The Photosynthetic Apparatus of Chlorophyll b- and d-Containing Oxyphotobacteria

Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 14)

Summary

Although the vast majority of oxyphotobacteria harvest light with complex supramolecular structures, the phycobilisomes, three atypical prokaryotic genera share the property of using a mere intrinsic chlorophyll (Chl) a/b-protein complex: Prochloron, Prochlorothrix and Prochlorococcus. Some strains of the latter genus do contain some phycoerythrin, but at too low concentration for having a significant role in light harvesting. In the context of the endosymbiotic theory of the origin of chloroplasts, it was proposed that these three prokaryotic genera might belong to a separate clade among Cyanobacteria, the ‘prochlorophytes’, which would have had a recent common ancestor with green algae and higher plants. Phylogenetic analyses using diverse genes however strongly suggest that these genera are polyphyletic within the cyanobacterial radiation and on a different branch than the one bearing green plastids. With this idea in mind, it was interesting to re-examine to what extent the photosynthetic apparatus of these Chl b-containing oxyphotobacteria are truly similar to one another and whether they share some relationships with those of green plastids. This chapter shows that the main trait linking these prokaryotes is the similar nature of their antenna proteins, called Pcbs for ‘prochlorophy te chlorophyll b-binding’ proteins. These are different from the light-harvesting complex (Lhc) proteins found in eukaryotes, but closely resemble iron-stress induced (IsiA) proteins, used for light-harvesting by Photosystem I in some cyanobacteria when iron-starved. More than the mere occurrence of Chl b, this similar antenna system likely conditions most of the other apparent similarities between these three atypical organisms, including those at the ultrastructural level. Besides reviewing the recent literature about these ‘green oxyphotobacteria,’ we discuss a newcomer among atypical oxygenic prokaryotes, Acaryochloris marina, which contains Chl d as the main light-harvesting pigment and a Pcb-like antenna system. The insights that the study of these prokaryotes have brought into the more general fields of algal photosynthesis and evolution are underlined.

Keywords

Thylakoid Membrane Photosynthetic Apparatus Antenna Protein Manganese Stabilise Protein Photosynthetic Prokaryote 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Akiyama M, Miyashita H, Kise H, Watanabe T, Miyadri S and Kobayashi M (2002) Detection of chlorophyll d’ and pheophytin a in a chlorophyll d-dominating oxygenic photosynthetic prokaryote Acaryochloris marina. Anal Sci 17: 205–208Google Scholar
  2. Alberte RS (1989) Physiological and cellular features of Prochloron. In: Lewin R and Cheng L (eds) Prochloron, a Microbial Enigma, pp 31-52. Chapman and Hall, New YorkGoogle Scholar
  3. Alberte RS, Cheng L and Lewin RA (1986) Photosynthetic characteristics of Prochloron sp.—ascidian symbioses. Mar Biol 90: 575–587Google Scholar
  4. Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098: 275–335PubMedGoogle Scholar
  5. Arudchandran A and Bullerjahn GS (1996) Expression of the petE gene encoding plastocyanin in the photosynthetic prokaryote, Prochlorothrix hollandica. Biochem Biophys Res Commun 226: 626–630PubMedGoogle Scholar
  6. Arudchandran A, Seeburg D, Burkhart W and Bullerjahn GS (1994) Nucleotide sequence of the petE gene encoding plastocyanin from the photosynthetic prokaryote, Prochlorothrix hollandica. Biochim Biophys Acta 1188: 447–449PubMedGoogle Scholar
  7. Babu CR, Arudchandran A, Hille R, Gross EL and Bullerjahn GS (1997) Reconstitution and characterization of a divergent plastocyanin from the photosynthetic prokaryote, Prochlorothrix hollandica, expressed in Escherichia coli. Biochem Biophys Res Commun 235: 631–635PubMedGoogle Scholar
  8. Babu CR, Volkman BF and Bullerjahn GS (1999) NMR solution structure of plastocyanin from the photosynthetic prokaryote, Prochlorothrix hollandica. Biochemistry 38: 4988–4995PubMedGoogle Scholar
  9. Barclay WR, Kennish JM, Goodrich VM and Fall R (1987) High levels of phenolic compounds in Prochloron species. Phytochem 26: 739–743Google Scholar
  10. Bazzaz MB (1981) New chlorophyll chromophores isolated from a chlorophyll-deficient mutant of maize. Photobiochem Photobiophys 2: 199–207Google Scholar
