Diversification and spectral tuning in marine proteorhodopsins

Abstract

contributed equally to this work Proteorhodopsins, ubiquitous retinylidene photoactive proton pumps, were recently discovered in the cosmopolitan uncultured SAR86 bacterial group in oceanic surface waters. Two related proteorhodopsin families were found that absorb light with different absorption maxima, 525 nm (green) and 490 nm (blue), and their distribution was shown to be strati®ed with depth. Using structural modeling comparisons and mutagenesis, we report here on a single amino acid residue at position 105 that functions as a spectral tuning switch and accounts for most of the spectral difference between the two pigment families. Furthermore, looking at natural environments, we found novel proteorhodopsin gene clusters spanning the range of 540±505 nm and containing changes in the same identi®ed key switch residue leading to changes in their absorption maxima. The results suggest a simultaneous diversi®cation of green proteorhodopsin and the new key switch variant pigments. Our observations demonstrate that this single-residue switch mechanism is the major determinant of proteorhodopsin wavelength regulation in natural marine environments.

Widespread distribution of proteorhodopsins in freshwater and brackish ecosystems

“…In these waters, green-light conditions prevail (Stomp et al, 2007b;Haverkamp et al, 2008) and hence green-absorbing PRs will have a selective advantage compared to blue-absorbing PRs. Yet, the PRs described here show more variability in their protein sequence than in previous studies (Man et al, 2003) and are largely distinct from the marine clades (Figure 1). Therefore, prediction of the color of light absorbed by these freshwater PRs based on a single position (such as position 105) in the overall sequence should be made with great caution.…”

“…Figure 2). This makes them suspected greenabsorbing PRs (Man et al, 2003). The predominance of green-absorbing PRs can be explained by the underwater light spectrum in coastal and freshwater ecosystems.…”

“…Known PR genes encode pigments with two distinct light absorption spectra, commonly referred to as 'blueabsorbing' PR and 'green-absorbing' PR (Béjà et al, 2001;Man et al, 2003). Blue-absorbing PRs are particularly widespread in the blue ocean waters that have been extensively sampled in earlier PR studies (Béjà et al, 2001;Sabehi et al, 2007).…”

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

“…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).…”

“…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). Moreover, a single amino-acid change at position 105 (leucine for green, glutamine for blue) functions as a spectral tuning switch to account for most of the spectral difference (Man et al, 2003). Here, we sought to determine how common spectral tuning is among PRs from diverse taxonomic backgrounds, and to what extent their distribution correlates to distinct oceanic regimes by comparing PR sequence diversity from different depths and different seasons from two oligotrophic seas, the eastern Mediterranean and Sargasso Seas.…”