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

doi:10.1073/pnas.1403051111

Cited by 141 publications

(154 citation statements)

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“…While MED134 and DSW-1 T have one copy of the rhodopsin gene, PRO95 contains two different rhodopsin genes: a H + rhodopsin (PR) and a Na + rhodopsin (NaR), based on sequence comparison (Yoshizawa et al, 2014;Bertsova et al, 2015). This Abbreviation: bp, base pair.…”

Section: Resultsmentioning

confidence: 99%

“…Recently, another flavobacterium, Nonlabens marinus S1-08, containing three different rhodopsin types (H + , Na + and Cl − pumps) has been described. Similarly to MED134, this bacterium grows better in the light compared with dark in a low organic matter medium (Yoshizawa et al, 2014). In contrast to these two Dokdonia (S1-08 and MED134), another strain of the same genus, PRO95, has not yet shown enhanced growth or increased PR gene expression in the light compared to the dark (Riedel et al, 2010).…”

Section: Introductionmentioning

confidence: 94%

“…In contrast to these two Dokdonia (S1-08 and MED134), another strain of the same genus, PRO95, has not yet shown enhanced growth or increased PR gene expression in the light compared to the dark (Riedel et al, 2010). PRO95 also has more than one rhodopsin type and, according to sequence similarities, one functions to pump H + and the other one to pump Na + ions (Yoshizawa et al, 2014, Bertsova et al, 2015. Together, the studies of PR in cultured bacteria reflect a diversity of physiological responses that still cannot be predicted solely based on whole-genome sequence information, and therefore a combination of different research approaches are required to elucidate the specific mechanisms of PR photoheterotrophy.…”

Section: Introductionmentioning

confidence: 99%

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Proteorhodopsin light-enhanced growth linked to vitamin-B1 acquisition in marine Flavobacteria

et al. 2015

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Proteorhodopsins (PR) are light-driven proton pumps widely distributed in bacterioplankton. Although they have been thoroughly studied for more than a decade, it is still unclear how the proton motive force (pmf) generated by PR is used in most organisms. Notably, very few PR-containing bacteria show growth enhancement in the light. It has been suggested that the presence of specific functions within a genome may define the different PR-driven light responses. Thus, comparing closely related organisms that respond differently to light is an ideal setup to identify the mechanisms involved in PR light-enhanced growth. Here, we analyzed the transcriptomes of three PR-harboring Flavobacteria strains of the genus Dokdonia: Dokdonia donghaensis DSW-1 T , Dokdonia MED134 and Dokdonia PRO95, grown in identical seawater medium in light and darkness. Although only DSW-1 T and MED134 showed light-enhanced growth, all strains expressed their PR genes at least 10 times more in the light compared with dark. According to their genomes, DSW-1 T and MED134 are vitamin-B 1 auxotrophs, and their vitamin-B 1 TonB-dependent transporters (TBDT), accounted for 10-18% of all pmf-dependent transcripts. In contrast, the expression of vitamin-B 1 TBDT was 10 times lower in the prototroph PRO95, whereas its vitamin-B 1 synthesis genes were among the highest expressed. Our data suggest that light-enhanced growth in DSW-1 T and MED134 derives from the use of PR-generated pmf to power the uptake of vitamin-B 1 , essential for central carbon metabolism, including the TCA cycle. Other pmf-generating mechanisms available in darkness are probably insufficient to power transport of enough vitamin-B 1 to support maximum growth of these organisms.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 94%

Section: Introductionmentioning

confidence: 99%

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Proteorhodopsin light-enhanced growth linked to vitamin-B1 acquisition in marine Flavobacteria

et al. 2015

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“…Essentially, all Flavobacteria switch from rodshaped cells to long filaments that can intertwine to form clumps (Jooste and Hugo 1999). They also contain a variety of pigments such as yellow pigments (Verma and Rathore 2015) or proteorhodopsin and can be stimulated by light (Gómez-Consarnau et al 2007); Yoshizawa et al 2014). In another example, R. biformata forms characteristic rusty red pigmented colonies and, like many Flavobacteria, contains genes for the complex pathway of carotenoid biosynthesis (Oh et al, 2009).…”

