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Frontiers of Environmental Science & Engineering

ISSN 2095-2201

ISSN 2095-221X(Online)

CN 10-1013/X

Postal Subscription Code 80-973

2018 Impact Factor: 3.883

Front Envir Sci Eng    0, Vol. Issue () : 98-106    https://doi.org/10.1007/s11783-010-0278-y
RESEARCH ARTICLE
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.

Keywords proteorhodopsin (PR)      microorganism community      diversity      marine environments     
Corresponding Author(s): WEI Bo,Email:weibo88@gmail.com   
Issue Date: 01 February 2012
 Cite this article:   
Bo WEI. Diversity and distribution of proteorhodopsin-containing microorganisms in marine environments[J]. Front Envir Sci Eng, 0, (): 98-106.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-010-0278-y
https://academic.hep.com.cn/fese/EN/Y0/V/I/98
Fig.1  Map of global ocean indicating the four sampling profile sites; a mosaic base map of chlorophyll—remote sensed images (Aqua-MODIS; http://oceancolor.gsfc.nasa.gov/) from 2005 to 2006
Fig.1  Map of global ocean indicating the four sampling profile sites; a mosaic base map of chlorophyll—remote sensed images (Aqua-MODIS; http://oceancolor.gsfc.nasa.gov/) from 2005 to 2006
nucleotide similarity levelobserved number of OTUsNo. of unique OTUsestimated number of OTUs (ACE)estimated number of OTUs (chao1)shannon diversity indexcoverageof ACE/%
95%4462077527165.1559
80%213743032904.2770
70%150371841763.9382
50%741182803.3390
Tab.1  Richness and diversity as well as coverage estimates in all extract PR sequences based on comparison of number of OTUs calculated by the ACE nonparametric richness estimator and OTUs for varying percent protein sequence differences
Fig.2  Unrooted phylogenetic tree of 2100 PR sequences from global ocean samples that were extracted from GDDP with a bootstrap replicating 100 times. The taxonomy was noted around the tree
Fig.2  Unrooted phylogenetic tree of 2100 PR sequences from global ocean samples that were extracted from GDDP with a bootstrap replicating 100 times. The taxonomy was noted around the tree
Fig.3  Phylogenetic analysis of PR sequences retrieved from four profiles sits. The tree was constructed by Bayesian method. All the nodes of the tree were supported by more than 50% MCMC posterior probability. Additional symbols show the total number of clones and where were they retrieved as represented by a sequence. Scale bars 5% estimated sequence divergence for PR
Fig.3  Phylogenetic analysis of PR sequences retrieved from four profiles sits. The tree was constructed by Bayesian method. All the nodes of the tree were supported by more than 50% MCMC posterior probability. Additional symbols show the total number of clones and where were they retrieved as represented by a sequence. Scale bars 5% estimated sequence divergence for PR
Fig.4  PCoA of PR sequences among 12 clone libraries as calculated using unweighted UniFrac analysis
Fig.4  PCoA of PR sequences among 12 clone libraries as calculated using unweighted UniFrac analysis
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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