  11. Bazzaz MB and Brereton RG (1982) 4-vinyl-4-desetyl chlorophyll a: A new naturally occurring chlorophyll. FEBS Lett 138: 104–108Google Scholar
  12. Bhaya D, DuFresne A, Vaulot D and Grossman A (2002) Analysis of the hli gene family in marine and freshwater cyanobacteris. FEMS Microbiol Lett 215: 209–219PubMedGoogle Scholar
  13. Bibby TS, Nield J and Barber J (2001a) A Photosystem II-like protein, induced under iron-stress, forms an antenna ring around the Photosystem I trimer in cyanobacteria. Nature: 412: 743–745PubMedGoogle Scholar
  14. Bibby TS, Nield J, Partensky F and Barber J (2001b) Antenna ring around Photosystem I. Nature 413: 590Google Scholar
  15. Boekema ES, Hifney A, Yakushevska AE, Piotrowski M, Keegstra W, Berry S, Michel KP, Pistorius EK and Kruip J (2001) A giant chlorophyll-protein complex induced by iron deficiency in cyanobacteria. Nature 413: 745–748Google Scholar
  16. Bryant DA (ed) (1994) The Molecular Biology of Cyanobacteria. Kluwer Academic Publishers, DordrechtGoogle Scholar
  17. Bullerjahn GS and Post AF (1993) The prochlorophytes: Are they more than just chlorophyll a/b-containing cyanobacteria? CRC Crit Rev Microbiol 19: 43–59Google Scholar
  18. Bullerjahn GS, Matthijs HC, Mur LR and Sherman LA (1987) Chlorophyll-protein composition of the thylakoid membrane from Prochlorothrix hollandica, a prokaryote containing chlorophyll b. Eur J Biochem 168: 295–300PubMedGoogle Scholar
  19. Bullerjahn GS, Jensen TC, Sherman DM and Sherman LA (1990) Immunological characterization of the Prochlorothrix hollandica and Prochloron sp. chlorophyll a/b antenna proteins. FEMS Microbiol Lett 67: 99–106Google Scholar
  20. Burger-Wiersma T and Matthijs HCP (1990) The Biology of the Prochlorales. In: Codd GA, Dijkhuizen L and Tabita FR (eds) Advances in Autotrophic Microbiology and One-Carbon Metabolism, Vol 1, pp 1-24. Kluwer Academic Publishers, DordrechtGoogle Scholar
  21. Burger-Wiersma T and Post AF (1989) Functional analysis of the photosynthetic apparatus of Prochlorothrix hollandica (Prochlorales), a chlorophyll b containing procaryote. Plant Physiol 91: 770–774PubMedGoogle Scholar
  22. Burger-Wiersma T, Veenhuis M, Korthals HJ, van de Wiel CCM and Mur LR (1986) A new prokaryote containing chlorophylls a and b. Nature 320: 262–264Google Scholar
  23. Burger-Wiersma T, Stal LJ and Mur LR (1989) Prochlorothrix hollandica gen. nov., sp. nov., a filamentous oxygenic photoautotrophic prokaryote containing chlorophylls a and b: Assignment to Prochlorotrichaceae fam. nov. and Order Prochlorales Florenzano, Balloni and Materassi 1986, with emendation of the ordinal description. Int J Syst Bacteriol 39: 250–257Google Scholar
  24. Burnap RL, Troyan T and Sherman LA (1993) The highly abundant chlorophyll-protein complex of iron-deficient Synechococcus sp. PCC7942 (CP43) is encoded by the isiA gene. Plant Physiol 103: 893–902PubMedGoogle Scholar
  25. Castenholz RW (2001) Phylum BX. Cyanobacteria. Oxygenic photosynthetic bacteria. In: Boone DR and Castenholz RW (eds) Bergey’s Manual of Systematic Bacteriology, 2nd Ed, Vol 1, pp 473-599. Springer-Verlag, New YorkGoogle Scholar
  26. Chen M, Quinnell R and Larkum AW (2002) The major lightharvesting protein of Acaryochloris marina. FEBS Lett 514: 142–152Google Scholar
  27. Chisholm SW, Olson RJ, Zettler ER, Waterbury J, Goericke R and Welschmeyer N (1988) A novel free-living prochlorophyte occurs at high cell concentrations in the oceanic euphotic zone. Nature 334: 340–343Google Scholar
  28. Chisholm SW, Frankel SL, Goericke R, Olson RJ, Palenik B, Waterbury JB, West-Johnsrud L and Zettler ER (1992) Prochlorococcus marinus nov. gen. nov. sp.: An oxyphototrophic marine prokaryote containing divinyl chlorophyll a and b. Arch Microbiol 157: 297–300Google Scholar
  29. Chitnis PR (1996) Update on photosynthetic electron transport. Photosystem I. Plant Physiol 111: 661–669PubMedGoogle Scholar
  30. Chitnis PR, Xu Q, Chitnis VP and Nechushtai R (1995) function and organization of Photosystem I polypeptides. Photosynth Res 44: 23–40Google Scholar
  31. Christen G, Stevens G, Lukins PB, Renger G, Larkum AW (1999) Isolation and characterisation of oxygen evolving thylakoids from the marine prokaryote Prochloron didemni. FEBS Lett 449: 264–268PubMedGoogle Scholar
  32. Clarke AK, Hurry VM, Gustafsson P and Öquist G (1993) Two functionally distinct forms of the Photosystem II reaction center D1 protein in the cyanobacterium Synechococcus sp. PCC7942. Proc Natl Acad Sci USA 90: 11985–11989PubMedGoogle Scholar
