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Diversity and evolution of phycobilisomes in marine Synechococcus spp.: a comparative genomics study

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Six, Christophe, Thomas, Jean-Claude , Garczarek, Laurence, Ostrowski, Martin, Dufresne, Alexis , Blot, Nicolas, Scanlan, David J. and Partensky, Frédéric. (2007) Diversity and evolution of phycobilisomes in marine Synechococcus spp.: a comparative genomics study. Genome Biology, Vol.8 (No.12). ISSN 1474-7596

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Official URL: http://dx.doi.org/10.1186/gb-2007-8-12-r259

Abstract

Background Marine Synechococcus owe their specific vivid color (ranging from blue-green to orange) to their large extrinsic antenna complexes called phycobilisomes, comprising a central allophycocyanin core and rods of variable phycobiliprotein composition. Three major pigment types can be defined depending on the major phycobiliprotein found in the rods (phycocyanin, phycoerythrin I or phycoerythrin II). Among strains containing both phycoerythrins I and II, four subtypes can be distinguished based on the ratio of the two chromophores bound to these phycobiliproteins. Genomes of eleven marine Synechococcus strains recently became available with one to four strains per pigment type or subtype, allowing an unprecedented comparative genomics study of genes involved in phycobilisome metabolism. Results By carefully comparing the Synechococcus genomes, we have retrieved candidate genes potentially required for the synthesis of phycobiliproteins in each pigment type. This includes linker polypeptides, phycobilin lyases and a number of novel genes of uncharacterized function. Interestingly, strains belonging to a given pigment type have similar phycobilisome gene complements and organization, independent of the core genome phylogeny (as assessed using concatenated ribosomal proteins). While phylogenetic trees based on concatenated allophycocyanin protein sequences are congruent with the latter, those based on phycocyanin and phycoerythrin notably differ and match the Synechococcus pigment types. Conclusion We conclude that the phycobilisome core has likely evolved together with the core genome, while rods must have evolved independently, possibly by lateral transfer of phycobilisome rod genes or gene clusters between Synechococcus strains, either via viruses or by natural transformation, allowing rapid adaptation to a variety of light niches.

Item Type:	Journal Article
Subjects:	Q Science > QK Botany Q Science > QR Microbiology
Divisions:	Faculty of Science > Life Sciences (2010- ) > Biological Sciences ( -2010)
Library of Congress Subject Headings (LCSH):	Cyanobacterial blooms, Gene mapping, Phycobilisomes
Journal or Publication Title:	Genome Biology
Publisher:	BioMed Central Ltd.
ISSN:	1474-7596
Date:	5 December 2007
Volume:	Vol.8
Number:	No.12
Identification Number:	10.1186/gb-2007-8-12-r259
Status:	Peer Reviewed
Access rights to Published version:	Open Access
Funder:	Natural Environment Research Council (Great Britain) (NERC), France. Agence nationale de la recherche (ANR), European Commission (EC)
Grant number:	NE/C000536/1 (NERC)
