Photosynthesis Research

, Volume 101, Issue 1, pp 1–19 | Cite as

Minimal genomes, maximal productivity: comparative genomics of the photosystem and light-harvesting complexes in the marine cyanobacterium, Prochlorococcus

  • Claire S. Ting
  • Meghan E. Ramsey
  • Yvette L. Wang
  • Alana M. Frost
  • Esther Jun
  • Timothy Durham
Regular Paper


Although Prochlorococcus isolates possess the smallest genomes of any extant photosynthetic organism, this genus numerically dominates vast regions of the world’s subtropical and tropical open oceans and has evolved to become an important contributor to global biogeochemical cycles. The sequencing of 12 Prochlorococcus genomes provides a glimpse of the extensive genetic heterogeneity and, thus, physiological potential of the lineage. In this study, we present an up-to-date comparative analysis of major proteins of the photosynthetic apparatus in 12 Prochlorococcus genomes. Our analyses reveal a striking diversity within the Prochlorococcus lineage in the major protein complexes of the photosynthetic apparatus. The heterogeneity that has evolved in the photosynthetic apparatus suggests versatility in strategies for optimizing photosynthesis under conditions of environmental variability and stress. This diversity could be particularly important in ensuring the survival of a lineage whose individuals have evolved minimal genomes and, thus, relatively limited repertoires for responding to environmental challenges.


Chlorophyll b-containing cyanobacteria Environmental stress Genomic diversity Global comparative genomics Oxychlorobacteria Pcb light-harvesting antenna 



This work was supported by the National Science Foundation (award no. MCB-0615680 to CST), the Woodrow Wilson National Fellowship Foundation (CST), and Williams College (CST, MER, YLW, AMF, EJ, TD). We would like to thank Christopher Warren, Office of Information Technology at Williams College for his invaluable assistance in the construction of our in-house genomic database system.

Supplementary material

11120_2009_9455_MOESM1_ESM.docx (19 kb)
Supplementary material 1 (DOCX 18 kb)


