As(III) oxidation in strain CZR27. Our study provides evidence for the presence of anaerobic photosynthesis‐coupled As(III) oxidation in paddy soils, highlighting the importance of light‐dependent, microbe‐mediated arsenic redox changes in paddy arsenic biogeochemistry. |
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AbstractList | Microbially mediated arsenic redox transformations are key for arsenic speciation and mobility in rice paddies. Whereas anaerobic anoxygenic photosynthesis coupled to arsenite (As(III)) oxidation has been widely examined in arsenic‐replete ecosystems, it remains unknown whether this light‐dependent process exists in paddy soils. Here, we isolated a phototrophic purple bacteria, Rhodobacter strain CZR27, from an arsenic‐contaminated paddy soil and demonstrated its capacity to oxidize As(III) to arsenate (As(V)) using malate as a carbon source photosynthetically. Genome sequencing revealed an As(III)‐oxidizing gene cluster (aioXSRBA) encoding an As(III) oxidase. Functional analyses showed that As(III) oxidation under anoxic phototrophic conditions correlated with transcription of the large subunit of the As(III) oxidase aioA gene. Furthermore, the non‐As(III) oxidizer Rhodobacter capsulatus SB1003 heterologously expressing aioBA from strain CZR27 was able to oxidize As(III), indicating that aioBA was responsible for the observed As(III) oxidation in strain CZR27. Our study provides evidence for the presence of anaerobic photosynthesis‐coupled As(III) oxidation in paddy soils, highlighting the importance of light‐dependent, microbe‐mediated arsenic redox changes in paddy arsenic biogeochemistry. Microbially mediated arsenic redox transformations are key for arsenic speciation and mobility in rice paddies. Whereas anaerobic anoxygenic photosynthesis coupled to arsenite (As(III)) oxidation has been widely examined in arsenic‐replete ecosystems, it remains unknown whether this light‐dependent process exists in paddy soils. Here, we isolated a phototrophic purple bacteria, Rhodobacter strain CZR27, from an arsenic‐contaminated paddy soil and demonstrated its capacity to oxidize As(III) to arsenate (As(V)) using malate as a carbon source photosynthetically. Genome sequencing revealed an As(III)‐oxidizing gene cluster ( aioXSRBA ) encoding an As(III) oxidase. Functional analyses showed that As(III) oxidation under anoxic phototrophic conditions correlated with transcription of the large subunit of the As(III) oxidase aioA gene. Furthermore, the non‐As(III) oxidizer Rhodobacter capsulatus SB1003 heterologously expressing aioBA from strain CZR27 was able to oxidize As(III), indicating that aioBA was responsible for the observed As(III) oxidation in strain CZR27. Our study provides evidence for the presence of anaerobic photosynthesis‐coupled As(III) oxidation in paddy soils, highlighting the importance of light‐dependent, microbe‐mediated arsenic redox changes in paddy arsenic biogeochemistry. Microbially mediated arsenic redox transformations are key for arsenic speciation and mobility in rice paddies. Whereas anaerobic anoxygenic photosynthesis coupled to arsenite (As(III)) oxidation has been widely examined in arsenic-replete ecosystems, it remains unknown whether this light-dependent process exists in paddy soils. Here, we isolated a phototrophic purple bacteria, Rhodobacter strain CZR27, from an arsenic-contaminated paddy soil and demonstrated its capacity to oxidize As(III) to arsenate (As(V)) using malate as a carbon source photosynthetically. Genome sequencing revealed an As(III)-oxidizing gene cluster (aioXSRBA) encoding an As(III) oxidase. Functional analyses showed that As(III) oxidation under anoxic phototrophic conditions correlated with transcription of the large subunit of the As(III) oxidase aioA gene. Furthermore, the non-As(III) oxidizer Rhodobacter capsulatus SB1003 heterologously expressing aioBA from strain CZR27 was able to oxidize As(III), indicating that aioBA was responsible for the observed As(III) oxidation in strain CZR27. Our study provides evidence for the presence of anaerobic photosynthesis-coupled As(III) oxidation in paddy soils, highlighting the importance of light-dependent, microbe-mediated arsenic redox changes in paddy arsenic biogeochemistry.Microbially mediated arsenic redox transformations are key for arsenic speciation and mobility in rice paddies. Whereas anaerobic anoxygenic photosynthesis coupled to arsenite (As(III)) oxidation has been widely examined in arsenic-replete ecosystems, it remains unknown whether this light-dependent process exists in paddy soils. Here, we isolated a phototrophic purple bacteria, Rhodobacter strain CZR27, from an arsenic-contaminated paddy soil and demonstrated its capacity to oxidize As(III) to arsenate (As(V)) using malate as