References:	1. Johnson PW, Sieburth JM: Chroococcoid cyanobacteria in the sea: a ubiquitous and diverse phototrophic biomass. Limnol Oceanogr 1979, 24:928-935. 2. Waterbury JB, Watson SW, Guillard RRL, Brand LE: Widespread occurrence of a unicellular, marine planktonic, cyanobacterium. Nature 1979, 277:293-294. 3. Gradinger R, Lenz J: Seasonal occurrence of picocyanobacteria in the Greenland Sea and central Arctic Ocean. Polar Biol 1995, 15:447-452. 4. Partensky F, Blanchot J, Lantoine F, Neveux J, Marie D: Vertical structure of picophytoplankton at different trophic sites of the tropical northeastern Atlantic Ocean. Deep-Sea Res I 1996, 43:1191-1213. 5. Zubkov MV, Sleigh MA, Tarran GA, Burkill PH, Leakey RJG: Picoplanktonic community structure on an Atlantic transect from 50 degrees N to 50 degrees S. Deep-Sea Res I 1998, 45:1339-1355. 6. Waterbury JB, Watson SW, Valois FW, Franks DG: Biological and ecological characterization of the marine unicellular cyanobacterium Synechococcus. Can Bull Fish Aquat Sci 1986, 472:71-120. 7. Olson RJ, Zettler ER, Armbrust EV, Chisholm SW: Pigment, size and distribution of Synechococcus in the North Atlantic and Pacific oceans. Limnol Oceanogr 1990, 35:45-58. 8. Partensky F, Blanchot J, Vaulot D: Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: a review. In Marine Cyanobacteria Volume 19. Edited by: Charpy L, Larkum A. Monaco: Musée Oceanographique; 1999:457-475. 9. Scanlan DJ, West NJ: Molecular ecology of the marine cyanobacterial genera Prochlorococcus and Synechococcus. FEMS Microbiol Ecol 2002, 40:1-12. 10. Scanlan DJ: Physiological diversity and niche adaptation in marine Synechococcus. Adv Microb Physiol 2003, 47:1-64. 11. Glazer AN, Williams RC, Yeh SW, Clark JH: Kinetics of energy flow in the phycobilisome core. Science 1985, 230:1051-1053. 12. Glazer AN: Light guides - directional energy transfer in a photosynthetic antenna. J Biol Chem 1989, 264:1-4. 13. Grossman AR, Schaefer MR, Chiang GG, Collier JL: The responses of cyanobacteria to environmental conditions: light and nutrients. In The Molecular Biology of Cyanobacteria Edited by: Bryant DA. Dordrecht: Kluwer Academic Publishers; 1994:677-692. 14. MacColl R: Cyanobacterial phycobilisomes. J Struct Biol 1998, 124:311-334. 15. Sidler WA: Phycobilisome and phycobiliprotein structure. In The Molecular Biology of Cyanobacteria Edited by: Bryant DA. Netherlands: Kluwer Academic Publishers; 1994:139-216. 16. Ong LJ, Glazer AN: R-phycocyanin II, a new phycocyanin occurring in marine Synechococcus species. J Biol Chem 1987, 262:6323-6327. 17. Ong LJ, Glazer AN: Structural studies of phycobiliproteins in unicellular marine cyanobacteria. In Light-energy Transduction in Photosynthesis: Higher Plant and Bacterial Models Edited by: Stevens SEJ, Bryant DA. Rockville, MD: American Society of Plant Physiologists; 1988:102-121. 18. Ong LJ, Glazer AN: Phycoerythrins of marine unicellular cyanobacteria. I. Bilin types and locations and energy transfer pathways in Synechococcus spp. phycoerythrins. J Biol Chem 1991, 266:9515-9527. 19. Six C, Thomas JC, Thion L, Lemoine Y, Zal F, Partensky F: Two novel phycoerythrin-associated linker proteins in the marine cyanobacterium Synechococcus sp. strain WH8102. J Bacteriol 2005, 187:1685-1694. 20. Everroad RC, Wood AM: Comparative molecular evolution of newly discovered picocyanobacterial strains reveals a phylogenetically informative variable region of beta-phycoerythrin. J Phycol 2006, 42:1300-1311. 21. Wilbanks SM, Glazer AN: Rod structure of a phycoerythrin IIcontaining phycobilisome. II. Complete sequence and bilin attachment site of a phycoerythrin γ subunit. J Biol Chem 1993, 268:1236-1241. 22. Urbach E, Scanlan DJ, Distel DL, Waterbury JB, Chisholm SW: Rapid diversification of marine picophytoplankton with dissimilar light-harvesting structures inferred from sequences of Prochlorococcus and Synechococcus (Cyanobacteria). J Mol Evol 1998, 46:188-201. 