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

Susumu Yoshizawa, Yohei Kumagai, Hana Kim, Yoshitoshi Ogura, Tetsuya Hayashi, Wataru Iwasaki, Edward F. DeLong, Kazuhiro Kogure

Research output: Contribution to journalArticle

79 Citations (Scopus)

Abstract

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 lightactivated 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.

Original languageEnglish
Pages (from-to)6732-6737
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume111
Issue number18
DOIs
Publication statusPublished - May 6 2014
Externally publishedYes

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Flavobacterium
Rhodopsin
Chlorides
Bacteria
Light
Halorhodopsins
Ion Pumps
Ions
Proton Pumps
Archaea

All Science Journal Classification (ASJC) codes

  • General

Cite this

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 F.; Kogure, Kazuhiro.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 111, No. 18, 06.05.2014, p. 6732-6737.

Research output: Contribution to journalArticle

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