Abstract
Photochemical reaction centers and rhodopsins are the only phototrophic mechanisms known to have evolved on Earth. The minimal cost of bearing a rhodopsin-based phototrophic mechanism in comparison to maintaining a photochemical reaction center suggests that rhodopsin is the more abundant of the two. We tested this hypothesis by conducting a global abundance calculation of phototrophic mechanisms from 116 marine and terrestrial microbial metagenomes. On average, 48% of the cells from which these metagenomes were generated harbored a rhodopsin gene, exceeding the reaction center abundance by threefold. Evidence from metatranscriptomic data suggests that this genomic potential is realized to a substantial extent, at least for the small-sized (>0.8 μm) of microbial fractions.
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References
Alperovitch A, Sharon I, Rohwer F, Aro E-M, Glaser F, Milo R et al. (2011). Reconstructing a puzzle: existence of cyanophages containing both photosystem-I & photosystem-II gene suites inferred from oceanic metagenomic datasets. Environ Microbiol 13: 24–32.
Béjà O, Aravind L, Koonin EV, Suzuki MT, Haad A, Nguyen LP et al. (2000). Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289: 1902.
Béjà O, Fridman S, Glaser F . (2012). Viral clones from the GOS expedition with an unusual photosystem-I gene cassette organization. ISME J 6: 1617–1620.
Béjà O, Spudich EN, Spudich JL, Leclerc M, DeLong EF . (2001). Proteorhodopsin phototrophy in the ocean. Nature 411: 786–789.
Blokhina O, Virolainen E, Fagerstedt KV . (2003). Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91: 179.
Bryant DA, Frigaard N-U . (2006). Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol 14: 488.
Field CB, Behrenfeld MJ, Randerson JT, Falkowski P . (1998) Science 281: 237.
de la Torre JR, Christianson LM, Béjà O, Suzuki MT, Karl DM, Heidelberg J et al. (2003). Proteorhodopsin genes are distributed among divergent marine bacterial taxa. Proc Natl Acad Sci USA 100: 12830–12835.
Frias-Lopez J, Shi Y, Tyson GW, Coleman ML, Schuster SC, Chisholm SW et al. (2008). Microbial community gene expression in ocean surface waters. Proc Natl Acad Sci USA 105: 3805–3810.
Frigaard N-U, Martinez A, Mincer TJ, DeLong EF . (2006). Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea. Nature 439: 847.
Fuhrman JA, Schwalbach MS, Sting U . (2008). Proteorhodopsins: an array of physiological roles. Nat Rev Microbiol 6: 488.
Gifford SM, Sharma S, Rinta-Kanto JM, Moran MA . (2011). Quantitative analysis of a deeply sequenced marine microbial metatranscriptome. ISME J 5: 461–472.
Gilbert JA, Dawn F, Huang Y, Edwards. Li W, Gilna P, Joint I . (2008). Detection of large numbers of novel sequences in the metatranscriptomes of complex marine microbial communities. PloS One 3: e3024.
Giovannoni SJ, Bibbs L, Cho JC, Stapels MD, Desiderio R, Vergin KL et al. (2005). Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438: 82.
Hohmann-Marriott MF, Blankenship RE . (2011). Evolution of photosynthesis. Annu Rev Plant Biol 62: 515.
Lindell D, Sullivan MB, Johnson ZI, Tolonen AC, Rohwer F, Chisholm SW . (2004). Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc Natl Acad Sci USA 101: 11013–11018.
Mann NH, Cook A, Millard A, Bailey S, Clokie M . (2003). Bacterial photosynthesis genes in a virus. Nature 424: 741.
Marchetti A, Schruth DM, Durkin CA, Parker MS, Kodner RB, Berthiaume CT et al. (2012). Comparative metatranscriptomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability. Proc Natl Acad Sci USA 109: E317–E325.
Meyer F, Paarmann D, D’Souza M, Olson R, Glass EM, Kubal M et al. (2008). The metagenomics RAST server–a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9: 386.
Millard A, Clokie MRJ, Shub DA, Mann NH . (2004). Genetic organization of the psbAD region in phages infecting marine Synechococcus strains. Proc Natl Acad Sci USA 101: 11007–11012.
Molenaar D, van Berlo R, de Ridder D, Teusink B . (2009). Shifts in growth strategies reflect tradeoffs in cellular economics. Mol Syst Biol 5: 323.
Poretsky RS, Hewson I, Sun S, Allen AE, Zehr JP, Moran MA . (2009). Comparative day/night metatranscriptomic analysis of microbial communities in the North Pacific subtropical gyre. Environ Microbiol 11: 1358–1375.
Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S et al. (2007). The sorcerer ii global ocean sampling expedition: northwest atlantic through eastern tropical pacific. PLoS Biol 5: e77.
Sharon I, Alperovitch A, Rohwer F, Haynes M, Glaser F, Atamna-Ismaeel N et al. (2009). Photosystem-I gene cassettes are present in marine virus genomes. Nature 461: 258–262.
Sharon I, Tzahor S, Williamson S, Shmoish M, Man-Aharonovich D, Rusch DB et al. (2007). Viral photosynthetic reaction centre genes and transcripts in the marine environment. ISME J 1: 492–501.
Shi Y, Tyson GW, Eppley JM, Delong EF . (2010). Integrated metatranscriptomic and metagenomic analyses of stratified microbial assemblages in the open ocean. ISME J 5: 999–1013.
Spudich JL, Jung KH . (2005). Microbial rhodopsins: phylogenetic and functional diversity. In: Briggs WR, Spudich JL, (eds). Handbook of Photosensory Receptors. WILEY-VCH Verlag GmbH & Co: Weinheim, pp 1–24.
Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW . (2005). Three Prochlorococcus cyanophage genomes: Signature features and ecological interpretations. PLoS Biol 3: e144.
Sullivan MB, Lindell D, Lee JA, Thompson LR, Bielawski JP, Chisholm SW . (2006). Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol 4: e234.
Wraight CA, Clayton RK . (1974). The absolute quantum efficiency of bacteriochlorophyll photooxidation in reaction centers. Biochim Biophys Acta 333: 246.
Zeidner G, Bielawski JP, Shmoish M, Scanlan DJ, Sabehi G, Béjà O . (2005). Potential photosynthesis gene recombination between Prochlorococcus & Synechococcus via viral intermediates. Environ Microbiol 7: 1505–1513.
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Finkel, O., Béjà, O. & Belkin, S. Global abundance of microbial rhodopsins. ISME J 7, 448–451 (2013). https://doi.org/10.1038/ismej.2012.112
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DOI: https://doi.org/10.1038/ismej.2012.112
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