  1. Barber J, Morris E, Buchel C (2000) Revealing the structure of the photosystem II chlorophyll binding proteins, CP43 and CP47. Biochim Biophys Acta 1459:239–247PubMedCrossRefGoogle Scholar
  2. Berry J, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543CrossRefGoogle Scholar
  3. Bibby TS, Nield J, Barber J (2001) Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature 412:743–745PubMedCrossRefGoogle Scholar
  4. Bibby TS, Mary I, Nield J et al (2003) Low-light-adapted Prochlorococcus species possess specific antennae for each photosystem. Nature 424:1051–1054PubMedCrossRefGoogle Scholar
  5. Boekema EJ, Hifney A, Yakushevska AE et al (2001) A giant chlorophyll–protein complex induced by iron deficiency in cyanobacteria. Nature 412:745–748PubMedCrossRefGoogle Scholar
  6. Boichenko VA, Pinevich AV, Stadnichuk IN (2007) Association of chlorophyll a/b-binding Pcb proteins with photosystems I and II in Prochlorothrix hollandica. Biochim Biophys Acta 1767:801–806PubMedCrossRefGoogle Scholar
  7. Bouyoub A, Vernotte C, Astier C (1993) Functional analysis of the two homologous psbA gene copies in Synechocystis PCC6714 and 6803. Plant Mol Biol 21:249–258PubMedCrossRefGoogle Scholar
  8. Buchel C, Kuhlbrandt W (2005) Structural differences in the inner part of Photosystem II between higher plants and cyanobacteria. Photosyn Res 85:3–13PubMedCrossRefGoogle Scholar
  9. Bumba L, Prasil O, Vacha F (2005) Antenna ring around trimeric photosystem I in chlorophyll b containing cyanobacterium Prochlorothrix hollandica. Biochim Biophys Acta 1708:1–5PubMedCrossRefGoogle Scholar
  10. Campbell D, Zhou G, Gustafsson P et al (1995) Electron transport regulates exchange of the two forms of photosystem II D1 protein in the cyanobacterium Synechococcus. EMBO J 14:5457–5466PubMedGoogle Scholar
  11. Carver TJ, Rutherford KM, Berriman M et al (2005) ACT: the Artemis comparison tool. Bioinformatics 21:3422–3423PubMedCrossRefGoogle Scholar
  12. Chen M, Bibby TS (2005) Photosynthetic apparatus of antenna-reaction centers supercomplexes in oxyphotobacteria: insight through significance of Pcb/IsiA proteins. Photosyn Res 86:165–173PubMedCrossRefGoogle Scholar
  13. Chen M, Bibby TS, Nield J et al (2005) Structure of a large photosystem II supercomplex from Acaryochloris marina. FEBS Lett 579:1306–1310PubMedCrossRefGoogle Scholar
  14. Chen M, Zhang Y, Blankenship RE (2008) Nomenclature for membrane-bound light-harvesting complexes of cyanobacteria. Photosyn Res 95:147–154PubMedCrossRefGoogle Scholar
  15. Chitnis PR (2001) Photosystem I: function and physiology. Annu Rev Plant Physiol Plant Mol Biol 52:593–626PubMedCrossRefGoogle Scholar
  16. Clarke AK, Campbell D, Gustafsson P et al (1995) Dynamic responses of the photosystem II reaction centre and phycobilisome to changing light intensity in the cyanobacterium Synechococcus sp. PCC 7942. Planta 197:553–562CrossRefGoogle Scholar
  17. Coleman M, Sullivan MB, Martiny AC et al (2006) Genomic islands and the ecology and evolution of Prochlorococcus. Science 311:1768–1770PubMedCrossRefGoogle Scholar
  18. Dalbey RE, Robinson C (1999) Protein translocation into and across the bacterial plasma membrane and the plant thylakoid membrane. Trends Biochem Sci 24:17–22PubMedCrossRefGoogle Scholar
  19. De Las Rivas J, Balsera M, Barber J (2004) Evolution of oxygenic photosynthesis: genome-wide analysis of the OEC extrinsic proteins. Trends Plant Sci 9:18–25PubMedCrossRefGoogle Scholar
  20. Dufresne A, Salanoubat M, Partensky F et al (2003) Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc Natl Acad Sci USA 100:10020–10025PubMedCrossRefGoogle Scholar
  21. Enami I, Suzuki T, Tada O et al (2005) Distribution of the extrinsic proteins as a potential marker for the evolution of photosynthetic oxygen-evolving photosystem II. FEBS J 272:5020–5030PubMedCrossRefGoogle Scholar
  22. Ferreira KN, Iverson TM, Maghlaoui K et al (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838PubMedCrossRefGoogle Scholar
  23. Garczarek L, Hess WR, Holtzendorff J et al (2000) Multiplication of antenna genes as a major adaptation to low light in a marine prokaryote. Proc Natl Acad Sci USA 97:4098–4101PubMedCrossRefGoogle Scholar
  24. Gingrich JC, Buzby JS, Stirewalt VL et al (1988) Genetic analysis of two new mutations resulting in herbicide resistance in the cyanobacterium Synechococcus sp. PCC 7002. Photosyn Res 16:83–99CrossRefGoogle Scholar
  25. Gingrich JC, Gasparich GE, Sauer K et al (1990) Nucleotide sequence and expression of the two genes encoding the D2 protein and the single gene encoding the CP43 protein of Photosystem II in the cyanobacterium Synechococcus sp. PCC7002. Photosyn Res 24:137–150Google Scholar
