Proteorhodopsin Phototrophy Promotes Survival of Marine Bacteria during Starvation

Abstract

Proteorhodopsins are globally abundant photoproteins found in bacteria in the photic zone of the ocean. Although their function as proton pumps with energy-yielding potential has been demonstrated, the ecological role of proteorhodopsins remains largely unexplored. Here, we report the presence and function of proteorhodopsin in a member of the widespread genus Vibrio, uncovered through whole-genome analysis. Phylogenetic analysis suggests that the Vibrio strain AND4 obtained proteorhodopsin through lateral gene transfer, which could have modified the ecology of this marine bacterium. We demonstrate an increased long-term survival of AND4 when starved in seawater exposed to light rather than held in darkness. Furthermore, mutational analysis provides the first direct evidence, to our knowledge, linking the proteorhodopsin gene and its biological function in marine bacteria. Thus, proteorhodopsin phototrophy confers a fitness advantage to marine bacteria, representing a novel mechanism for bacterioplankton to endure frequent periods of resource deprivation at the ocean's surface.

Expression of holo-proteorhodopsin in Synechocystis sp. PCC 6803

“…The drop in PR content during the stationary phase may be in part due to the promoter we selected, because it is known that psbA2 expression and transcript stability are light-intensity dependent (68)(69)(70)(71)(72)(73), and so is heterologous expression driven by this promoter (74,75). It is worth noting that several of the recently discovered proteorhodopsins in 'chemotrophic', often psychrophilic, bacteria only contribute detectably to growth rate or cell yield when the cells are stressed and/or in stationary phase (6,(14)(15)(16)(18)(19)(20).…”

“…To show that PR is able to make a contribution to light-energy conversion in Synechocystis, we also made use of starvation/stressful conditions, just like it was initially done in E. coli (21) and in some of the organisms in which it is endogenously present (6,(14)(15)(16)(18)(19)(20). However, no fully consistent data have been obtained under these conditions so far.…”

“…Since then, PRs have turned out to be highly abundant in the oceans (6)(7)(8)(9), and organisms containing them, including a cyanobacterium (10) can be found in many other habitats as well (7,(11)(12)(13). In vivo experiments have shown that pumping of protons by PR can lead to increases in growth rate under nutrient-limited conditions (6,14,15), production of ATP (16), increased fixation of CO 2 (6,17), and/or survival under starvation or stress conditions (16,(18)(19)(20). However, these enhancements generally require nutrient-limitation or stress conditions before they exceed experimental error.…”

Comparative single-cell genomics reveals potential ecological niches for the freshwater acI Actinobacteria lineage

“…Rhodopsin in Pelagibacter ubique and other marine bacteria promotes survival during nutrient starvation periods (Gomez-Consarnau et al, 2007;DeLong and Beja, 2010;Gó mez-Consarnau et al, 2010;Steindler et al, 2011); thus actinorhodopsin may serve a similar function in acI. In such an auxiliary system, it remains to be explored why there is not co-localization of the rhodopsin gene, the oxygenase gene and the core carotenoid synthesis operon, in acI genomes.…”

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

“…P. ubique) HTCC1062, for which a greater survival capacity and ATP-dependent substrate uptake in the light have been reported (Steindler et al, 2011). Also, two closely related marine Vibrio strains (AND4 and BAA-1116) have shown better survival to starvation or respiratory stress in the light (Gómez-Consarnau et al, 2010;Wang et al, 2012). However, a light-stimulated growth response could not be detected in other cultured bacteria like the gammaproteobacterium HTCC2207 in the SAR92 clade (Stingl et al, 2007).…”