A light-driven sodium ion pump in marine bacteria

Abstract

Light-driven proton-pumping rhodopsins are widely distributed in many microorganisms. They convert sunlight energy into proton gradients that serve as energy source of the cell. Here we report a new functional class of a microbial rhodopsin, a light-driven sodium ion pump. We discover that the marine flavobacterium Krokinobacter eikastus possesses two rhodopsins, the first, KR1, being a prototypical proton pump, while the second, KR2, pumps sodium ions outward. Rhodopsin KR2 can also pump lithium ions, but converts to a proton pump when presented with potassium chloride or salts of larger cations. These data indicate that KR2 is a compatible sodium ion-proton pump, and spectroscopic analysis showed it binds sodium ions in its extracellular domain. These findings suggest that light-driven sodium pumps may be as important in situ as their proton-pumping counterparts.

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

“…The three N. marinus rhodopsins have similar absorption spectra ( Fig. 2A), similar to those of other known green-light absorbing rhodopsins (6,9). Light-induced pH changes in E. coli cell suspensions expressing NM-R1, NM-R2, or NM-R3 were determined (Fig.…”

“…To determine the ion specificities of NM-R2 and NM-R3, we performed similar measurements in various salt solutions, as described previously (9). In the case of NM-R2, the same lightinduced pH increases as observed in NaCl solutions were also observed in NaBr and Na 2 SO 4 solutions, but not in KCl solutions (Fig.…”

“…Subsequent culture-independent surveys indicated that rhodopsin genes are taxonomically and geographically broadly distributed among marine bacteria and archaea and occur in a high proportion of surface-dwelling oceanic microbial species (8). Furthermore, recent whole genome analyses coupled with biochemical and physiological analyses have revealed that some marine bacteria also have a newly discovered rhodopsin functionality, an outward Na + -pumping rhodopsin (NaR) (9). These studies indicate that light utilization by microbial rhodopsins is a favorable survival strategy that has been broadly distributed via both vertical and horizontal transmission events, and has resulted in considerable diversification of rhodopsin's functional properties and taxon distributions.…”

“…HR; N85 and Q96 in NaR). Inoue et al (9) suggested that NaR, carboxylic residue D89 (BR numbering) has a significant role in Na + pumping, because a D89N mutant of NaR lost Na + -pumping activity. For BR, PR, and HR, neutral amino acid residues are found at the same positions (T89 in BR, T89 in PR, and S89 in HR).…”

A new class of marine Euryarchaeota group II from the mediterranean deep chlorophyll maximum

“…Residue 105, involved in spectral tuning, was a methionine, characteristic of green absorbing rhodopsins from shallow depths (Fuhrman et al, 2008) of the Bacteriodetes proteorhodopsin isoform, such as in the marine flavobacterium Dokdonia donghaensis MED134 (Gomez-Consarnau et al, 2007;Riedel et al, 2010). It is known that different amino acid substitutions in residues aspartic-97 (D) and glutamic-108 (E), which function as Schiff base proton acceptor and donor in many proteorhodopsins, provide different capacities to pump outward different ions, varying from H þ (Gushchin et al, 2013), Na þ (Inoue et al, 2013) and even lithium (Inoue et al, 2013). These residues are partially conserved in the thalassorhodopsins and instead of the E, the basic aminoacid lysine (K) is found, a very unusual residue in proton pumping rhodopsins found previously only in Exiguobacterium sibiricum, a permafrost soil Gram-positive (Balashov et al, 2013;Gushchin et al, 2013).…”