Functional characterization of flavobacteria rhodopsins reveals a unique class of light-driven chloride pump in bacteria

• Main Authors: Yoshizawa, Susumu (Contributor), Kumagai, Yohei (Author), Kim, Hana (Contributor), Ogura, Yoshitoshi (Author), Hayashi, Tetsuya (Author), Iwasaki, Wataru (Author), DeLong, Edward (Contributor), Kogure, Kazuhiro (Author)
• Other Authors: Massachusetts Institute of Technology. Department of Biological Engineering (Contributor), Massachusetts Institute of Technology. Department of Civil and Environmental Engineering (Contributor)
• Format: Article
• Language: English
• Published: National Academy of Sciences (U.S.), 2014-12-01T21:43:54Z.
• Subjects: Article
• Online Access: Get fulltext

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)