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

Genome Biology

Volumn 8, Issue 12, 2007, Pages

  Six, Christophe ^a,b   Thomas, Jean Claude ^c   Garczarek, Laurence ^a   Ostrowski, Martin ^d   Dufresne, Alexis ^a   Blot, Nicolas ^a   Scanlan, David J ^d   Partensky, Frédéric ^a  

^a STATION BIOLOGIQUE DE ROSCOFF   (France)

^b MOUNT ALLISON UNIVERSITY   (Canada)

^c ECOLE NORMALE SUPÉRIEURE   (France)

^d UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOPHYCOCYANIN; AMINO ACID; LYASE; PHYCOBILIN; PHYCOBILIPROTEIN; PHYCOCYANIN; PHYCOERYTHRIN; POLYPEPTIDE; RIBOSOME PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; GENE CLUSTER; GENE FUNCTION; GENE NUMBER; GENETIC COMPLEMENTATION; GENETIC CONSERVATION; GENETIC ORGANIZATION; GENETIC VARIABILITY; GENOMICS; MARINE BACTERIUM; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYCOBILISOME; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; SYNECHOCOCCUS; CLASSIFICATION; COMPARATIVE STUDY; GENETICS; METABOLISM; MOLECULAR EVOLUTION; PHYLOGENY;

SYNECHOCOCCUS;

EVOLUTION, MOLECULAR; GENOMICS; PHYCOBILIPROTEINS; PHYCOBILISOMES; PHYLOGENY; SYNECHOCOCCUS;

EID: 40449089171     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2007-8-12-r259     Document Type: Article

References (77)