  33. Colon-Lopez MS and Sherman LA (1998) Transcriptional and translational regulation of Photosystem I and II genes in lightdark-and continuous-light-grown cultures of the unicellular cyanobacterium Cyanothece sp. strain ATCC 51142. J Bact 180: 519–526PubMedGoogle Scholar
  34. Cox G (1986) Comparison of Prochloron from different hosts. I Structural and ultrastructural characteristics. New Phytol 88: 427–438Google Scholar
  35. Delwiche CF and Palmer JD (1996) Rampant horizontal transfer and duplication of Rubisco genes in eubacteria and plastids. Mol Biol Evol 13: 873–882PubMedGoogle Scholar
  36. Douglas S (1998) Plastid evolution: Origins, diversity, trends. Curr Op Gen Dev 8: 655–661Google Scholar
  37. Durnford DG, Deane JA, Tan S, McFadden GI, Gantt E and Green BR (1999) A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins, with implications forplastids evolution. J Mol Evol 48: 59–68PubMedGoogle Scholar
  38. Engle JM, Burkhart W, Sherman DM and Bullerjahn GS (1991) Purification and characterization of a surface-associated carotenoid-binding complex from the photosynthetic prokaryote, Prochlorothrix hollandica. Arch Microbiol 155: 453–458Google Scholar
  39. Ferris MJ and Palenik B (1998) Niche adaptation in ocean cyanobacteria. Nature 396: 226–228Google Scholar
  40. Flieger K, Oelmüller R and Herrmann RG (1993) Isolation and characterization of cDNA clones encoding a 18.8 kDa polypeptide, the product of the gene psaL, associated with Photosystem I reaction center from spinach. Plant Mol Biol 22: 703–709PubMedGoogle Scholar
  41. Florenzano G, Balloni W and Materassi R (1986) Nomenclature of Prochloron didemni (Lewin 1977) sp. nov., nom. rev., Prochloron (Lewin 1976) gen. nov., nom. rev., Prochloraceae fam. nov., Prochlorales ord. nov., nom. rev. in the class Photobacteria Gibbons and Murray 1978. Int J Syst Bacteriol 36: 351–353Google Scholar
  42. Foss P, Lewin RA and Liaaen-Jensen S (1987) The carotenoids of Prochloron sp. (Prochlorophyta). Phycologia 26: 142–144Google Scholar
  43. Fredrick JF (1980) The alpha-1,4-glucans of Prochloron, a prokaryotic green marine alga. Phytochem 19: 2611–2613Google Scholar
  44. Fujita Y, Murakami A and Aizawa K (1994) Short-term adaptation of the photosynthetic apparatus: Homeostatic properties of thylakoids. In: Bryant DA (ed) The Molecular Biology of Cyanobacteria, pp 677-692. Kluwer Academic Publishers, DordrechtGoogle Scholar
  45. Garcia-Fernandez JM, Hess WR, Houmard J and Partensky F (1998) Expression of the psbA gene in the marine oxyphotobacteria Prochlorococcus spp. Arch Biochem Biophys 359: 17–23PubMedGoogle Scholar
  46. Garczarek L (2000) Caractérisation biochimique et génétique des complexes pigment-protéines chez le procaryote marin Prochlorococcus: origine évolutive et rôle dans l’adaptation de l’appareil photosynthétique aux conditions lumineuses. Thøse de Doctorat. Institut National Paris-Grignon, ParisGoogle Scholar
  47. Garczarek L, van der Staay GWM, Thomas JC and Partensky F (1998) Isolation and characterization of Photosystem I from two strains of the marine oxychlorobacterium Prochlorococcus. Photosynth Res 56: 131–141Google Scholar
  48. Garczarek L, Hess WR, Holtzendorff J, van der Staay GWM and Partensky F (2000) Multiplication of antenna genes as a major adaptation to low light in a marine prokaryote. Proc Natl Acad Sci USA 97: 4098–4101PubMedGoogle Scholar
  49. Garczarek L, Partensky F, Irlbacher H, Holtzendorff J, Babin M, Mary I, Thomas JC and Hess WR (2001a) Differential expression of antenna and core genes in Prochlorococcus PCC9511 (Oxyphotobacteria) grown under light-dark cycles. Environ Microbiol 3: 168–175PubMedGoogle Scholar
  50. Garczarek L, van der Staay GWM, Hess WR, Legall F and Partensky F (2001 b) Expression and phylogeny of the multiple antenna genes of the low-light adapted strain Prochlorococcus SSI20 (Oxyphotobacteria). Plant Mol Biol 46: 683–693PubMedGoogle Scholar
  51. Geiss U, Vinnemeier J, Schoor A and Hagemann M (2001) The iron-regulated isiA gene of Fischerella muscicola strain PCC 73103 is linked to a likewise regulated gene encoding a Pcblike chlorophyll-binding protein. FEMS Microbiol Lett 197: 123–129PubMedGoogle Scholar
  52. Giddings TH, Withers NW and Staehelin LA (1980) Supramolecular structure of stacked and unstacked regions of the photosynthetic membranes of Prochloron sp., a prokaryote. Proc Natl Acad Sci USA 77: 352–356PubMedGoogle Scholar
