Function and evolution of the psbA gene family in marine Synechococcus: Synechococcus sp. WH7803 as a case study

ISME Journal

Volumn 2, Issue 9, 2008, Pages 937-953

  Garczarek, Laurence ^a   Dufresne, Alexis ^a   Blot, Nicolas ^a   Cockshutt, Amanda M ^b   Peyrat, Anne ^a   Campbell, Douglas A ^b   Joubin, Ludovic ^a   Six, Christophe ^b  

^a STATION BIOLOGIQUE DE ROSCOFF   (France)

^b MOUNT ALLISON UNIVERSITY   (Canada)

Author keywords

D1; Photoacclimation; Photoinhibition; Photosystem II; PsbA; Ultraviolet radiation

Indexed keywords

FRESH WATER; ISOPROTEIN; PHOTOSYSTEM II, PSBA SUBUNIT; SEA WATER;

ADAPTATION; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BIOSYNTHESIS; GENE DOSAGE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE ORDER; GENETIC RECOMBINATION; GENETICS; LIGHT; MICROBIOLOGY; MOLECULAR EVOLUTION; PHOTOSYSTEM II; PHYLOGENY; PHYSIOLOGY; RADIATION EXPOSURE; SEQUENCE HOMOLOGY; SYNECHOCOCCUS; ULTRAVIOLET RADIATION;

ADAPTATION, PHYSIOLOGICAL; EVOLUTION, MOLECULAR; FRESH WATER; GENE DOSAGE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE ORDER; GENES, BACTERIAL; GENOME, BACTERIAL; LIGHT; PHOTOSYSTEM II PROTEIN COMPLEX; PHYLOGENY; PROTEIN ISOFORMS; RECOMBINATION, GENETIC; SEAWATER; SEQUENCE HOMOLOGY, AMINO ACID; SYNECHOCOCCUS; ULTRAVIOLET RAYS;

CYANOBACTERIA; SYNECHOCOCCUS; SYNECHOCOCCUS SP.;

EID: 51449089207     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2008.46     Document Type: Article

References (71)

