TY - JOUR
T1 - Presence of a haloarchaeal halorhodopsin-like Cl– pump in marine bacteria
AU - Nakajima, Yu
AU - Tsukamoto, Takashi
AU - Kumagai, Yohei
AU - Ogura, Yoshitoshi
AU - Hayashi, Tetsuya
AU - Song, Jaeho
AU - Kikukawa, Takashi
AU - Demura, Makoto
AU - Kogure, Kazuhiro
AU - Sudo, Yuki
AU - Yoshizawa, Susumu
N1 - Funding Information:
We are grateful to the captains and crews of R/V Mirai (JAMSTEC) and R/V Tansei Maru (Atmosphere and Ocean Research Institute, The University of Tokyo and JAMSTEC) for their assistance and support with sample collection. This work was supported by the Japan Society for the Promotion of Science (JSPS) to TT (15K18519) and SY (15H02800) and the Interdisciplinary Collaborative Research Program of the Atmosphere and Ocean Research Institute, the University of Tokyo. This work was also supported by JST-CREST and AMED to YS.
Publisher Copyright:
© 2018, Japanese Society of Microbial Ecology. All rights reserved.
PY - 2018
Y1 - 2018
N2 - Light-driven ion-pumping rhodopsins are widely distributed among bacteria, archaea, and eukaryotes in the euphotic zone of the aquatic environment. H+-pumping rhodopsin (proteorhodopsin: PR), Na+-pumping rhodopsin (NaR), and Cl–-pumping rhodopsin (ClR) have been found in marine bacteria, which suggests that these genes evolved independently in the ocean. Putative microbial rhodopsin genes were identified in the genome sequences of marine Cytophagia. In the present study, one of these genes was heterologously expressed in Escherichia coli cells and the rhodopsin protein named Rubricoccus marinus halorhodopsin (RmHR) was identified as a light-driven inward Cl– pump. Spectroscopic assays showed that the estimated dissociation constant (Kd,int.) of this rhodopsin was similar to that of haloarchaeal halorhodopsin (HR), while the Cl–-transporting photoreaction mechanism of this rhodopsin was similar to that of HR, but different to that of the already-known marine bacterial ClR. This amino acid sequence similarity also suggested that this rhodopsin is similar to haloarchaeal HR and cyanobacterial HRs (e.g., SyHR and MrHR). Additionally, a phylogenetic analysis revealed that retinal biosynthesis pathway genes (blh and crtY) belong to a phylogenetic lineage of haloarchaea, indicating that these marine Cytophagia acquired rhodopsin-related genes from haloarchaea by lateral gene transfer. Based on these results, we concluded that inward Cl–-pumping rhodopsin is present in genera of the class Cytophagia and may have the same evolutionary origins as haloarchaeal HR.
AB - Light-driven ion-pumping rhodopsins are widely distributed among bacteria, archaea, and eukaryotes in the euphotic zone of the aquatic environment. H+-pumping rhodopsin (proteorhodopsin: PR), Na+-pumping rhodopsin (NaR), and Cl–-pumping rhodopsin (ClR) have been found in marine bacteria, which suggests that these genes evolved independently in the ocean. Putative microbial rhodopsin genes were identified in the genome sequences of marine Cytophagia. In the present study, one of these genes was heterologously expressed in Escherichia coli cells and the rhodopsin protein named Rubricoccus marinus halorhodopsin (RmHR) was identified as a light-driven inward Cl– pump. Spectroscopic assays showed that the estimated dissociation constant (Kd,int.) of this rhodopsin was similar to that of haloarchaeal halorhodopsin (HR), while the Cl–-transporting photoreaction mechanism of this rhodopsin was similar to that of HR, but different to that of the already-known marine bacterial ClR. This amino acid sequence similarity also suggested that this rhodopsin is similar to haloarchaeal HR and cyanobacterial HRs (e.g., SyHR and MrHR). Additionally, a phylogenetic analysis revealed that retinal biosynthesis pathway genes (blh and crtY) belong to a phylogenetic lineage of haloarchaea, indicating that these marine Cytophagia acquired rhodopsin-related genes from haloarchaea by lateral gene transfer. Based on these results, we concluded that inward Cl–-pumping rhodopsin is present in genera of the class Cytophagia and may have the same evolutionary origins as haloarchaeal HR.
KW - Chloride ion pump
KW - Family Rhodothermaceae
KW - Genome analysis
KW - Rhodopsin
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U2 - 10.1264/jsme2.ME17197
DO - 10.1264/jsme2.ME17197
M3 - Article
C2 - 29553064
AN - SCOPUS:85044621971
VL - 33
SP - 89
EP - 97
JO - Microbes and Environments
JF - Microbes and Environments
SN - 1342-6311
IS - 1
ER -