  26. Golden SS, Stearns GW (1988) Nucleotide sequence and transcript analysis of three photosystem II genes from the cyanobacterium Synechococcus sp. PCC7942. Gene 67:85–96PubMedCrossRefGoogle Scholar
  27. Golden SS, Brusslan J, Haselkorn R (1986) Expression of a family of psbA genes encoding a photosystem II polypeptide in the cyanobacterium Anacystis nidulans R2. EMBO J 5:2789–2798PubMedGoogle Scholar
  28. Golden SS, Cho DS, Nalty MS (1989) Two functional psbD genes in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 171:4707–4713PubMedGoogle Scholar
  29. Grotjohann I, Fromme P (2005) Structure of cyanobacterial Photosystem I. Photosyn Res 85:51–72PubMedCrossRefGoogle Scholar
  30. Hess WR, Rocap G, Ting CS et al (2001) The photosynthetic apparatus of Prochlorococcus: insights through comparative genomics. Photosyn Res 70:53–71PubMedCrossRefGoogle Scholar
  31. Ina Y (1995) New methods for estimating the numbers of synonymous and nonsynonymous substitutions. J Mol Evol 40:190–226PubMedCrossRefGoogle Scholar
  32. Johnson ZI, Zinser ER, Coe A et al (2006) Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311:1737–1740PubMedCrossRefGoogle Scholar
  33. Jordan P, Fromme P, Witt HT et al (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411:909–917PubMedCrossRefGoogle Scholar
  34. Juncker AS, Willenbrock H, von Heijne G et al (2003) Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci 12:1652–1662PubMedCrossRefGoogle Scholar
  35. Kamiya N, Shen J-R (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. Proc Natl Acad Sci USA 100:98–103PubMedCrossRefGoogle Scholar
  36. Keren N, Aurora R, Pakrasi HB (2004) Critical roles of bacterioferritins in iron storage and proliferation of cyanobacteria. Plant Physiol 135:1666–1673PubMedCrossRefGoogle Scholar
  37. Kettler GC, Martiny AC, Huang K et al (2007) Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PloS Genet 3:2515–2528CrossRefGoogle Scholar
  38. Kimura A, Eaton-Rye JJ, Morita EH et al (2002) Protection of the oxygen-evolving machinery by the extrinsic proteins of Photosystem II is essential for development of cellular thermotolerance in Synechocystis sp. PCC 6803. Plant Cell Physiol 43:932–938PubMedCrossRefGoogle Scholar
  39. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  40. La Roche J, van der Staay GW, Partensky F et al (1996) Independent evolution of the prochlorophyte and green plant chlorophyll a/b light-harvesting proteins. Proc Natl Acad Sci USA 93:15244–15248PubMedCrossRefGoogle Scholar
  41. Laudenbach DE, Reith ME, Straus NA (1988) Isolation, sequence analysis, and transcriptional studies of the flavodoxin gene from Anacystis nidulans R2. J Bacteriol 170:258–265PubMedGoogle Scholar
  42. Leonhardt K, Straus NA (1994) Photosystem II genes isiA, psbDI and psbC in Anabaena sp. PCC 7120: cloning, sequencing and the transcriptional regulation in iron-stressed and iron-repleted cells. Plant Mol Biol 24:63–73PubMedCrossRefGoogle Scholar
  43. Mayfield SP, Yohn CB, Cohen A et al (1995) Regulation of chloroplast gene expression. Annu Rev Plant Physiol Plant Mol Biol 46:147–166CrossRefGoogle Scholar
  44. Moore LR, Chisholm SW (1999) Photophysiology of the marine cyanobacterium Prochlorococcus: ecotypic differences among cultured isolates. Limnol Oceanogr 44:628–638CrossRefGoogle Scholar
  45. Moore LR, Rocap G, Chisholm SW (1998) Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393:464–467PubMedCrossRefGoogle Scholar
  46. Mulkidjanian AY, Koonin EV, Makarova KS et al (2006) The cyanobacterial genome core and the origin of photosynthesis. Proc Natl Acad Sci USA 103:13126–13131PubMedCrossRefGoogle Scholar
  47. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426PubMedGoogle Scholar
  48. Nelson N, Yocum CF (2006) Structure and function of Photosystems I and II. Annu Rev Plant Biol 57:521–565PubMedCrossRefGoogle Scholar
  49. Nishiyama Y, Hayashi H, Watanabe Y et al (1994) Photosynthetic oxygen evolution is stabilized by cytochrome c 550 against heat activation in Synechococcus sp. PCC 7002. Plant Physiol 105:1313–1319PubMedCrossRefGoogle Scholar
  50. Nishiyama Y, Los DA, Hayashi H et al (1997) Thermal protection of the oxygen-evolving machinery by PsbU, an extrinsic protein of Photosystem II, in Synechococcus species PCC 7002. Plant Physiol 115:1473–1480PubMedCrossRefGoogle Scholar
  51. Nishiyama Y, Los DA, Murata N (1999) PsbU, a protein associated with Photosystem II, is required for the acquisition of cellular thermotolerance in Synechococcus species PCC 7002. Plant Physiol 120:301–308PubMedCrossRefGoogle Scholar
  52. Oquist G, Campbell D, Clarke A et al (1995) The cyanobacterium Synechococcus modulates Photosystem II function in response to excitation stress through D1 exchange. Photosyn Res 46:151–158CrossRefGoogle Scholar