1. Ahlgren NA, Rocap G. (2006). Culture isolation and culture-independent clone libraries reveal new marine Synechococcus ecotypes with distinctive light and N physiologies. Appl Envirol Microbiol 72: 7193-7204.
2. Allakhverdiev SI, Murata N. (2004). Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of Photosystem II in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1657: 23-32.
3. Altschul S, Madden T, Schaffer A, Zhang J, Zhang Z, Miller W et al. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
4. Aro EM, Suorsa M, Rokka A, Allahverdiyeva Y, Paakkarinen V, Saleem A et al. (2005). Dynamics of photo-system II: a proteomic approach to thylakoid protein complexes. J Exp Bot 56: 347-356.
5. Aro EM, Virgin I, Andersson B. (1993). Photoinhibition of photosystem 2 - inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113-134.
6. Bouchard JE, Roy S, Ferreyra GA, Campbell DA, Curtosi A. (2005). Ultraviolet-B effects on photosystem II efficiency of natural phytoplankton communities from Antarctica. Polar Biol 28: 607-618.
7. Bruen TC, Philippe H, Bryant D. (2006). A simple and robust statistical test for detecting the presence of recombination. Genetics 172: 2665-2681.
8. Bustos SA, Schaefer MR, Golden SS. (1990). Different and rapid responses of four cyanobacterial psbA transcripts to changes in light intensity. J Bacteriol 172: 1998-2004.
9. Campbell D, Bruce D, Carpenter C, Gustafsson P, Oquist G. (1996). Two forms of the photosystem II D1 protein alter energy dissipation and state transitions in the cyanobacterium Synechococcus sp. PCC 7942. Photosynth Res 47: 131-144.
10. Campbell D, Clarke AK, Gustafsson P, Öquist G. (1999). Oxygen-dependent electron flow influences Photo-system II function and psbA gene expression in the cyanobacterium Synechococcus sp. PCC 7942. Physiol Plant 105: 746-755.
11. Campbell D, Eriksson MJ, Oquist G, Gustafsson P, Clarke AK. (1998). The cyanobacterium Synechococcus resists UV-B by exchanging photosystem II reaction-center D1 proteins. Proc Natl Acad Sci USA 95: 364-369.
12. Campbell D, Zhou GQ, Gustafsson P, Oquist G, Clarke AK. (1995). Electron transport regulates exchange of two forms of photosystem II D1 protein in the cyanobacterium Synechococcus. EMBO J 14: 5457-5466.
13. Clarke AK, Campbell D, Gustafsson P, Öquist G. (1995). Dynamic responses of the photosystem II and phycobilisomes to changing light in the cyanobacterium Synechococcus sp. PCC 7942. Planta 197: 553-562.
14. Clarke AK, Hurry VM, Gustafsson P, Oquist G. (1993a). Two functionally distinct forms of the photosystem II reaction-center protein D1 in the cyanobacterium Synechococcus sp. PCC 7942. Proc Natl Acad Sci USA 90: 11985-11989.
15. Clarke AK, Soitamo A, Gustafsson P, Oquist G. (1993b). Rapid interchange between two distinct forms of cyanobacterial photosystem II reaction-center protein D1 in response to photoinhibition. Proc Natl Acad Sci USA 90: 9973-9977.
16. Enright AJ, van Dongen S, Ouzonis CA. (2002). An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 30: 1575-1584.
17. Fuller NJ, Marie D, Partensky F, Vaulot D, Post AF, Scanlan DJ. (2003). 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 Envirol Microbiol 69: 2430-2443.
18. Garcia-Fernandez JM, Hess WR, Houmard J, Partensky F. (1998). Expression of the psbA gene in the marine oxyphotobacteria Prochlorococcus spp. Arch Biochem Biophys 359: 17-23.
19. Garczarek L, Hess WR, Holtzendorff J, van der Staay GW, Partensky F. (2000). Multiplication of antenna genes as a major adaptation to low light in a marine prokaryote. Proc Natl Acad Sci USA 97: 4098-4101.
20. Giorgi LB, Nixon PJ, Merry SA, Joseph DM, Durrant JR, de Las Rivas J et al. (1996a). Comparison of primary charge separation in the photosystem II reaction center complex isolated from wild-type and D1-130 mutants of the cyanobacterium Synechocystis PCC 6803. J Biol Chem 271: 2093-2101.
21. Giorgi LB, Nixon PJ, Merry SA, Joseph DM, Durrant JR, De Las Rivas J et al. (1996b). Comparison of primary charge separation in the photosystem II reaction center complex isolated from wild-type and D1-130 mutants of the cyanobacterium Synechocystis PCC 6803. J Biol Chem 271: 2093-2101.
22. Guindon S, Gascuel O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
23. Hall TA. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98.
24. Hess WR, Weihe A, Loiseaux-de Goër S, Partensky F, Vaulot D. (1995). Characterization of the single psbA gene of Prochlorococcus marinus CCMP 1375 (Prochlorophyta). Plant Mol Biol 27: 1189-1196.