  53. Goericke R and Repeta DJ (1992) The pigments of Prochlorococcus marinus: The presence of divinyl chlorophyll a and b in a marine prochlorophyte. Limnol Oceanogr 37: 425–433Google Scholar
  54. Goericke R and Repeta DJ (1993) Chlorophylls a and b and divinyl chlorophylls a and b in the open subtropical North Atlantic Ocean. Mar Ecol Prog Ser 101: 307–313Google Scholar
  55. Goericke R, Olson RJ and Shalapyonok A (2000) A novel niche for Prochlorococcus sp in low-light suboxic environments in the Arabian Sea and the Eastern Tropical North Pacific. Deep Sea Res Pt I Oceanog Res 47: 1183–1205Google Scholar
  56. Golbeck JH (1994) Photosystem I in cyanobacteria. In: Bryant DA (ed) The Molecular Biology of Cyanobacteria, pp 319-360. Kluwer Academic Publishers, DordrechtGoogle Scholar
  57. Golden SS, Brusslan J and Haselkorn R (1986) Expression of a family of psbA genes encoding a Photosystem II polypcptide in the cyanobacterium Anacystis nidulans R2. EMBO J 5: 2789–2798PubMedGoogle Scholar
  58. Golecki JR (1989) Ultrastructural studies on the membrane systems and cell inclusions of the filamentous prochlorophyte Prochlorothrix hollandica. Arch Microbiol 152: 77–82Google Scholar
  59. Goodwin TW and Britton G (1988) Distribution and analysis of carotenoids. In: Goodwin TW (ed) Plant pigment, pp 61-132. Academic Press, New YorkGoogle Scholar
  60. Green BR (1988) The chlorophyll-protein complexes of higher plant photosynthetic membranes, or just what green band is that? Photosynth Res 15: 3–32Google Scholar
  61. Green BR and Durnford DG (1996) The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Ann Rev Plant Physiol Plant Mol Biol 47: 685–714Google Scholar
  62. Green BR and Pichersky E (1994) Hypothesis for the evolution of three-helix Chl a/b and Chl a/c light-harvesting antenna proteins from two-helix and four-helix ancestors. Photosynth Res 39: 149–162Google Scholar
  63. Greer KL and Golden SS (1991) Nucleotide sequence of psbB from Prochlorothrix hollandica. PlantMol Biol 17: 915–917Google Scholar
  64. Greer KL and Golden SS (1992) Conserved relationship between psbH and petBD genes: Presence of a shared upstream element in Prochlorothrix hollandica. Plant Mol Biol 19: 355–365PubMedGoogle Scholar
  65. Grossman AR, Bhaya D, Apt KE and Kehoe DM (1995) Lightharvesting complexes in oxygenic photosynthesis: Diversity, control and evolution. Ann Rev Genet 29: 231–288PubMedGoogle Scholar
  66. Guillard RRL, Murphy LS, Foss P and Liaaen-Jensen S (1985) Synechococcus spp. as likely zeaxanthin-dominant ultraphytoplankton in the North-Atlantic. Limnol Oceanogr 30: 412–414Google Scholar
  67. Helfrich M, Ross A, King GC, Turner AG and Larkum AW (1999) Identification of [8-vinyl]-protochlorophyllide a in phototrophic prokaryotes and algae: Chemical and spectroscopic properties. Biochim Biophys Acta 1410: 262–272PubMedGoogle Scholar
  68. Hess WR, Weihe A, Loiseaux-de Goër S, Partensky F and Vaulot D (1995) Characterization of the single psbA gene of Prochlorococcus marinus CCMP1375 (Prochlorophyta). Plant Mol Biol 27: 1189–1196PubMedGoogle Scholar
  69. Hess WR, Partensky F, van der Staay GW, Garcia-Fernandez JM, Börner T and Vaulot D (1996) Coexistence of phycoerythrin and a chlorophyll a/b antenna in a marine prokaryote. Proc Natl Acad Sci USA 93: 11126–11130PubMedGoogle Scholar
  70. Hess WR, Steglich C, Lichtlé C and Partensky F (1999) Phycoerythrins of the oxyphotobacterium Prochlorococcus marinus are associated to the thylakoid membrane and are encoded by a single large gene cluster. Plant Mol Biol 40: 507–521PubMedGoogle Scholar
  71. Hess WR, Rocap G, Ting C and Chisholm SW (2001) The photosynthetic apparatus of Prochlorococcus: Insights through comparative genomics. Photosynth Res 70: 53–71PubMedGoogle Scholar
  72. Hiller RG and Larkum AWD (1985) The chlorophyll-protein complexes of Prochloron sp. (Prochlorophyta). Biochim Biophys Acta 806: 107–115Google Scholar
  73. Hoffmann L and Greuter W (1993) Validation of Prochloron didemni (Cyanophyta) and nomenclatural discussion of correlated names at the higher ranks. Taxon 42: 641–645Google Scholar
  74. Honda D, Yokota A and Sugiyama J (1999) Detection of seven major evolutionary lineages in cyanobacteria based on the 16S rRNA gene sequence analysis with new sequences of five marine Synechococcus strains. J Mol Evol 48: 723–739PubMedGoogle Scholar