a carbon source photosynthetically. Genome sequencing revealed an As(III)-oxidizing gene cluster (aioXSRBA) encoding an As(III) oxidase. Functional analyses showed that As(III) oxidation under anoxic phototrophic conditions correlated with transcription of the large subunit of the As(III) oxidase aioA gene. Furthermore, the non-As(III) oxidizer Rhodobacter capsulatus SB1003 heterologously expressing aioBA from strain CZR27 was able to oxidize As(III), indicating that aioBA was responsible for the observed As(III) oxidation in strain CZR27. Our study provides evidence for the presence of anaerobic photosynthesis-coupled As(III) oxidation in paddy soils, highlighting the importance of light-dependent, microbe-mediated arsenic redox changes in paddy arsenic biogeochemistry. |
Author | Rosen, Barry P. Kappler, Andreas Zhao, Fang‐Jie Chen, Jian Peng, Chao Tang, Shi‐Tong Wu, Yi‐Fei Zhang, Jun Xie, Wan‐Ying |
AuthorAffiliation | 4 Geomicrobiology, Department of Geoscience, University of Tuebingen, Tuebingen 72076, Germany 1 Jiangsu Key Laboratory for Organic Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, China 2 Department of Cellular Biology and Pharmacology, Herbert Wertheim College of Medicine, Florida International University, Miami, Florida 33199, USA 3 College of Life Sciences, China West Normal University, Nanchong, China 5 Cluster of Excellence: EXC 2124: Controlling Microbes to Fight Infection, Tuebingen 72076, Germany |
AuthorAffiliation_xml | – name: 3 College of Life Sciences, China West Normal University, Nanchong, China – name: 4 Geomicrobiology, Department of Geoscience, University of Tuebingen, Tuebingen 72076, Germany – name: 5 Cluster of Excellence: EXC 2124: Controlling Microbes to Fight Infection, Tuebingen 72076, Germany – name: 1 Jiangsu Key Laboratory for Organic Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, China – name: 2 Department of Cellular Biology and Pharmacology, Herbert Wertheim College of Medicine, Florida International University, Miami, Florida 33199, USA |
Author_xml | – sequence: 1 givenname: Yi‐Fei surname: Wu fullname: Wu, Yi‐Fei organization: Nanjing Agricultural University – sequence: 2 givenname: Jian surname: Chen fullname: Chen, Jian organization: Florida International University – sequence: 3 givenname: Wan‐Ying surname: Xie fullname: Xie, Wan‐Ying organization: Nanjing Agricultural University – sequence: 4 givenname: Chao surname: Peng fullname: Peng, Chao organization: China West Normal University – sequence: 5 givenname: Shi‐Tong surname: Tang fullname: Tang, Shi‐Tong organization: Nanjing Agricultural University – sequence: 6 givenname: Barry P. surname: Rosen fullname: Rosen, Barry P. organization: Florida International University – sequence: 7 givenname: Andreas surname: Kappler fullname: Kappler, Andreas organization: Cluster of Excellence: EXC 2124: Controlling Microbes to Fight Infection – sequence: 8 givenname: Jun orcidid: 0000-0003-1965-7224 surname: Zhang fullname: Zhang, Jun email: zhangjun1208@njau.edu.cn organization: Nanjing Agricultural University – sequence: 9 givenname: Fang‐Jie orcidid: 0000-0002-0164-169X surname: Zhao fullname: Zhao, Fang‐Jie organization: Nanjing Agricultural University |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 AUTHOR CONTRIBUTIONS Yi-Fei Wu: Conceptualization (equal); data curation (equal); writing – original draft (equal). Jian Chen: Methodology (equal). Wan-Ying Xie: Data curation (equal); writing – review and editing (equal). Chao Peng: Methodology (equal); resources (equal). Shi-Tong Tang: Investigation (equal); methodology (equal). Barry P. Rosen: Conceptualization (equal); data curation (equal); funding acquisition (equal); writing – review and editing (equal). Andreas Kappler: Resources (equal); writing – review and editing (equal). Jun Zhang: Methodology (equal); resources (equal). Fangjie Zhao: Resources (equal); supervision (equal); validation (equal). |
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Snippet | Microbially mediated arsenic redox transformations are key for arsenic speciation and mobility in rice paddies. Whereas anaerobic anoxygenic photosynthesis... |
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SubjectTerms | Anoxia Arsenates Arsenic Arsenite Arsenites Bacteria Biogeochemistry carbon Carbon sources Ecosystem Gene sequencing Genomes malates Microbiological strains microbiology multigene family oxidants Oxidase Oxidation Oxidation-Reduction Oxidizing agents Oxidoreductases paddies paddy soils Photosynthesis Rhodobacter Rhodobacter - genetics Rhodobacter capsulatus rice Rice fields Soil Soil contamination Soil pollution Soils Speciation Transcription |
Title | Anoxygenic phototrophic arsenite oxidation by a Rhodobacter strain |
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