Abstract
Proteorhodopsin (PR) is a light-driven proton pump that is found in diverse bacteria and archaea species, and is widespread in marine microbial ecosystems. To date, many studies have suggested the advantage of PR for microorganisms in sunlit environments. The ecophysiological significance of PR is still not fully understood however, including the drivers of PR gene gain, retention, and loss in different marine microbial species. To explore this question we sequenced 21 marine Flavobacteriia genomes of polyphyletic origin, which encompassed both PR-possessing as well as PR-lacking strains. Here, we show that the possession or alternatively the lack of PR genes reflects one of two fundamental adaptive strategies in marine bacteria. Specifically, while PR-possessing bacteria utilize light energy (“solar-panel strategy”), PR-lacking bacteria exclusively possess UV-screening pigment synthesis genes to avoid UV damage and would adapt to microaerobic environment (“parasol strategy”), which also helps explain why PR-possessing bacteria have smaller genomes than those of PR-lacking bacteria. Collectively, our results highlight the different strategies of dealing with light, DNA repair, and oxygen availability that relate to the presence or absence of PR phototrophy.
Highlights
Proteorhodopsin (PR) plays a fundamental role in marine ecosystems as a light-driven proton pump protein that converts light energy to proton motive force [1]
We subsequently downloaded 55 genomes of marine Flavobacteriia from the NCBI RefSeq database [17] and constructed a genomic data set of 76 marine Flavobacteriia strains, 41 and 35 of which were PR− and PR+ strains, respectively (Supplementary Table S2; their sampling sites are shown in Supplementary Fig. S1)
The polyphyletic distribution of PR genes (Fig. 1) and genomic traces indicated that PR genes have been gained and lost during evolution (Fig. 6), suggesting that the conditions that have made each of the PR– and PR + lifestyles advantageous have not been stable during the course of evolution
Summary
Proteorhodopsin (PR) plays a fundamental role in marine ecosystems as a light-driven proton pump protein that converts light energy to proton motive force [1]. The other eight strains were isolated from environmental samples in 2009 [3]: four strains from surface seawater at Western North Pacific Station S (30°40′N, 138°00′E) during cruise KT-09-11 of the R/V ‘Tansei Maru’ (Atmosphere and Ocean Research Institute, The University of Tokyo and Japan Agency for MarineEarth Science and Technology (JAMSTEC)) Genomes of two strains were sequenced using a 454 FLX+ System (Roche) and an Ion PGM System (Thermo Fisher Scientific) and assembled using the Newbler assembler v2.7 software (Roche). Genomes of 11 strains were sequenced using a 454 FLX+ System and a MiSeq (Illumina) platform and assembled using the Newbler assembler v2.7 software. Genomes of the other eight strains were sequenced using a PacBio RS II (Pacific Biosciences) instrument and assembled using Sprai v0.9.5.1.3 (http://zombie.cb.k.u-tokyo.ac.jp/sprai/) and subsequent manual curation. All sequencing was performed by following manufacturers' protocols, and all assembling steps were performed using default parameters
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