  75. Hu Q, Ishikawa T, Inoue Y, Miyashita H, Kurano N, Miyachi S, Iwaki M, Itoh S, Marquardt J and Mörschel E (1998a) Heterogeneity of chlorophyll d-binding Photosystem I reaction centers from the photosynthetic prokaryote Acaryochloris marina. In: Garab G (ed) Photosynthesis: Mechanisms and Effectsv Vol 1, pp 437-440. Kluwer Academic Publishers, DordrechtGoogle Scholar
  76. Hu Q, Miyashita H, Iwasaki I, Kurano N, Miyachi S, Iwaki M and Itoh S (1998b) A Photosystem I reaction center driven by chlorophyll d in oxygenic photosynthesis. Proc Natl Acad of Sci USA 95: 13319–13323Google Scholar
  77. Jeffrey SW, Mantoura RFC and Wright SW (1997) Phytoplankton Pigments in Oceanography. UNESCO Publishing, ParisGoogle Scholar
  78. Johnson PW and Sieburth JM (1979) Chroococcoid cyanobacteria in the sea: A ubiquitous and diverse phototrophic biomass. Limnol Oceanogr 24: 928–935Google Scholar
  79. Kishino H, Miyata T and Hasegawa M (1990) Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. J Mol Evol 31: 151–160Google Scholar
  80. Kashino Y, Lauber WM, Caroll JA, Wang Q, Whitmarsh J, Satoh K, Pakrasi HB (2002) Proteomic analysis of a highly active Photosystem II preparation from the cyanobacterium Synechocystis sp. PCC 6803 reveals the presence of novel polypepties. Biochemistry 41: 8004–8012PubMedGoogle Scholar
  81. Larkum AWD and Howe CJ (1997) Molecular aspects of lightharvesting processes in algae. Adv Bot Res 27: 257–330Google Scholar
  82. Larkum AWD, Scaramuzzi C, Cox GC, Hiller RG and Turner AG (1994) Light-harvesting chlorophyll c-like pigment in Prochloron. Proc Natl Acad Sci USA 91: 679–683PubMedGoogle Scholar
  83. La Roche J, van der Staay GW, Partensky F, Ducret A, Aebersold R, Li R, Golden SS, Hiller RG, Wrench PM, Larkum AW and Green BR (1996) Independent evolution of the prochlorophyte and green plant chlorophyll a/b light-harvesting proteins. Proc Natl Acad Sci USA 93: 15244–15248Google Scholar
  84. Laudenbach DE and Straus NA (1988) Characterization of a cyanobacterial iron stress-induced gene similar to psbC. J Bacteriol 170: 5018–5026PubMedGoogle Scholar
  85. Leonhardt K and Straus NA (1992) An iron stress operon involved in photosynthetic electron transport in the marine cyanobacterium Synechococcus sp. PCC7002. J Gen Microbiol 138: 1613–1621PubMedGoogle Scholar
  86. Lewin RA (1977) Prochloron, type genus of the Prochlorophyta. Phycologia 16: 217Google Scholar
  87. Lewin RA and Cheng L (1989) Prochloron, a Microbial Enigma. Chapman and Hall, LondonGoogle Scholar
  88. Lewin RA and Withers NW (1975) Extraordinary pigment composition of a prokaryotic alga. Nature 256: 735–737Google Scholar
  89. Lichtlé C, Thomas JC, Spilar A and Partensky F (1995) Immunological and ultrastructural characterization of the photosynthetic complexes of the prochlorophyte Prochlorococcus (Oxychlorobacteria). J Phycol 31: 934–941Google Scholar
  90. Lockhart PJ, Beanland TJ, Howe CJ and Larkum AW (1992a) Sequence of Prochloron didemni atpBE and the inference of chloroplast origins. Proc Natl Acad Sci USA 89: 2742–2746PubMedGoogle Scholar
  91. Lockhart PJ, Penny D, Hendy MD, Howe CJ, Beanland TJ and Larkum AW (1992b) Controversy on chloroplast origins. FEBS Lett 301: 127–131PubMedGoogle Scholar
  92. Lockhart PJ, Penny D, Hendy MD and Larkum ADW (1993) Is Prochlorothrix hollandica the best choice as a prokaryotic model for higher plant Chl a/b photosynthesis? Photosynth Res 37: 61–68Google Scholar
  93. Lokstein H, Steglich C and Hess WR (1999) Light-harvesting antenna function of phycoerythrin in Prochlorococcus marinus. Biochim Biophys Acta 1410: 97–98PubMedGoogle Scholar
  94. Manning WM and Strain HH (1943) Chlorophyll d, a green pigment of red algae. J Biol Chem 151: 1–19Google Scholar
  95. Marquardt J and Morschel E(1999) The photosynthetic apparatus of Prochloron-like cyanobacteria. In: Argyroudi-Akoyunoglou JH and Senger H (eds) Chloroplast: From Molecular Biology to Biotechnology, Vol 1, pp 41-46. Kluwer Academic Publishers, DordrechtGoogle Scholar
  96. Marquardt J, Senger H, Miyashita H, Miyachi S and Morschel E (1997) Isolation and characterization of biliprotein aggregates from Acaryochloris marina, a Prochloron-like prokaryote containing mainly chlorophyll d. FEBS Lett 410: 428–432PubMedGoogle Scholar
  97. Marquardt J, Morschel E, Rhiel E and Westermann M (2000) Ultrastructure of Acaryochloris marina, an oxyphotobacterium containing mainly chlorophyll d. Arch Microbiol 174: 181–188PubMedGoogle Scholar
  98. Matthijs HCP, Neuteboom AM and Mur LR (1988) Energy metabolism and cytochrome in the prochlorophyte Prochlorothrix hollandica. In: Mur LR and Burger-Wiersma T (eds) Proceedings of the VI International Symposium on Phototrophic Prokaryotes, Amsterdam, pp 109. Laboratory for Microbiology, University of Amsterdam, AmsterdamGoogle Scholar
