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 CO(2) 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.

Fig. 1.

Images of MED152. (A) Colonies on marine agar showing the characteristic orange color. (B) SEM image of a typical aggregate showing abundant extracellular material. (C) SEM image showing individual cells.

Fig. 2.

Diagram of a MED152 cell. Processes that generate a H⁺ or Na⁺ gradient are shown Lower and Left. Central metabolism pathways, as well as anaplerotic reactions, are indicated. Bicarbonate transporters are shown Lower.

Fig. 3.

Bicarbonate uptake. Striped columns denote subsamples from cultures grown in the dark, incubated with H¹⁴CO₃⁻ in the light (dark-to-light) or dark (dark-to-dark). Solid columns indicate subsamples from cultures grown in the light, incubated with H¹⁴CO₃⁻ in the light (light-to-light) or dark (light-to-dark). (Inset) Growth of cultures in the dark (filled circles) and in the light (open circles) from where subsamples for bicarbonate uptake assays were collected at 50 h; the x axis shows time (hours) and the y axis, optical density. Error bars denote SD for duplicates.

Fig. 4.

Domain architectures of selected peptides involved in signal transduction in MED152. MED152_00100 is a hybrid two-component His kinase sensor with both a HEW type His kinase (HEW HK) and a response regulator (REC). It contains a phytochrome domain that detects red and far-red light in a number of organisms. PAC, PAS, and GAF domains are common components of phytochromes. HK is a His kinase domain with its cognate ATPase domain (HK ATPase). In MED152_08960, a BLUF domain (shown to sense blue light) is next to a DNA-interacting AraC-type helix-turn-helix domain (HTC AraC). CHASE3 is an extracellular sensory domain, and HAMP has been suggested to regulate signal transduction. CheB methylesterase and CheR methyltransferase are part of chemiotaxis signaling in bacteria. Solid bars represent transmembrane regions.