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Diversity and distribution of proteorhodopsin-containing microorganisms in marine environments |
Bo WEI() |
School of Life Sciences, Xiamen University, Xiamen 361005, China |
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Abstract Proteorhodopsin (PR) is a recently discovered protein involved in the utilization of light energy. Several studies have shown that PR-containing microorganisms are widespread and compose a large proportion of the biomass in marine ecosystems. A better understanding of the ecological role of PR will help clarify the effect of the global flow of energy and the carbon cycle on marine communities. In this study, a bioinformatical database of PR codon sequences, the Global Distribution Database of Proteorhodopsin (GDDP), as a tool for analyzing the diversity and distribution of PR-containing microorganisms in marine environments throughout the world was designed. The community structure of PR microorganisms were also compared using PCR assays and UniFrac analyses of 12 samples collected from three water layers (0, 75, and 200 m) at four representative sites in the Pacific, Atlantic, and Indian Oceans. The results indicate that PR-containing microorganisms can be grouped into two distribution types: widespread and location-specific. Representative cases of the former include SAR11-PR and HOT2C01-PR. Interestingly, PR communities cluster by geographic locale but not by water depth.
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Keywords
proteorhodopsin (PR)
microorganism community
diversity
marine environments
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Corresponding Author(s):
WEI Bo,Email:weibo88@gmail.com
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Issue Date: 01 February 2012
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1 |
Béjà O, Aravind L, Koonin E V, Suzuki M T, Hadd A, Nguyen L P, Jovanovich S B, Gates C M, Feldman R A, Spudich J L, Spudich E N, DeLong E F. Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science , 2000, 289(5486): 1902–1906 doi: 10.1126/science.289.5486.1902 pmid:10988064
|
2 |
Dioumaev A K, Wang J M, Bálint Z, Váró G, Lanyi J K. Proton transport by proteorhodopsin requires that the retinal Schiff base counterion Asp-97 be anionic. Biochemistry , 2003, 42(21): 6582–6587 doi: 10.1021/bi034253r pmid:12767242
|
3 |
de la Torre J R, Christianson L M, Béjà O, Suzuki M T, Karl D M, Heidelberg J, DeLong E F. Proteorhodopsin genes are distributed among divergent marine bacterial taxa. Proceedings of the National Academy of Sciences of the United States of America , 2003, 100(22): 12830–12835 doi: 10.1073/pnas.2133554100 pmid:14566056
|
4 |
Balashov S P, Imasheva E S, Boichenko V A, Antón J, Wang J M, Lanyi J K. Xanthorhodopsin: a proton pump with a light-harvesting carotenoid antenna. Science , 2005, 309(5743): 2061–2064 doi: 10.1126/science.1118046 pmid:16179480
|
5 |
Spudich J L, Yang C S, Jung K H, Spudich E N. Retinylidene proteins: structures and functions from archaea to humans. Annual Review of Cell and Developmental Biology , 2000, 16(1): 365–392 doi: 10.1146/annurev.cellbio.16.1.365 pmid:11031241
|
6 |
Sabehi G, Béjà O, Suzuki M T, Preston C M, DeLong E F. Different SAR86 subgroups harbour divergent proteorhodopsins. Environmental Microbiology , 2004, 6(9): 903–910 doi: 10.1111/j.1462-2920.2004.00676.x pmid:15305915