  99. Matthijs HCP, van der Staay GWM, van Amerongen H, van Grondelle R and Garab G (1989) Structural organization of chlorophyll b in the prochlorophyte Prochlorothrix hollandica. Biochim Biophys Acta 975: 185–187Google Scholar
  100. Matthijs HCP, van der Staay GWM and Mur LR (1994) Prochlorophytes: The ‘other’ cyanobacteria? In: Bryant DA (ed) The Molecular Biology of Cyanobacteria, pp 49-64. Kluwer Academic Publishers, DordrechtGoogle Scholar
  101. McKay R, Salgado D, Bonen I, Stackebrandt E and Doolittle W (1982) The 5S ribosomal RNAs of Paracoccus denitrifians and Prochloron. Nucl Acids Res 10: 2963Google Scholar
  102. Miller KR, Jacob JS, Burger-Wiersma T and Matthijs HC (1988) Supramolecular structure of the thylakoid membrane of Prochlorothrix hollandica: A chlorophyll b-containing prokaryote. J Cell Sci 91: 577–586PubMedGoogle Scholar
  103. Mimuro M, Akimoto S, Yamazaki I, Miyashita H and Miyachi S (1999) Fluorescence properties of chlorophyll d-dominating prokaryotic alga, Acaryochloris marina: Studies using timeresolved fluorescence spectroscopy on intact cells. Biochim Biophys Acta 1412: 37–46PubMedGoogle Scholar
  104. Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M and Miyachi S (1996) Chlorophyll d as a major pigment. Nature 383: 402Google Scholar
  105. Miyashita H, Adachi K, Kurano N, Ikemoto H, Chihara M and Miyachi S (1997) Pigment composition of a novel oxygenic photosynthetic prokaryote containing chlorophyll d as the major chlorophyll. Plant Cell Physiol 38: 274–281Google Scholar
  106. Moore LR (1997) Physiological ecology of Prochlorococcus: A comparison of isolates from diverse oceanographie regimes. PhD Thesis. Massachusetts Institute of Technology, CambridgeGoogle Scholar
  107. Moore LR and Chisholm SW (1999) Photophysiology of the marine cyanobacterium Prochlorococcus: Ecotypic differences among cultured isolates. Limnol Oceanogr 44: 628–638Google Scholar
  108. Moore LR, Goericke R and 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: 259–275Google Scholar
  109. Moore LR, Rocap G and Chisholm SW (1998) Physiology and molecular phylogeny of coexisting prochlorococcus ecotypes. Nature 393: 464–467PubMedGoogle Scholar
  110. Moore LR, Post AF, Rocap G and Chisholm SW (2002) Utilization of different nitrogen sources by the marine cyanobacteria Prochlorococcus and Synechococcus. Limnol Oceanogr 47: 989–996Google Scholar
  111. Mor TS, Post AF and Ohad I (1993) The manganese stabilising protein (MSP) of Prochlorothrix hollandica is a hydrophobic membrane-bound protein. Biochim Biophys Acta: 206-212Google Scholar
  112. Morden CW and Golden SS (1989a) psbA genes indicate common ancestry of prochlorophytes and chloroplasts. Nature 337: 382–385PubMedGoogle Scholar
  113. Morden CW and Golden SS (1989b) psbA genes indicate common ancestry of prochlorophytes and chloroplasts: Corrigendum. Nature 339: 400Google Scholar
  114. Morel A, Ahn Y-W, Partensky F, Vaulot D and Claustre H (1993) Prochlorococcus and Synechococcus: A comparative study of their size, pigmentation and related optical properties. J Mar Res 51: 617–649Google Scholar
  115. Muhlenhoff U, Haehnel W, Witt H and Herrmann RG (1993) Genes encoding eleven subunits of Photosystem I from the thermophilic cyanobacterium Synechococcus sp. Gene 127: 71–78PubMedGoogle Scholar
  116. Mullineaux CW (1999) The thylakoid membranes of cyanobacteria: Structure, dynamics and function. Aust J Plant Physiol 26: 671–677Google Scholar
  117. Mullineaux CW, Tobin MJ and Jones GR (1997) Mobility of photosynthetic complexes in thylakoid membranes. Nature 390: 421–424Google Scholar
  118. Murakami A and Fujita Y (1991) Regulation of photosystem stoichiometry in the photosynthetic system of the cyanophyte Synechocystis PCC6714 in response to light intensity. Plant Cell Physiol 32: 223–230Google Scholar
  119. Nelissen B, van de Peer Y, Wilmotte A and De Wachter R (1995) An early origin of plastids within the cyanobacterial divergence is suggested by evolutionary trees based on complete 16S rRNA sequences. Mol Biol Evol 12: 1166–1173PubMedGoogle Scholar
  120. Newcomb EH and Pugh TD (1975) Blue-green algae associated with ascidians of the Great Barrier Reef. Nature 253: 533–534Google Scholar
  121. Omata T, Okada M and Murata N (1985) Separation and partial characterization of membranes from Prochloron sp. Plant Cell Physiol 26: 579–584Google Scholar