Section: Dfi Genes Occur In Select Microorganisms Onlymentioning

confidence: 99%

On the role, ecology, phylogeny, and structure of dual-family immunophilins

Barik¹

2017

Cell Stress and Chaperones

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The novel class of dual-family immunophilins (henceforth abbreviated as DFI) represents naturally occurring chimera of classical FK506-binding protein (FKBP) and cyclophilin (CYN), connected by a flexible linker that may include a three-unit tetratricopeptide (TPR) repeat. Here, I report a comprehensive analysis of all current DFI sequences and their host organisms. DFIs are of two kinds: CFBP (cyclosporin-and FK506-binding protein) and FCBP (FK506-and cyclosporin-binding protein), found in eukaryotes. The CFBP type occurs in select bacteria that are mostly extremophiles, such as psychrophilic, thermophilic, halophilic, and sulfur-reducing. Essentially all DFI organisms are unicellular. I suggest that DFIs are specialized bifunctional chaperones that use their flexible interdomain linker to associate with large polypeptides or multisubunit megacomplexes to promote simultaneous folding or renaturation of two clients in proximity, essential in stressful and denaturing environments. Analysis of sequence homology and predicted 3D structures of the FKBP and CYN domains as well as the TPR linkers upheld the modular nature of the DFIs and revealed the uniqueness of their TPR domain. The CFBP and FCBP genes appear to have evolved in parallel pathways with no obvious single common ancestor. The occurrence of both types of DFI in multiple unrelated phylogenetic clades supported their selection in metabolic and environmental niche roles rather than a traditional taxonomic relationship.Nonetheless, organisms with these rare immunophilins may define an operational taxonomic unit (OTU) bound by the commonality of chaperone function.

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“…A while after these discoveries, microbial rhodopsins were thought to be restricted to hypersaline environments. However, because of the recent developments in molecular biology techniques, three different functional rhodopsins, a light-driven H ϩ -pumping proteorhodopsin, a light-driven Na ϩ (sodium ion)-pumping rhodopsin, and a light-driven Cl Ϫ -pumping rhodopsin, were found in marine microorganisms (3)(4)(5). Now it is known that ion-translocating rhodopsins are widely distributed in a variety of microorganisms in all three domains of life (6 -8).…”

mentioning

confidence: 99%

Structural Mechanism for Light-driven Transport by a New Type of Chloride Ion Pump, Nonlabens marinus Rhodopsin-3

Hosaka

Yoshizawa

Nakajima

et al. 2016

Journal of Biological Chemistry

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The light-driven inward chloride ion-pumping rhodopsin Nonlabens marinus rhodopsin-3 (NM-R3), from a marine flavobacterium, belongs to a phylogenetic lineage distinct from the halorhodopsins known as archaeal inward chloride ion-pumping rhodopsins. NM-R3 and halorhodopsin have distinct motif sequences that are important for chloride ion binding and transport. In this study, we present the crystal structure of a new type of light-driven chloride ion pump, NM-R3, at 1.58 Å resolution. The structure revealed the chloride ion translocation pathway and showed that a single chloride ion resides near the Schiff base. The overall structure, chloride ion-binding site, and translocation pathway of NM-R3 are different from those of halorhodopsin. Unexpectedly, this NM-R3 structure is similar to the crystal structure of the light-driven outward sodium ion pump, Krokinobacter eikastus rhodopsin 2. Structural and mutational analyses of NM-R3 revealed that most of the important amino acid residues for chloride ion pumping exist in the ion influx region, located on the extracellular side of NM-R3. In contrast, on the opposite side, the cytoplasmic regions of K. eikastus rhodopsin 2 were reportedly important for sodium ion pumping. These results provide new insight into ion selection mechanisms in ion pumping rhodopsins, in which the ion influx regions of both the inward and outward pumps are important for their ion selectivities.

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

Cited by 141 publications

References 47 publications

Proteorhodopsin light-enhanced growth linked to vitamin-B1 acquisition in marine Flavobacteria

Proteorhodopsin light-enhanced growth linked to vitamin-B1 acquisition in marine Flavobacteria

On the role, ecology, phylogeny, and structure of dual-family immunophilins

Structural Mechanism for Light-driven Transport by a New Type of Chloride Ion Pump, Nonlabens marinus Rhodopsin-3

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