  53. Palenik B, Brahamsha B, Larimer FW et al (2003) The genome of a motile marine Synechococcus. Nature 424:1037–1042PubMedCrossRefGoogle Scholar
  54. Porankiewicz J, Schelin J, Clarke AK (1998) The ATP-dependent Clp protease is essential for acclimation to UV-B and low temperature in the cyanobacterium Synechococcus. Mol Microbiol 29:275–283PubMedCrossRefGoogle Scholar
  55. Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16:276–277PubMedCrossRefGoogle Scholar
  56. Rocap G, Distel DL, Waterbury JB et al (2002) Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S–23S ribosomal DNA internal transcribed spacer sequences. Appl Environ Microbiol 68:1180–1191PubMedCrossRefGoogle Scholar
  57. Rocap G, Larimer FW, Lamerdin J et al (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424:1042–1047PubMedCrossRefGoogle Scholar
  58. Rutherford K, Parkhill J, Crook J et al (2000) Artemis: sequence visualization and annotation. Bioinformatics 16:944–945PubMedCrossRefGoogle Scholar
  59. Sane PV, Ivanov AG, Sveshnikov D et al (2002) A transient exchange of the Photosystem II reaction center protein D1:1 with D1:2 during low temperature stress of Synechococcus sp. PCC7942 in the light lowers the redox potential of QB*. J Biol Chem 277:32739–32745PubMedCrossRefGoogle Scholar
  60. Schluchter WM, Shen G, Zhao J et al (1996) Characterization of psaI and psaL mutants of Synechococcus sp. strain PCC 7002: a new model for state transitions in cyanobacteria. Photochem Photobiol 64:53–66PubMedCrossRefGoogle Scholar
  61. Shi T, Bibby TS, Jiang L et al (2005) Protein interactions limit the rate of evolution of photosynthesis genes in cyanobacteria. Mol Biol Evol 22:2179–2189PubMedCrossRefGoogle Scholar
  62. Straus NA (1994) Iron deprivation: Physiology and gene regulation. In: Bryant DA (ed) The molecular biology of cyanobacteria, vol 1. Kluwer, Dordrecht, The Netherlands, pp 731–750CrossRefGoogle Scholar
  63. 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. Nucl Acid Res 22:4673–4680CrossRefGoogle Scholar
  64. Thornton LE, Ohkawa H, Roose JL et al (2004) Homologs of plant PsbP and PsbQ proteins are necessary for regulation of Photosystem II activity in the cyanobacterium Synechocystis 6803. Plant Cell 16:2164–2175PubMedCrossRefGoogle Scholar
  65. Ting CS, Rocap G, King J et al (2002) Cyanobacterial photosynthesis in the oceans: the origins and significance of divergent light-harvesting strategies. Trends Microbiol 10:134–142PubMedCrossRefGoogle Scholar
  66. Ting CS, Westly E, Russell-Roy E (2005) Genome diversification in marine cyanobacteria: implications for photosynthetic physiology and environmental stress response mechanisms. In: van der Est A, Bruce D (eds) Photosynthesis: fundamental aspects to global perspectives. Alliance Communications Group, Lawrence, Kansas, USA, pp 614–616Google Scholar
  67. Ting CS, Hsieh C, Sundararaman S et al (2007) Cryo-electron tomography reveals the comparative three-dimensional architecture of Prochlorococcus, a globally important marine cyanobacterium. J Bacteriol 189:4485–4493PubMedCrossRefGoogle Scholar
  68. van der Staay GWM, Moon-van der Staay SY, Garczarek L et al (2000) Rapid evolutionary divergence of Photosystem I core subunits PsaA and PsaB in the marine prokaryote Prochlorococcus. Photosyn Res 65:131–139PubMedCrossRefGoogle Scholar
  69. Venter JC, Remington K, Heidelberg JF et al (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74PubMedCrossRefGoogle Scholar
  70. von Heijne G (1989) The structure of signal peptides from bacterial lipoproteins. Protein Eng 2:531–534CrossRefGoogle Scholar
  71. Vrba JM, Curtis SE (1989) Characterization of a four-member psbA gene family from the cyanobacterium Anabaena PCC7120. Plant Mol Biol 14:81–92CrossRefGoogle Scholar
  72. Williams JGK, Chisholm DA (1987) Nucleotide sequences of both psbD genes from the cyanobacterium Synechocystis 6803. In: Biggins J (ed) Progress in photosynthesis research, vol IV. Martinus Nijhoff, Dordrecht, The Netherlands, pp 809–812Google Scholar
  73. Xu Q, Hoppe D, Chitnis VP et al (1995) Mutational analysis of Photosystem I polypeptides in the cyanobacterium Synechocystis sp. PCC 6803. Targeted inactivation of psaI reveals the function of psaI in the structural organization of psaL. J Biol Chem 270:16243–16250PubMedCrossRefGoogle Scholar
  74. Zouni A, Witt H-T, Kern J et al (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409:739–743PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Claire S. Ting
    • 1
  • Meghan E. Ramsey
    • 1
  • Yvette L. Wang
    • 1
  • Alana M. Frost
    • 1
  • Esther Jun
    • 1
  • Timothy Durham
    • 1
  1. 1.Thompson Biology Lab, Department of BiologyWilliams CollegeWilliamstownUSA

Personalised recommendations