  122. Omata T, Price GD, Badger MR, Okamura M, Gohta S and Ogawa T (1999) Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. strain PCC 7942. Proc Natl Acad Sci USA 96: 13571–13576PubMedGoogle Scholar
  123. Paerl HW, Lewin RA and Cheng L (1984) Variations in chlorophyll and carotenoid pigmentation among Prochloron (Prochlorophyta) symbionts in diverse marine ascidians. Bot Mar 27: 257–264Google Scholar
  124. Palenik B and Haselkom R (1992) Multiple evolutionary origins of prochlorophytes, the chlorophyll b-containing prokaryotes. Nature 355: 265–267PubMedGoogle Scholar
  125. Park YI, Sandstrom S, Gustafsson P and Öquist G (1999) Expression of the isiA gene is essential for the survival of the cyanobacterium Synechococcus sp. PCC7942 by protecting Photosystem II from excess light under iron limitation. Mol Microbiol 32: 123–129PubMedGoogle Scholar
  126. Partensky F, Hoepffner N, Li WKW, Ulloa O and Vaulot D (1993) Photoacclimation of Prochlorococcussp (Prochlorophyta) strains isolated from the North Atlantic and the Mediterranean Sea. Plant Physiol 101: 295–296Google Scholar
  127. Partensky F, La Roche J, Wyman K and Falkowski PG (1997) The divinyl-chlorophyll a/b-protein complexes of two strains of the oxyphototrophic marine prokaryote Prochlorococcus— Characterization and response to changes in growth irradiance. Photosynth Res 51: 209–222Google Scholar
  128. Partensky F, Blanchot J and Vaulot D (1999a) Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: A review. In: Charpy L and Larkum AWD (eds) Marine Cyanobacteria, pp 457-475. Institut Océanographique, MonacoGoogle Scholar
  129. Partensky F, Hess WR and Vaulot D (1999b) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63: 106–127PubMedGoogle Scholar
  130. Penno S, Campbell L and Hess WR (2000) Presence of phycoerythrin in two strains of Prochlorococcus (Cyanobacteria) isolated from the subtropical north Pacific Ocean. J Phycol 36: 723–729Google Scholar
  131. Pichard SL, Campbell L and Paul JH (1997) Diversity of the ribulose bisphosphate carboxylase/oxygenase form I gene (rbcL) in natural phytoplankton communities. Appl Environ Microbiol 63: 3600–3606PubMedGoogle Scholar
  132. Pinevich AV, Matthijs HCP, Gavrilova OV, Averina SG and Velichko NV (1996) New ultrastructural aspects of membranes and cell inclusions in Prochlorothrix hollandica (Prochlorales, Cyanobacteria). Microbios 87: 217–225Google Scholar
  133. Pinevich AV, Matthijs HCP, Averina SG and Gavrilova OV (1997) Picocyanophyte (cyanobacterium) from the boreal inland water accumulates phycoerythrin as a major biliprotein. Algol Stud 87: 99–108Google Scholar
  134. Pinevich AV, Skulberg OM, Matthijs HCP, Schubert H, Willen E, Gavrilova OV and Velichko N (1999) Characterization of a novel chlorophyll b-containing Prochlorothrix species (Prochlorophyta) and its photosynthetic apparatus. Microbios 100: 159–174Google Scholar
  135. Pinevich AB, Velichko NB and Bazanova AV (2000) Prochlorophytes twenty years on. Russ J Plant Physiol 47: 639–643Google Scholar
  136. Post AF and Bullerjahn GS (1994) The photosynthetic machinery in Prochlorophytes: Structural properties and ecological significance. FEMS Microbiol Rev 13: 393–414Google Scholar
  137. Post AF, Gal A, Ohad I, Milbauer KM and Bullerjahn GS (1992) Characterization of light-activated reversible phosphorylation of a chlorophyll a/b antenna apoprotein in the photosynthetic prokaryote Prochlorothrix hollandica. Biochim Biophys Acta 1100: 75–82Google Scholar
  138. Post AF, Ohad I, Warner KM and Bullerjahn GS (1993) Energy distribution between Photosy stems I and II in the photosynthetic prokaryote Prochlorothrix hollandica involves a chlorophyll a/b antenna which associates with Photosystem I. Biochim Biophys Acta 1144: 374–384Google Scholar
  139. Reith M (1996) The evolution of plastids and the photosynthetic apparatus. In: Ort DR and Yocum CF (eds) Oxygenic Photosynthesis: The Light Reactions, pp 643-657. Kluwer Academic Publishers, DordrechtGoogle Scholar
  140. Rippka R, Deruelles J, Waterbury JB, Herdmann M and Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111: 1–61Google Scholar
  141. Rippka R, Coursin T, Hess W, Lichtlé C, Scanlan DJ, Palinska KA, Iteman I, Partensky F, Houmard J and Herdman M (2000) Prochlorococcus marinus Chisholm et al. 1992 subsp. pastoris subsp. nov. strain PCC9511, the first axenic chlorophyll a 2/b 2 containing cyanobacterium (Oxyphotobacteria). Int J Syst Evol Microbiol 50: 1833–1847PubMedGoogle Scholar
