Evidence of microbial rhodopsins in Antarctic Dry Valley edaphic systems

Abstract

Microorganisms able to synthesize rhodopsins have the capacity to translocate ions through their membranes, using solar energy to generate a proton motive force. Rhodopsins are the most abundant phototrophic proteins in oceanic surface waters and are key constituents in marine bacterial ecology. However, it remains unclear how rhodopsins are used in most microorganisms. Despite their abundance in marine and fresh-water systems, the presence of functional rhodopsin systems in edaphic habitats has never been reported. Here, we show the presence of several new putative H+, Na+ and Cl+ pumping rhodopsins identified by metagenomic analysis of Antarctic desert hypolithic communities. Reconstruction of two Proteobacteria genomes harboring xanthorhodopsin-like proteins and one Bacteroidetes genome with a Na-pumping-like rhodopsin indicated that these bacteria were aerobic heterotrophs possessing the apparent capacity for the functional expression of rhodopsins. The existence of these protein systems in hypolithic bacteria expands the known role of rhodopsins to include terrestrial environments and suggests a possible predominant function as heterotrophic energy supply proteins, a feasible microbial adaptation to the harsh conditions prevalent in Antarctic edaphic systems.