Functional characterization of flavobacteria rhodopsins reveals a unique class of light-driven chloride pump in bacteria
Light-activated, ion-pumping rhodopsins are broadly distributed among many different bacteria and archaea inhabiting the photic zone of aquatic environments. Bacterial proton- or sodium-translocating rhodopsins can convert light energy into a chemiosmotic force that can be converted into cellular bi...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | en_US |
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National Academy of Sciences (U.S.)
2014
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| Online Access: | http://hdl.handle.net/1721.1/91985 |
| _version_ | 1811087593468592128 |
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| author | Yoshizawa, Susumu Kumagai, Yohei Kim, Hana Ogura, Yoshitoshi Hayashi, Tetsuya Iwasaki, Wataru DeLong, Edward Kogure, Kazuhiro |
| author2 | Massachusetts Institute of Technology. Department of Biological Engineering |
| author_facet | Massachusetts Institute of Technology. Department of Biological Engineering Yoshizawa, Susumu Kumagai, Yohei Kim, Hana Ogura, Yoshitoshi Hayashi, Tetsuya Iwasaki, Wataru DeLong, Edward Kogure, Kazuhiro |
| author_sort | Yoshizawa, Susumu |
| collection | MIT |
| description | Light-activated, ion-pumping rhodopsins are broadly distributed among many different bacteria and archaea inhabiting the photic zone of aquatic environments. Bacterial proton- or sodium-translocating rhodopsins can convert light energy into a chemiosmotic force that can be converted into cellular biochemical energy, and thus represent a widespread alternative form of photoheterotrophy. Here we report that the genome of the marine flavobacterium Nonlabens marinus S1-08T encodes three different types of rhodopsins: Nonlabens marinus rhodopsin 1 (NM-R1), Nonlabens marinus rhodopsin 2 (NM-R2), and Nonlabens marinus rhodopsin 3 (NM-R3). Our functional analysis demonstrated that NM-R1 and NM-R2 are light-driven outward-translocating H+ and Na+ pumps, respectively. Functional analyses further revealed that the light-activated NM-R3 rhodopsin pumps Cl− ions into the cell, representing the first chloride-pumping rhodopsin uncovered in a marine bacterium. Phylogenetic analysis revealed that NM-R3 belongs to a distinct phylogenetic lineage quite distant from archaeal inward Cl−-pumping rhodopsins like halorhodopsin, suggesting that different types of chloride-pumping rhodopsins have evolved independently within marine bacterial lineages. Taken together, our data suggest that similar to haloarchaea, a considerable variety of rhodopsin types with different ion specificities have evolved in marine bacteria, with individual marine strains containing as many as three functionally different rhodopsins. |
| first_indexed | 2024-09-23T13:48:33Z |
| format | Article |
| id | mit-1721.1/91985 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T13:48:33Z |
| publishDate | 2014 |
| publisher | National Academy of Sciences (U.S.) |
| record_format | dspace |
| spelling | mit-1721.1/919852022-09-28T16:21:10Z Functional characterization of flavobacteria rhodopsins reveals a unique class of light-driven chloride pump in bacteria Yoshizawa, Susumu Kumagai, Yohei Kim, Hana Ogura, Yoshitoshi Hayashi, Tetsuya Iwasaki, Wataru DeLong, Edward Kogure, Kazuhiro Massachusetts Institute of Technology. Department of Biological Engineering Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Yoshizawa, Susumu Kim, Hana DeLong, Edward Light-activated, ion-pumping rhodopsins are broadly distributed among many different bacteria and archaea inhabiting the photic zone of aquatic environments. Bacterial proton- or sodium-translocating rhodopsins can convert light energy into a chemiosmotic force that can be converted into cellular biochemical energy, and thus represent a widespread alternative form of photoheterotrophy. Here we report that the genome of the marine flavobacterium Nonlabens marinus S1-08T encodes three different types of rhodopsins: Nonlabens marinus rhodopsin 1 (NM-R1), Nonlabens marinus rhodopsin 2 (NM-R2), and Nonlabens marinus rhodopsin 3 (NM-R3). Our functional analysis demonstrated that NM-R1 and NM-R2 are light-driven outward-translocating H+ and Na+ pumps, respectively. Functional analyses further revealed that the light-activated NM-R3 rhodopsin pumps Cl− ions into the cell, representing the first chloride-pumping rhodopsin uncovered in a marine bacterium. Phylogenetic analysis revealed that NM-R3 belongs to a distinct phylogenetic lineage quite distant from archaeal inward Cl−-pumping rhodopsins like halorhodopsin, suggesting that different types of chloride-pumping rhodopsins have evolved independently within marine bacterial lineages. Taken together, our data suggest that similar to haloarchaea, a considerable variety of rhodopsin types with different ion specificities have evolved in marine bacteria, with individual marine strains containing as many as three functionally different rhodopsins. Japan Society for the Promotion of Science (Kakenhi Grant 24681003) Japan Society for the Promotion of Science (Kakenhi Grant 23710231) Canon Foundation Japan Society for the Promotion of Science (Strategic Young Researcher Overseas Visits Program for Accelerating Brain Circulation (Grant G2401)) Japan. Ministry of Education, Culture, Sports, Science and Technology (Grant-in-aid for Scientific Research on Innovative Area, "Genome Science," (22120518)) Japan. Science and Technology Agency Gordon and Betty Moore Foundation (GBMF 492.01) National Science Foundation (U.S.) (Grant EF0424599) 2014-12-01T21:43:54Z 2014-12-01T21:43:54Z 2014-03 2014-02 Article http://purl.org/eprint/type/JournalArticle 0027-8424 1091-6490 http://hdl.handle.net/1721.1/91985 Yoshizawa, S., Y. Kumagai, H. Kim, Y. Ogura, T. Hayashi, W. Iwasaki, E. F. DeLong, and K. Kogure. “Functional Characterization of Flavobacteria Rhodopsins Reveals a Unique Class of Light-Driven Chloride Pump in Bacteria.” Proceedings of the National Academy of Sciences 111, no. 18 (March 31, 2014): 6732–6737. en_US http://dx.doi.org/10.1073/pnas.1403051111 Proceedings of the National Academy of Sciences Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf National Academy of Sciences (U.S.) National Academy of Sciences (U.S.) |
| spellingShingle | Yoshizawa, Susumu Kumagai, Yohei Kim, Hana Ogura, Yoshitoshi Hayashi, Tetsuya Iwasaki, Wataru DeLong, Edward Kogure, Kazuhiro Functional characterization of flavobacteria rhodopsins reveals a unique class of light-driven chloride pump in bacteria |
| title | Functional characterization of flavobacteria rhodopsins reveals a unique class of light-driven chloride pump in bacteria |
| title_full | Functional characterization of flavobacteria rhodopsins reveals a unique class of light-driven chloride pump in bacteria |
| title_fullStr | Functional characterization of flavobacteria rhodopsins reveals a unique class of light-driven chloride pump in bacteria |
| title_full_unstemmed | Functional characterization of flavobacteria rhodopsins reveals a unique class of light-driven chloride pump in bacteria |
| title_short | Functional characterization of flavobacteria rhodopsins reveals a unique class of light-driven chloride pump in bacteria |
| title_sort | functional characterization of flavobacteria rhodopsins reveals a unique class of light driven chloride pump in bacteria |
| url | http://hdl.handle.net/1721.1/91985 |
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