Proteorhodopsin phototrophy in the ocean

Abstract

Proteorhodopsin, a retinal-containing integral membrane protein that functions as a light-driven proton pump, was discovered in the genome of an uncultivated marine bacterium; however, the prevalence, expression and genetic variability of this protein in native marine microbial populations remain unknown. Here we report that photoactive proteorhodopsin is present in oceanic surface waters. We also provide evidence of an extensive family of globally distributed proteorhodopsin variants. The protein pigments comprising this rhodopsin family seem to be spectrally tuned to different habitats--absorbing light at different wavelengths in accordance with light available in the environment. Together, our data suggest that proteorhodopsin-based phototrophy is a globally significant oceanic microbial process.

Adaptation and spectral tuning in divergent marine proteorhodopsins from the eastern Mediterranean and the Sargasso Seas

“…The PR gene fragments fell into several families not restricted to the PR groups previously reported using non-degenerate PCR primers (Béjà et al, 2001;Sabehi et al, 2003) and the overall diversity of the PR sequences was comparable to that previously detected in the Sargasso Sea metagenome (Venter et al, 2004). No apparent bias was also observed regarding any potential preference of our primers toward low G þ C amplicons (Suzuki and Giovannoni, 1996) (Supplementary Figure S2), further supporting the adequacy of these primers to sample across different subpopulation of the PR family.…”

“…Environmental sequences are represented by blue or green bands corresponding to their predicted absorption maxima to illustrate their distribution in different depths and seasons. The two subfamilies previously reported to be spectrally tuned (Béjà et al, 2001) are marked in blue and green boxes. SAR86 and SAR11 PR families, as well as few different PR representative's names from the Pacific Ocean (Béjà et al, 2001), Sargasso Sea shotgun-sequencing project (Venter et al, 2004), Mediterranean Sea bacterial artificial chromosomes (BACs) (Sabehi et al, , 2005, Pelagibacter ubique (Giovannoni et al, 2005a) and marine Archaea (Frigaard et al, 2006) are indicated to serve as orientation marks.…”

“…PRs have been observed in different ocean regions (Béjà et al, 2000(Béjà et al, , 2001de la Torre et al, 2003;Man et al, 2003;Sabehi et al, 2003Sabehi et al, , 2004Sabehi et al, , 2005Venter et al, 2004;Frigaard et al, 2006) and are found in diverse taxonomic backgrounds, including the ubiquitous marine gammaproteobacterial SAR86 (Béjà et al, 2000;Sabehi et al, 2004Sabehi et al, , 2005 and alphaproteobacterial SAR11 (Giovannoni et al, 2005a, b;Sabehi et al, 2005) groups, as well as in marine Bacteroidetes (Venter et al, 2004;Gó mez-Consarnau et al, 2007), planktonic Archaea (Frigaard et al, 2006) and other microbial taxa (de la Torre et al, 2003;Sabehi et al, 2003Sabehi et al, , 2005Venter et al, 2004;McCarren and DeLong, 2007). While previous work did not detect light enhanced growth in PR-containing SAR11 (Giovannoni et al, 2005a), or in the gammaproteobacterial SAR92 (Stingl et al, 2007) isolates grown in seawater, significant enhancement of both growth rate and yield was recently reported in PR-expressing marine Bacteroidetes (Gó mez- Consarnau et al, 2007).…”

“…Proteorhodopsins (PRs) (Béjà et al, 2000(Béjà et al, , 2001 are bacterial retinal-binding membrane pigments that belong to the microbial rhodopsin superfamily (Spudich et al, 2000) and are predicted to have an important role in supplying light energy for microbial metabolism in marine ecosystems (Béjà et al, 2000(Béjà et al, , 2001Sabehi et al, 2005;Martinez et al, 2007;Walter et al, 2007). PRs have been observed in different ocean regions (Béjà et al, 2000(Béjà et al, , 2001de la Torre et al, 2003;Man et al, 2003;Sabehi et al, 2003Sabehi et al, , 2004Sabehi et al, , 2005Venter et al, 2004;Frigaard et al, 2006) and are found in diverse taxonomic backgrounds, including the ubiquitous marine gammaproteobacterial SAR86 (Béjà et al, 2000;Sabehi et al, 2004Sabehi et al, , 2005 and alphaproteobacterial SAR11 (Giovannoni et al, 2005a, b;Sabehi et al, 2005) groups, as well as in marine Bacteroidetes (Venter et al, 2004;Gó mez-Consarnau et al, 2007), planktonic Archaea (Frigaard et al, 2006) and other microbial taxa (de la Torre et al, 2003;Sabehi et al, 2003Sabehi et al, , 2005Venter et al, 2004;McCarren and DeLong, 2007).…”

“…PR spectral tuning was first observed among genes amplified directly from the environment by using highly specific polymerase chain reaction (PCR) primers (Béjà et al, 2001) to the gammaproteobacterial SAR86 group. These genes produced pigments of two distinct absorption spectra where 'greenabsorbing' PR (GPR) and 'blue-absorbing' PR (BPR) types shared 478% of their amino-acid residues (200 out of 247 are identical).…”