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

Abstract

Proteorhodopsins (PRs) phototrophy was recently discovered in oceanic surface waters. PRs have been observed in different marine environments and in diverse taxa, including the ubiquitous marine alphaproteobacterial SAR11 group and the uncultured gammaproteobacterial SAR86 group. Previously, two SAR86 PR subgroups, discovered in the Pacific Ocean, were shown to absorb light with different maxima, k max 527 nm (green) and k max 490 nm (blue) and their distribution was explained by prevailing light conditions -green pigments at the surface and blue in deeper waters. Here, we show that PRs display high diversity in geographically distinct patterns despite similar physical water column properties such as mixing and light penetration. We compared summer and winter samples representing stratified and mixed conditions from both the Mediterranean and Sargasso Sea. As expected, in the Mediterranean Sea, green pigments were mainly confined to the surface and the percentage of blue pigments increased toward deeper samples; in the Sargasso Sea, unexpectedly, all PRs were of the blue type. As an additional result, both locations show seasonal dependence in the distribution of different PR families. Finally, spectral tuning was not restricted to a single PR family as previously reported but occurs across the sampled PR families from various microbial taxa. The distribution of tunable PRs across the PR tree suggests that ready adaptability has been distributed widely among microorganisms, and may be a reason that PRs are abundant and taxonomically widely dispersed.

Widespread distribution of proteorhodopsins in freshwater and brackish ecosystems

“…Different GOS scaffolds (GS12 singleton-1096686052401, scaffold-1096627380104) that clustered within clade 6 and 7 were highly similar to P. ubique based on gene content but the genomic organization was different with an operon for carotene biosynthesis adjacent to the PR gene. Similar operon organization is observed in many uncultured PR-carrying organisms (Sabehi et al, 2005b(Sabehi et al, , 2007 but is different from the organization in P. ubique, where an acetyl-CoA synthetase and a ferredoxin are adjacent to the PR gene and the retinal biosynthesis operon is found elsewhere in the genome (Giovannoni et al, 2005a, b). We, therefore, assigned clades 6 and 7 as SAR11-related clades (Figure 1).…”

“…(Béjà et al, 2001)) to cover possible new PR diversity in brackish and freshwater ecosystems. The same PR regions were previously used to recover PRs from different marine environments and from BAC libraries (Sabehi et al, 2005b(Sabehi et al, , 2007Campbell et al, 2008). Four forward primers and twelve reverse primers (Table 2) were used to perform multiplex PCR reactions on Lake Kinneret samples.…”

“…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). The underwater light color of most freshwater ecosystems, however, is shifted towards the green and red part of the light spectrum (Kirk, 1994;Stomp et al, 2007a, b).…”

“…PRs have been observed in a wide variety of ocean regions (Béjà et al, 2000(Béjà et al, , 2001de la Torre et al, 2003;Sabehi et al, 2003Sabehi et al, , 2004Sabehi et al, , 2005aSabehi et al, , 2007Venter et al, 2004;Rusch et al, 2007;Campbell et al, 2008) and were found in diverse bacterial groups, including the ubiquitous marine gammaproteobacterial SAR86 (Béjà et al, 2000;Sabehi et al, 2004Sabehi et al, , 2005a and alphaproteobacterial SAR11 groups (Giovannoni et al, 2005a, b;Sabehi et al, 2005a), as well as in Roseobacter (alphaproteobacterium HTCC2255), 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, , 2005aVenter et al, 2004;McCarren and DeLong, 2007;Rusch et al, 2007). While previous work did not detect light enhanced growth neither in PR-containing SAR11 (Giovannoni et al, 2005a) nor 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 Flavobacteria (Gó mez- Consarnau et al, 2007).…”

Development of a "genome-proxy" microarray for profiling marine microbial communities, and its application to a time series in Monterey Bay, California

“…SAR86 has been commonly reported in marine samples (Eilers et al, 2000, Rappe et al, 2000, Suzuki et al, 2001, Morris et al, 2006, is known to partition with depth (Morris et al, 2006), and can comprise up to 10% of the cells in a community (Mullins et al, 1995, Eliers et al, 2000, Morris et al, 2006. Furthermore, it has been previously described as abundant in Monterey Bay, as 3-6% of total bacterial SSU DNAs in the Bay during an upwelling event (Suzuki et al, 2001), and as 5.6%, 5.5%, and 1.6% of the SSU operon-containing clones in 0m, 80m and 100m large-insert clone libraries from this location types have been hypothesized to be photoheterotrophs (Beja et al, 2000, Sabehi et al, 2004, Sabehi et al, 2005, Mou et al, 2007, Sabehi et al, 2007. The distribution of the SAR86-III clone also helped drive the differentiation of 30m…”