Genome analysis of the proteorhodopsin-containing marine bacterium Polaribacter sp. MED152 (Flavobacteria)

Abstract

Analysis of marine cyanobacteria and proteobacteria genomes has provided a profound understanding of the life strategies of these organisms and their ecotype differentiation and metabolisms. However, a comparable analysis of the Bacteroidetes, the third major bacterioplankton group, is still lacking. In the present paper, we report on the genome of Polaribacter sp. strain MED152. On the one hand, MED152 contains a substantial number of genes for attachment to surfaces or particles, gliding motility, and polymer degradation. This agrees with the currently assumed life strategy of marine Bacteroidetes. On the other hand, it contains the proteorhodopsin gene, together with a remarkable suite of genes to sense and respond to light, which may provide a survival advantage in the nutrient-poor sun-lit ocean surface when in search of fresh particles to colonize. Furthermore, an increase in CO2 fixation in the light suggests that the limited central metabolism is complemented by anaplerotic inorganic carbon fixation. This is mediated by a unique combination of membrane transporters and carboxylases. This suggests a dual life strategy that, if confirmed experimentally, would be notably different from what is known of the two other main bacterial groups (the autotrophic cyanobacteria and the heterotrophic proteobacteria) in the surface oceans. The Polaribacter genome provides insights into the physiological capabilities of proteorhodopsin-containing bacteria. The genome will serve as a model to study the cellular and molecular processes in bacteria that express proteorhodopsin, their adaptation to the oceanic environment, and their role in carbon-cycling.Bacteroidetes ͉ marine bacteria ͉ whole-genome analysis ͉ heterotrophic CO2 fixation

Expression of holo-proteorhodopsin in Synechocystis sp. PCC 6803

“…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.…”

Ecology of marine Bacteroidetes: a comparative genomics approach

“…MED152 and Dokdonia sp. MED134 have been published (Gó nzalez et al, 2008(Gó nzalez et al, , 2011. The genome of MED152 has been closed (González et al, unpublished results).…”

“…In Polaribacter sp. MED152, it was proposed that PR, in combination with a large suite of light sensing genes and a remarkable number of proteins involved in anaplerotic carbon fixation, represented adaptations to survive in the surface ocean while traveling between particles (Gó nzalez et al, 2008). This bacterium has a relatively small genome and it was postulated that it was only able to use a small number of monomeric carbon compounds, a fact consistent with the very low number of transporters compared with other bacteria and with a lower number of sugars used compared with MED217 (O Nedashkovskaya, personal communication).…”

“…These traits were also observed in Polaribacter sp. MED152, the second free-living marine Bacteroidetes genome analyzed (Gó nzalez et al, 2008). The latter authors proposed a dual life strategy for Polaribacter.…”

Actinorhodopsin genes discovered in diverse freshwater habitats and among cultivated freshwater Actinobacteria

“…However, exploratory studies such as ours can only provide insight into sequence diversity, generating fundamental questions regarding rhodopsin function and its impact at both cellular and ecosystem levels. A recent analysis by Gonzalez et al (2008) of the genome sequence of a proteorhodopsin-encoding marine bacterium proposed this organism may be capable of both carbon fixation and rhodopsin-based phototrophy. Such ideas highlight the vast potential for novel metabolic strategies involving rhodopsins.…”