23. Fuller NJ, Marie D, Partensky F, Vaulot D, Post AF, Scanlan DJ: Clade-specific 16S ribosomal DNA oligonucleotides reveal the predominance of a single marine Synechococcus clade throughout a stratified water column in the Red Sea. Appl Environ Microbiol 2003, 69:2430-2443. 24. Ahlgren NA, Rocap G: Culture isolation and culture-independent clone libraries reveal new marine Synechococcus ecotypes with distinctive light and N physiologies. Appl Environ Microbiol 2006, 72:7193-7204. 25. Chen F, Wang K, Kan J, Suzuki MT, Wommack KE: Diverse and unique picocyanobacteria in Chesapeake Bay, revealed by 16S-23S rRNA internal transcribed spacer sequences. Appl Environ Microbiol 2006, 72:2239-2243. 26. Herdman M, Castenholz RW, Waterbury JB, Rippka R: Form-genus XIII. Synechococcus. In Bergey's Manual of Systematic Bacteriology Volume 1. 2nd edition. Edited by: Boone DR, Castenholz RW. New York: Springer-Verlag; 2001:508-512. 27. Waterbury J, Rippka R: Order Chroococcales Wettstein Emend. Rippka et al., 1979. In Bergey's Manual of Systematic Bacteriology Edited by: Krieg N, Holt J. Baltimore: Williams and Wilkins; 1989:1728-1746. 28. Toledo G, Palenik B, Brahamsha B: Swimming marine Synechococcus strains with widely different photosynthetic pigment ratios form a monophyletic group. Appl Environ Microbiol 1999, 65:5247-5251. 29. Penno S, Lindell D, Post AF: Diversity of Synechococcus and Prochlorococcus populations determined from DNA sequences of the N-regulatory gene ntcA. Environ Microbiol 2006, 8:1200-1211. 30. Wood AM, Phinney DA, Yentsch CS: Water column transparency and the distribution of spectrally distinct forms of phycoerythrin- containing organisms. Mar Ecol Prog Ser 1998, 162:25-31. 31. Wood AM, Lipsen M, Coble P: Fluorescence-based characterization of phycoerythrin-containing cyanobacterial communities in the Arabian Sea during the Northeast and early Southwest Monsoon (1994-1995). Deep-Sea Res II 1999, 46:1769-1790. 32. Six C, Thomas J-C, Brahamsha B, Lemoine Y, Partensky F: Photophysiology of the marine cyanobacterium Synechococcus sp. WH a new model organism. Aquat Microb Ecol 2004, 35:17-29. 33. Palenik B: Chromatic adaptation in marine Synechococcus strains. Appl Environ Microbiol 2001, 67:991-994. 34. Everroad C, Six C, Partensky F, Thomas J-C, Holtzendorff J, Wood AM: Biochemical bases of type IV chromatic adaptation in marine Synechococcus spp. J Bacteriol 2006, 188:3345-3356. 35. Jones H, Ostrowski M, Scanlan DJ: A suppression subtractive hybridization approach reveals niche-specific genes that may be involved in predator avoidance in marine Synechococcus isolates. Appl Environ Microbiol 2006, 72:2730-2737. 36. Alberte RS, Wood AM, Kursar TA, Guillard RRL: Novel phycoerythrins in marine Synechococcus spp. Plant Physiol 1984, 75:732-739. 37. Wilbanks SM, Glazer AN: Rod structure of a phycoerythrin IIcontaining phycobilisome. I. Organization and sequence of the gene cluster encoding the major phycobiliprotein rod components in the genome of marine Synechococcus sp. WH8020. J Biol Chem 1993, 268:1226-1235. 38. Frankenberg N, Mukougawa K, Kohchi T, Lagarias JC: Functional genomic analysis of the HY2 family of ferredoxin-dependent bilin reductases from oxygenic photosynthetic organisms. Plant Cell 2001, 13:965-978. 39. Cobley JG, Clark AC, Weerasurya S, Queseda FA, Xiao JY, Bandrapali N, D'Silva I, Thounaojam M, Oda JF, Sumiyoshi T, Chu MH: CpeR is an activator required for expression of the phycoerythrin operon (cpeBA) in the cyanobacterium Fremyella diplosiphon and is encoded in the phycoerythrin linker-polypeptide operon (cpeCDESTR). Mol Microbiol 2002, 44:1517-1531. 