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 10.1038/277293a0
3. Gradinger R Lenz J Seasonal occurrence of picocyanobacteria in the Greenland Sea and central Arctic Ocean. Polar Biol 1995 15 447-452 10.1007/BF00239722
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 10.1016/ 0967-0637(96)00056-8
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 10.1016/S0967-0637(98)00015-6
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. Marine Cyanobacteria Monaco: Musée Oceanographique Charpy L, Larkum A 1999 19 457-475
9. Scanlan DJ West NJ Molecular ecology of the marine cyanobacterial genera Prochlorococcus and Synechococcus. FEMS Microbiol Ecol 2002 40 1-12 10.1111/j.1574-6941.2002.tb00930.x
10. Scanlan DJ Physiological diversity and niche adaptation in marine Synechococcus. Adv Microb Physiol 2003 47 1-64 14560662
11. Glazer AN Williams RC Yeh SW Clark JH Kinetics of energy flow in the phycobilisome core. Science 1985 230 1051-1053 10.1126/ science.230.4729.1051 17814931
12. Glazer AN Light guides - directional energy transfer in a photosynthetic antenna. J Biol Chem 1989 264 1-4 2491842
13. Grossman AR Schaefer MR Chiang GG Collier JL The responses of cyanobacteria to environmental conditions: Light and nutrients. The Molecular Biology of Cyanobacteria Dordrecht: Kluwer Academic Publishers Bryant DA 1994 677-692
14. MacColl R Cyanobacterial phycobilisomes. J Struct Biol 1998 124 311-334 10.1006/jsbi.1998.4062 10049814
15. Sidler WA Phycobilisome and phycobiliprotein structure. The Molecular Biology of Cyanobacteria Netherlands: Kluwer Academic Publishers Bryant DA 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 3571260
17. Ong LJ Glazer AN Structural studies of phycobiliproteins in unicellular marine cyanobacteria. Light-energy Transduction in Photosynthesis: Higher Plant and Bacterial Models Rockville, MD: American Society of Plant Physiologists Stevens SEJ, Bryant DA 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 1903388
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 1064003 15716439 10.1128/JB.187.5.1685-1694.2005
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 10.1111/j.1529-8817.2006.00282.x
21. Wilbanks SM Glazer AN Rod structure of a phycoerythrin II-containing phycobilisome. II. Complete sequence and bilin attachment site of a phycoerythrin γ subunit. J Biol Chem 1993 268 1236-1241 8419326
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 10.1007/ PL00006294 9452521
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 154553 12732508 10.1128/AEM.69.5.2430-2443.2003
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 1636174 16936060 10.1128/AEM.00358-06
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 1393199 16517680 10.1128/AEM.72.3.2239-2243.2006
26. Herdman M Castenholz RW Waterbury JB Rippka R Form-genus XIII. Synechococcus. Bergey's Manual of Systematic Bacteriology New York: Springer-Verlag Boone DR, Castenholz RW 2 2001 1 508-512
27. Waterbury J Rippka R Order Chroococcales Wettstein Emend. Rippka et al., 1979. Bergey's Manual of Systematic Bacteriology Baltimore: Williams and Wilkins Krieg N, Holt J 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 91712 10583972
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 10.1111/j.1462-2920.2006.01010.x 16817928
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 10.3354/meps162025
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 10.1016/S0967-0645(99)00043-0
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 10.3354/ame035017
33. Palenik B Chromatic adaptation in marine Synechococcus strains. Appl Environ Microbiol 2001 67 991-994 92680 11157276 10.1128/ AEM.67.2.991-994.2001
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 1447437 16621829 10.1128/JB.188.9.3345-3356.2006
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 1449036 16597977 10.1128/AEM.72.4.2730-2737.2006
36. Alberte RS Wood AM Kursar TA Guillard RRL Novel phycoerythrins in marine Synechococcus spp. Plant Physiol 1984 75 732-739 1066985 16663696
37. Wilbanks SM Glazer AN Rod structure of a phycoerythrin II-containing 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 8419325
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 135530 11283349 10.1105/tpc.13.4.965
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 10.1046/j.1365-2958.2002.02966.x 12067341
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 523187 15489454 10.1128/ JB.186.21.7420-7428.2004
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 1901865
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 49636 1495995 10.1073/pnas.89.15.7017
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 8132596
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 10.1007/BF00039542 7524727
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 1644802
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 10.1111/j.1742-4658.2006.05149.x 16519690
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 10.1016/ S0014-5793(00)01245-X 10708746
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 10.1021/bi010776s 11591166
49. Zhao KH Ping S Bohm S Bo S Ming Z Bubenzer C Scheer H Reconstitution of phycobilisome core-membrane linker, L-CM, by autocatalytic chromophore binding to ApcE. Biochim Biophys Acta 2005 1706 81-87 10.1016/ j.bbabio.2004.09.008 15620367
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 10.1074/ jbc.M602563200 16644722
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 10.1074/jbc.M513796200 16452471
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 1955460 17726096 10.1073/ pnas.0706209104
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 178790 9023176
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 209696 2644218
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 1324987 16380422 10.1073/pnas.0507266103
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 137493 12417758 10.1073/pnas.222508899
57. Kehoe DM Gutu A Responding to color: The regulation of complementary chromatic adaptation. Ann Rev Plant Biol 2006 57 127-150 10.1146/ annurev.arplant.57.032905.105215
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 10.1006/ jmbi.1998.1678 9571058
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 10.1007/BF00402349
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 213394 1694529
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 17903216
63. Apt KE Collier JL Grossman AR Evolution of the phycobiliproteins. J Mol Biol 1995 248 79-96 10.1006/jmbi.1995.0203 7731046
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 503735 15256601 10.1073/ pnas.0401526101
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 1082820 15838046 10.1128/JB.187.9.3188-3200.2005
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 10.1111/j.1462-2920.2007.01285.x 17564603
67. Clokie MRJ Mann NH Marine cyanophages and light. Environ Microbiol 2006 8 2074-2082 10.1111/j.1462-2920.2006.01171.x 17107549
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 10.1371/journal.pbio.0030144
69. 2-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 146917 9254694 10.1093/nar/ 25.17.3389
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 101833 11917018 10.1093/nar/30.7.1575
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 308517 7984417 10.1093/nar/22.22.4673
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 10.1002/jez.b.21026
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 9021275
75. Guindon S Gascuel O A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003 52 696-704 10.1080/10635150390235520 14530136
76. Kumar S Tamura K Nei M MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 2004 5 150 163 10.1093/bib/5.2.150 15260895
77. Berlyn MK Linkage map of Escherichia coli K-12, edition 10: The traditional map. Microbiol Mol Biol Rev 1998 62 814-984 98936 9729611