|
7 |
Frigaard N U, Martinez A, Mincer T J, DeLong E F. Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea. Nature , 2006, 439(7078): 847–850 doi: 10.1038/nature04435 pmid:16482157
|
8 |
McCarren J, DeLong E F. Proteorhodopsin photosystem gene clusters exhibit co-evolutionary trends and shared ancestry among diverse marine microbial phyla. Environmental Microbiology , 2007, 9(4): 846–858 doi: 10.1111/j.1462-2920.2006.01203.x pmid:17359257
|
9 |
G?mez-Consarnau L, González J M, Coll-Llad? M, Gourdon P, Pascher T, Neutze R, Pedr?s-Ali? C, Pinhassi J. Light stimulates growth of proteorhodopsincontaining marine Flavobacteria. Nature , 2007, 445: 210–213 pmid:17215843
|
10 |
Campbell B J, Waidner L A, Cottrell M T, Kirchman D L. Abundant proteorhodopsin genes in the North Atlantic Ocean. Environmental Microbiology , 2008, 10(1): 99–109 pmid:18211270
|
11 |
Sabehi G, Kirkup B C, Rozenberg M, Stambler N, Polz M F, Béjà O. Adaptation and spectral tuning in divergent marine proteorhodopsins from the eastern Mediterranean and the Sargasso Seas. The ISME Journal , 2007, 1(1): 48–55 doi: 10.1038/ismej.2007.10 pmid:18043613
|
12 |
Rusch D B, Halpern A L, Sutton G, Heidelberg K B, Williamson S, Yooseph S, Wu D, Eisen J A, Hoffman J M, Remington K, Beeson K, Tran B, Smith H, Baden-Tillson H, Stewart C, Thorpe J, Freeman J, Andrews-Pfannkoch C, Venter J E, Li K, Kravitz S, Heidelberg J F, Utterback T, Rogers Y H, Falcón L I, Souza V, Bonilla-Rosso G, Eguiarte L E, Karl D M, Sathyendranath S, Platt T, Bermingham E, Gallardo V, Tamayo-Castillo G, Ferrari M R, Strausberg R L, Nealson K, Friedman R, Frazier M, Venter J C. The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biology , 2007, 5(3): e77 doi: 10.1371/journal.pbio.0050077 pmid:17355176
|
13 |
Fuhrman J A, Schwalbach M S, Stingl U. Proteorhodopsins: an array of physiological roles. Nature Reviews Microbiology , 2008, 6(6): 488–494 pmid:18475306
|
14 |
Giovannoni S J, Bibbs L, Cho J C, Stapels M D, Desiderio R, Vergin K L, Rappé M S, Laney S, Wilhelm L J, Tripp H J, Mathur E J, Barofsky D F. Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature , 2005, 438(7064): 82–85 doi: 10.1038/nature04032 pmid:16267553
|
15 |
Stingl U, Desiderio R A, Cho J C, Vergin K L, Giovannoni S J. The SAR92 clade: an abundant coastal clade of culturable marine bacteria possessing proteorhodopsin. Applied and Environmental Microbiology , 2007, 73(7): 2290–2296 doi: 10.1128/AEM.02559-06 pmid:17293499
|
16 |
Thompson J D, Gibson T J, Plewniak F, Jeanmougin F, Higgins D G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research , 1997, 25(24): 4876–4882 doi: 10.1093/nar/25.24.4876 pmid:9396791
|
17 |
Francis C A, Roberts K J, Beman J M, Santoro A E, Oakley B B. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proceedings of the National Academy of Sciences of the United States of America , 2005, 102(41): 14683–14688 doi: 10.1073/pnas.0506625102 pmid:16186488
|
18 |
Sabehi G, Loy A, Jung K H, Partha R, Spudich J L, Isaacson T, Hirschberg J, Wagner M, Béjà O, Eisen J. New insights into metabolic properties of marine bacteria encoding proteorhodopsins. PLoS Biology , 2005, 3(8): e273 doi: 10.1371/journal.pbio.0030273 pmid:16008504
|
19 |
Altschul S F, Madden T L, Sch?ffer A A, Zhang J, Zhang Z, Miller W, Lipman D J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research , 1997, 25(17): 3389–3402 doi: 10.1093/nar/25.17.3389 pmid:9254694