40. Montgomery BL, Casey ES, Grossman AR, Kehoe DM: AplA, a member of a new class of phycobiliproteins lacking a traditional role in photosynthetic light harvesting. J Bacteriol 2004, 186:7420-7428. 41. Capuano V, Braux AS, Tandeau de Marsac N, Houmard J: The "anchor polypeptide" of cyanobacterial phycobilisomes. Molecular characterization of the Synechococcus sp. PCC 6301 apcE gene. J Biol Chem 1991, 266:7239-7247. 42. Fairchild CD, Zhao J, Zhou J, Colson SE, Bryant DA, Glazer AN: Phycocyanin alpha-subunit phycocyanobilin lyase. Proc Natl Acad Sci USA 1992, 89:7017-7021. 43. Fairchild CD, Glazer AN: Oligomeric structure, enzyme kinetics, and substrate specificity of the phycocyanin alpha subunit phycocyanobilin lyase. J Biol Chem 1994, 269:8686-8694. 44. Bhalerao RP, Lind LK, Gustafsson P: Cloning of the cpcE and cpcF genes from Synechococcus sp. PCC 6301 and their inactivation in Synechococcus sp. PCC 7942. Plant Mol Biol 1994, 26:313-326. 45. Swanson RV, Zhou J, Leary JA, Williams T, de Lorimier R, Bryant DA, Glazer AN: Characterization of phycocyanin produced by cpcE and cpcF mutants and identification of an intergenic suppressor of the defect in bilin attachment. J Biol Chem 1992, 267:16146-16154. 46. Zhao KH, Wu D, Zhang L, Zhou M, Bohm S, Bubenzer C, Scheer H: Chromophore attachment in phycocyanin - functional amino acids of phycocyanobilin-alpha-phycocyanin lyase and evidence for chromophore binding. FEBS J 2006, 273:1262-1274. 47. Zhao KH, Deng MG, Zheng M, Zhou M, Parbel A, Storf M, Meyer M, Strohmann B, Scheer H: Novel activity of a phycobiliprotein lyase: both the attachment of phycocyanobilin and the isomerization to phycoviolobilin are catalyzed by the proteins PecE and PecF encoded by the phycoerythrocyanin operon. FEBS Lett 2000, 469:9-13. 48. Storf M, Parbel A, Meyer M, Strohmann B, Scheer H, Deng MG, Zheng M, Zhou M, Zhao KH: Chromophore attachment to biliproteins: Specificity of PecE/PecF, a lyase-isomerase for the photoactive 3(1)-Cys-alpha 84-phycoviolobilin chromophore of phycoerythrocyanin. Biochemistry 2001, 40:12444-12456. 49. Zhao KH, Ping S, Bohm S, Bo S, Ming Z, Bubenzer C, Scheer H: Reconstitution of phycobilisome core-membrane linker, LCM, by autocatalytic chromophore binding to ApcE. Biochim Biophys Acta 2005, 1706:81-87. 50. Shen G, Saunée NA, Williams SR, Gallo EF, Schluchter WM, Bryant DA: Identification and characterization of a new class of bilin lyase: the cpcT gene encodes a bilin lyase responsible for attachment of phycocyanobilin to Cys-153 on the beta subunit of phycocyanin in Synechococcus sp. PCC 7002. J Biol Chem 2006, 281:17768-17778. 51. Zhao KH, Su P, Li J, Tu JM, Zhou M, Bubenzer C, Scheer H: Chromophore attachment to phycobiliprotein beta-subunits: phycocyanobilin: cystein-beta84 phycobiliprotein lyase activity of CpeS-like protein from Anabaena sp. PCC7120. J Biol Chem 2006, 281:8573-8581. 52. Zhao K, Su P, Tu J, Wang X, Liu H, Plöscher M, Eichacker L, Yang B, Zhou M, Scheer H: Phycobilin:cystein-84 biliprotein lyase, a near-universal lyase for cysteine-84-binding sites in cyanobacterial phycobiliproteins. Proc Natl Acad Sci USA 2007, 104:14300-14305. 53. Kahn K, Mazel D, Houmard J, Tandeau de Marsac N, Schaefer MR: A role for cpeYZ in cyanobacterial phycoerythrin biosynthesis. J Bacteriol 1997, 179:998-1006. 54. Jacobson M, Brigle K, Bennett L, Setterquist R, Wilson M, Cash V, Beynon J, Newton W, Dean D: Physical and genetic map of the major nif gene cluster from Azotobacter vinelandii. J Bacteriol 1989, 171:1017-1027. 55. Hagiwara Y, Sugishima M, Takahashi Y, Fukuyama K: Crystal structure of phycocyanobilin: ferredoxin oxidoreductase in complex with biliverdin IX alpha, a key enzyme in the biosynthesis of phycocyanobilin. Proc Natl Acad Sci USA 2006, 103:27-32. 