25. Hurles M. (2004). Gene duplication: the genomic trade in spare parts. PLoS Biol 2: E206.
26. Huson DH, Bryant D. (2006). Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254-267.
27. -1 on marine Synechococcus WH7803-II. Photosynthetic responses mechanisms.. Deep-Sea Res 34: 497-516.
28. Keren N, Berg A, van Kan PJ, Levanon H, Ohad II. (1997). Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: the role of back electron flow. Proc Natl Acad Sci USA 94: 1579-1584.
29. Kos PB, Deak Z, Cheregi O, Vass I. (2008). Differential regulation of psbA and psbD gene expression, and the role of the different D1 protein copies in the cyanobacterium Thermosynechococcus elongatus BP-1. Biochim Biophys Acta 1777: 74-83.
30. Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SDW. (2006). Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol 23: 1891-1901.
31. Krupa Z, Oquist G, Gustafsson P. (1991). Photoinhibition of photosynthesis and growth responses at different light levels in psbA gene mutants of the cyanobacterium Synechococcus. Physiol Plant 82: 1-8.
32. Kumar S, Tamura K, Nei M. (2004). MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5: 150-163.
33. LaRoche J, van der Staay GW, Partensky F, Ducret A, Aebersold R, Li R et al. (1996). Independent evolution of the prochlorophyte and green plant chlorophyll a/b light-harvesting proteins. Proc Natl Acad Sci USA 93: 15244-15248.
34. Lindell D, Penno S, Al-Qutob M, David E, Rivlin T et al. (2005). Expression of the nitrogen stress response gene ntcA reveals nitrogen-sufficient Synechococcus populations in the oligotrophic northern Red Sea. Limnol Oceanogr 50: 1932-1944.
35. MacDonald TM, Dubois L, Smith LC, Campbell DA. (2003). Sensitivity of cyanobacterial antenna, reaction center and CO2 assimilation transcripts and proteins to moderate UVB: light acclimation potentiates resistance to UVB. Photochem Photobiol 77: 405-412.
36. Marie D, Brussaard C, Partensky F, Vaulot D. (1999). Flow cytometric analysis of phytoplankton, bacteria and viruses. In: Sons JW (ed). Current Protocols in Cytometry. International Society for Analytical Cytology. pp 11.11.11-11.11.15.
37. Marie D, Simon N, Guillou L, Partensky F, Vaulot D. (2000). DNA, RNA analysis of phytoplankton by flow cytometry. In: Current Protocols in Cytometry. John Wiley & Sons, pp 11.12.11-11.12.14.
38. Mary I, Vaulot D. (2003). Two-component systems in Prochlorococcus MED4: Genomic analysis and differential expression under stress. FEMS Microbiol Lett 226: 135-144.
39. Mate Z, Sass L, Szekeres M, Vass I, Nagy F. (1998). UV-B-induced differential transcription of psbA genes encoding the D1 protein of photosystem II in the cyanobacterium Synechocystis 6803. J Biol Chem 273: 17439-17444.
40. Moore LR, Goericke R, Chisholm SW. (1995). Comparative physiology of Synechococcus and Prochlorococcus: influence of light and temperature on growth, pigments, fluorescence and absorptive properties. Mar Ecol Prog Ser 116: 259-275.
41. Nishiyama Y, Allakhverdiev SI, Murata N. (2006). A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757: 742-749.
42. Nishiyama Y, Yamamoto H, Allakhverdiev SI, Inaba M, Yokota A, Murata N. (2001). Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J 20: 5587-5594.
43. Olson RJ, Zettler ER, Armbrust EV, Chisholm SW. (1990). Pigment, size and distribution of Synechococcus in the North Atlantic and Pacific oceans. Limnol Oceanogr 35: 45-58.
44. Palenik B. (2001). Chromatic adaptation in marine Synechococcus strains. Appl Envirol Microbiol 67: 991-994.
45. Partensky F, Blanchot J, Vaulot D. (1999). Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: a review. In: Charpy L, Larkum AWD (eds). Marine Cyanobacteria. Musée Océanographique: Monaco. pp 457-475.
46. Partensky F, Garczarek L. (2003). The photosynthetic apparatus of chlorophyll b- and d-containing Oxychlorobacteria. In: Larkum AWD (ed). Photosynthesis in Algae. Kluwer Academic Publishers: Dordrecht. pp 29-62.
47. Rippka R, Coursin T, Hess W, Lichtlé C, Scanlan DJ, Palinska KA et al. (2000). Prochlorococcus marinus Chisholm et al. 1992 subsp. pastoris subsp. nov. strain PCC 9511, the first axenic chlorophyll a2/b2-containing cyanobacterium (Oxyphotobacteria). Int J Syst Evol Microbiol 50: 1833-1847.
48. Rocap G, Distel DL, Waterbury JB, Chisholm SW. (2002). Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences. Appl Envirol Microbiol 68: 1180-1191.