|
20 |
Schloss P D, Handelsman J. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Applied and Environmental Microbiology , 2005, 71(3): 1501–1506 doi: 10.1128/AEM.71.3.1501-1506.2005 pmid:15746353
|
21 |
Lozupone C, Hamady M, Knight R. UniFrac—an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics , 2006, 7(1): 371 doi: 10.1186/1471-2105-7-371 pmid:16893466
|
22 |
Ronquist F, Huelsenbeck J P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (Oxford, England) , 2003, 19(12): 1572–1574 doi: 10.1093/bioinformatics/btg180 pmid:12912839
|
23 |
McGuire G, Wright F. TOPAL 2.0: improved detection of mosaic sequences within multiple alignments. Bioinformatics (Oxford, England) , 2000, 16(2): 130–134 doi: 10.1093/bioinformatics/16.2.130 pmid:10842734
|
24 |
Venter J C, Remington K, Heidelberg J F, Halpern A L, Rusch D, Eisen J A, Wu D Y, Paulsen I, Nelson K E, Nelson W, Fouts D E, Levy S, Knap A H, Lomas M W, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers Y H, Smith H O. Environmental genome shotgun sequencing of the Sargasso Sea. Science , 2004, 304(5667): 66–74 doi: 10.1126/science.1093857 pmid:15001713
|
25 |
Jiao N, Zhang Y, Zeng Y, Hong N, Liu R, Chen F, Wang P. Distinct distribution pattern of abundance and diversity of aerobic anoxygenic phototrophic bacteria in the global ocean. Environmental Microbiology , 2007, 9(12): 3091–3099 doi: 10.1111/j.1462-2920.2007.01419.x pmid:17991036
|
26 |
Penno S, Lindell D, Post A F. Diversity of Synechococcus and Prochlorococcus populations determined from DNA sequences of the N-regulatory gene ntcA. Environmental Microbiology , 2006, 8(7): 1200–1211 doi: 10.1111/j.1462-2920.2006.01010.x pmid:16817928
|
27 |
Morris R M, Rappé M S, Connon S A, Vergin K L, Siebold W A, Carlson C A, Giovannoni S J. SAR11 clade dominates ocean surface bacterioplankton communities. Nature , 2002, 420(6917): 806–810 doi: 10.1038/nature01240 pmid:12490947
|
28 |
Baas-Becking L G M. Geobiologie of inleiding tot demilieukunde (W P van Stockum & Zoon N V, The Hague, Netherlands, 1934)
|
29 |
Cottrell M T, Kirchman D L. Photoheterotrophic microbes in the Arctic Ocean in summer and winter. Applied and Environmental Microbiology , 2009, 75(15): 4958–4966 doi: 10.1128/AEM.00117-09 pmid:19502441
|
30 |
Béjà O, Spudich E N, Spudich J L, Leclerc M, DeLong E F. Proteorhodopsin phototrophy in the ocean. Nature , 2001, 411(6839): 786–789 doi: 10.1038/35081051 pmid:11459054
|
31 |
Sabehi G, Massana R, Bielawski J P, Rosenberg M, Delong E F, Béjà O. Novel Proteorhodopsin variants from the Mediterranean and Red Seas. Environmental Microbiology , 2003, 5(10): 842–849 doi: 10.1046/j.1462-2920.2003.00493.x pmid:14510837
|
32 |
Gómez-Consarnau L, González J M, Coll-Lladó M, Gourdon P, Pascher T, Neutze R, Pedrós-Alió C, Pinhassi J. Light stimulates growth of proteorhodopsin-containing marine Flavobacteria. Nature , 2007, 445(7124): 210–213 doi: 10.1038/nature05381 pmid:17215843
|
33 |
DeLong E F, Preston C M, Mincer T, Rich V, Hallam S J, Frigaard N U, Martinez A, Sullivan M B, Edwards R, Brito B R, Chisholm S W, Karl D M. Community genomics among stratified microbial assemblages in the ocean’s interior. Science , 2006, 311(5760): 496–503 doi: 10.1126/science.1120250 pmid:16439655
|
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