56. Bickel PJ, Kechris KJ, Spector PC, Wedemayer GJ, Glazer AN: Finding important sites in protein sequences. Proc Natl Acad Sci USA 2002, 99:14764-14771. 57. Kehoe DM, Gutu A: Responding to color: The regulation of complementary chromatic adaptation. Ann Rev Plant Biol 2006, 57:127-150. 58. Ducret A, Muller SA, Goldie KN, Hefti A, Sidler WA, Zuber H, Engel A: Reconstitution, characterisation and mass analysis of the pentacylindrical allophycocyanin core complex from the cyanobacterium Anabaena sp. PCC 7120. J Mol Biol 1998, 278:369-388. 59. Elmorjani K, Thomas J-C, Sebban P: Phycobilisomes of wild type and pigment mutants of the cyanobacterium Synechocystis PCC 6803. Arch Microbiol 1986, 146:186-191. 60. Glazer AN: Phycobilisome: a macromolecular complex optimized for light energy transfer. Biochim Biophys Acta 1984, 768:29-51. 61. Federspiel NA, Grossman AR: Characterization of the light-regulated operon encoding the phycoerythrin-associated linker proteins from the cyanobacterium Fremyella diplosiphon. J Bacteriol 1990, 172:4072-4081. 62. Haverkamp T, Acinas SG, Doeleman M, Stomp M, Huisman J, Stal LJ: Diversity and phylogeny of Baltic Sea picocyanobacteria inferred from their ITS and phycobiliprotein operons. Environ Microbiol 2007. 63. Apt KE, Collier JL, Grossman AR: Evolution of the phycobiliproteins. J Mol Biol 1995, 248:79-96. 64. Lindell D, Sullivan MB, Johnson ZI, Tolonen AC, Rohwer F, Chisholm SW: Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc Natl Acad Sci USA 2004, 101:11013-11018. 65. Mann NH, Clokie MR, Millard A, Cook A, Wilson WH, Wheatley PJ, Letarov A, Krisch HM: The genome of S-PM2, a "photosynthetic" T4-type bacteriophage that infects marine Synechococcus strains. J Bacteriol 2005, 187:3188-3200. 66. Weigele PR, Pope WH, Pedulla ML, Houtz JM, Smith AL, Conway JF, King J, Hatfull GF, Lawrence JG, Hendrix RW: Genomic and structural analysis of Syn9, a cyanophage infecting marine Prochlorococcus and Synechococcus. Environ Microbiol 2007, 9:1675-1695. 67. Clokie MRJ, Mann NH: Marine cyanophages and light. Environ Microbiol 2006, 8:2074-2082. 68. Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW: Three Prochlorococcus cyanophage genomes: Signature features and ecological interpretations. PLOS Biol 2005, 3:790-806. 69. Rippka R, Coursin T, Hess W, Lichtlé C, Scanlan DJ, Palinska KA, Iteman I, Partensky F, Houmard J, Herdman M: Prochlorococcus marinus Chisholm et al. 1992 subsp. pastoris subsp. nov. strain PCC the first axenic chlorophyll a2/b2-containing cyanobacterium (Oxyphotobacteria). Intl J Syst Evol Microbiol 2000, 50:1833-1847. 70. Altschul S, Madden T, Schaffer A, Zhang J, Zhang Z, Miller W, Lipman D: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402. 71. Enright AJ, van Dongen S, Ouzounis CA: An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 2002, 30:1575-1584. 72. Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-4680. 73. Gadagkar SR, Rosenberg MS, Kumar S: Inferring species phylogenies from multiple genes: concatenated sequence tree versus consensus gene tree. J Exp Zool B 2005, 304:64-74. 74. Galtier N, Gouy M, Gautier C: SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 1996, 12:543-548. 75. Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704. 76. Kumar S, Tamura K, Nei M: MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 2004, 5:150-163. 77. Berlyn MK: Linkage map of Escherichia coli K-12, edition 10: the traditional map. Microbiol Mol Biol Rev 1998, 62:814-984.
URI:	http://wrap.warwick.ac.uk/id/eprint/544