49. Sander J, Nowaczyk M, Rogner M. (2007). Role of the psbA gene family of PSII from the thermophilic cyanobacterium. Thermosynechococcus elongatus. 14th Photosynthesis Congress, Glasgow, p PS4.14.
50. Sane PV, Ivanov AG, Sveshnikov D, Huner NPA, Oquist G. (2002). A transient exchange of the photosystem II reaction center protein D1:1 with D1:2 during low temperature stress of Synechococcus sp. PCC 7942 in the light lowers the redox potential of Q(B). J Biol Chem 277: 32739-32745.
51. Santoyo G, Romero D. (2005). Gene conversion and concerted evolution in bacterial genomes. FEMS Microbiol Rev 29: 169-183.
52. Schaefer MR, Golden SS. (1989). Differential expression of members of a cyanobacterial psbA gene family in response to light. J Bacteriol 171: 3973-3981.
53. Shi T, Bibby TS, Jiang L, Irwin AJ, Falkowski PG. (2005). Protein interactions limit the rate of evolution of photosynthetic genes in cyanobacteria. Mol Biol Evol 22: 2179-2189.
54. Sicora CI, Appleton SE, Brown CM, Chung J, Chandler J, Cockshutt AM et al. (2006). Cyanobacterial psbA families in Anabaena and Synechocystis encode trace, constitutive and UVB-induced D1 isoforms. Biochim Biophys Acta 1757: 47-56.
55. Sicora CI, Brown CM, Vass I, Cheregi O, Campbell DA. (2008). The psbA gene family responds differentially to light and UVB stress in Gloeobacter violaceus PCC 7421, a deeply divergent cyanobacterium. BBA 777: 130-139.
56. Sippola K, Kanervo E, Murata N, Aro EM. (1998). A genetically engineered increase in fatty acid unsatura-tion in Synechococcus sp. PCC 7942 allows exchange of D1 protein forms and sustenance of photosystem II activity at low temperature. Eur J Biochem 251: 641-648.
57. Six C, Finkel ZV, Irwin AJ, Campbell DA. (2007a). Light variability illuminates Niche-Partitioning among Marine Picocyanobacteria. PLoS ONE 2: e1341.
58. Six C, Joubin L, Partensky F, Holtzendorff J, Garczarek L. (2007b). UV-induced phycobilisome dismantling in the marine picocyanobacterium Synechococcus sp. WH 8102. Photosynth Res 92: 75-86.
59. Six C, Thomas JC, Garczarek L, Ostrowski M, Dufresne A, Blot N et al. (2007c). Diversity and evolution of phycobilisomes in marine Synechococcus spp.: a comparative genomics study. Genome Biol 8: R259.
60. Six C, Thomas JC, Brahamsha B, Lemoine Y, Partensky F. (2004). Photophysiology of the marine cyanobacterium Synechococcus sp. WH8102, a new model organism. Aquat Microb Ecol 35: 17-29.
61. 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.
62. Thompson JD, Higgins DG, Gibson TJ. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
63. Tichy M, Lupinkova L, Sicora C, Vass I, Kuvikova S, Prasil O et al. (2003). Synechocystis 6803 mutants expressing distinct forms of the Photosystem II D1 protein from Synechococcus 7942: relationship between the psbA coding region and sensitivity to visible and UV-B radiation. Biochim Biophys Acta 1605: 55-66.
64. Vass I, Styring S, Hundal T, Koivuniemi A, Aro E, Andersson B. (1992). Reversible and irreversible intermediates during photoinhibition of photosystem II: stable reduced QA species promote chlorophyll triplet formation. Proc Natl Acad Sci USA 89: 1408-1412.
65. Vass I, Kirilovsky D, Perewoska I, Mate Z, Nagy F, Etienne AL. (2000). UV-B radiation induced exchange of the D1 reaction centre subunits produced from the psbA2 and psbA3 genes in the cyanobacterium Synechocystis sp PCC 6803. Eur J Biochem 267: 2640-2648.
66. Vrba JM, Curtis SE. (1990). Characterization of a four-member psbA gene family from the cyanobacterium Anabaena PCC 7120. Plant Mol Biol 14: 81-92.
67. Waterbury JB, Watson SW, Valois FW, Franks DG. (1986). Biological and ecological characterization of the marine unicellular cyanobacterium Synechococcus. Can Bull Fish Aquat Sci 214: 71-120.
68. Wilson MI, Ghosh S, Gerhardt KE, Holland N, Babu TS, Edelman M et al. (1995). In vivo photomodification of ribulose-1,5-bisphosphate carboxylase/oxygenase
69. holoenzyme by Ultraviolet-B radiation (formation of a 66-Kilodalton Variant of the Large Subunit). Plant Physiol 109: 221-229.
70. Yosef I, Irihimovitch V, Knopf JA, Cohen I, Orr-Dahan I, Nahum E et al. (2004). RNA binding activity of the ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit from Chlamydomonas reinhardtii. J Biol Chem 279: 10148-10156.
71. Zeidner G, Bielawski JP, Shmoish M, Scanlan DJ, Sabehi G, Beja O. (2005). Potential photosynthesis gene recombination between Prochlorococcus and Synechococcus via viral intermediates. Environ Microbiol 7: 1505-1513.