  142. Sandmann G (1985) Consequences of iron deficiency on photosynthetic and respiratory electron transport in blue-green algae. Photosynth Res 6: 261–271Google Scholar
  143. Sareina M, Tobin MJ and Mullineaux CW (2001) Diffusion of phycobilisomes on the thylakoid membranes of the cyanobacterium Synechococcus 7942: Effects of phycobilisome size, temperature and membrane lipid composition. J Biol Chem 276: 46830–46834Google Scholar
  144. Satoh S, Ikeuchi M, Mimuro M and Tanaka A (2001) Chlorophyll b expressed in cyanobacteria functions as a light-harvesting antenna in Photosystem I through flexibility of the proteins. J Biol Chcm 276: 4293–297Google Scholar
  145. Scanlan DJ, Hess WR, Partensky F, Scanlan J and Vaulot D (1996) High degree of genetic variation in Prochlorococcus (Prochlorophyta) revealed by RFLP analysis. Eur J Phycol 31: 1–9Google Scholar
  146. Serieller HV, Naver H and Moller BL (1997) Molecular aspects of Photosystem I. Physiol Plant 100: 842–851Google Scholar
  147. Schiller H, Senger H, Miyashita H, Miyachi S and Dau H (1997) Light-harvesting in Acaryochloris marina—spectroscopic characterization of a chlorophyll d-dominated photosynthetic antenna system. FEBS Lett 410: 433–436PubMedGoogle Scholar
  148. Schreiber U, Gademann R, Ralph PJ and Larkum AWD (1997) Assessment of photosynthetic performance of Prochloron in Lissoclinum patella in hospite by chlorophyll fluorescence measurements. Plant Cell Physiol 38: 945–951Google Scholar
  149. Schulz-Baldes M and Lewin R (1976) Fine structure of Synechocystis didemni (Cyanophyta: Chroococcales). Phycologia 15: 1–6Google Scholar
  150. Schuster G, Owens GC, Cohen Y and Ohad I (1984) Thylakoid polypeptide composition and light-independent phosphorylation of the chlorophyll a/b-protein in Prochloron, a prokaryote exhibiting oxygenic photosynthesis. Biochim Biophys Acta 767: 596–605Google Scholar
  151. Schyns G, Rippka R, Namane A, Campbell D, Herdman M and Houmard J (1997) Prochlorothrix hollandica PCC9006: Genomic properties of an axenic representative of the chlorophyll a/b-containing oxyphotobacteria. Res Microbiol 148: 345–354PubMedGoogle Scholar
  152. Seewaldt E and Stackebrandt E (1982) Partial sequence of 16S ribosomal RNA and the phylogeny of Prochloron. Nature 295: 618–620Google Scholar
  153. Shen JR and Inoue Y (1993) Binding and functional properties of two new extrinsic components, cytochrome c-550 and a 12kDa protein, in cyanobacterial Photosystem II. Biochemistry 32: 1825–1832PubMedGoogle Scholar
  154. Shen JR, Ikeuchi M and Inoue Y (1997) Analysis of the psbU gene cncoding the 12-kDa extrinsic protein of Photosystem II and studies on its role by deletion mutagenesis in Synechocystis sp. PCC6803. JBiol Chem 272: 17821–17826Google Scholar
  155. Shimada A, Kanai S, Lewin RA and Maruyama T (1999) Molecular phylogenetic relationship between Synechocystis trididemni and Prochloron didemni. In: Charpy L and Larkum AWD (eds) Marine Cyanobacteria, pp 117-120. Institut Océanographique, MonacoGoogle Scholar
  156. Siefermann-Harms D (1985) Carotenoids in photosynthesis. I. Location in photosynthetic membranes and light-harvesting function. Biochim Biophys Acta 811: 325–355Google Scholar
  157. Staehelin LA and van der Staay GWM (1996) Structure, composition, functional organization and dynamic properties of thylakoid membranes. In: Ort DR and Yocum F (eds) Oxygenic Photosynthesis: The Light Reactions, pp 11-30. Kluwer Academic Publishers, DordrechtGoogle Scholar
  158. Stiller JW and Hall BD (1997) The origin of red algae: Implications for plasmid evolution. Proc Natl Acad Sci USA 94: 4520–4525PubMedGoogle Scholar
  159. Swift H (1989) The cytology of Prochloron. In: Lewin R and Cheng L (eds) Prochloron, a microbial enigma, pp 71-81. Chapman and Hall, New YorkGoogle Scholar
  160. Swift H and Leser GP (1989) Cytochemical studies on prochlorophytes: Localization of DNA and ribulose 1,5biphosphate carboxylase-oxygenase. J Phycol 25: 751–761Google Scholar
  161. Tanaka A, Ito H, Tanaka R, Tanaka NK, Yoshida K and Okada K (1998) Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. Proc Natl Acad Sci USA 95: 12719–12723PubMedGoogle Scholar
  162. Thorne SW, Newcomb EH and Osmond CB (1977) Identification of chlorophyll b in extracts of prokaryotic algae by fluorescence spectroscopy. Proc Acad Nat Sci Philadelphia 74: 575–578Google Scholar
  163. Ting C, Rocap G, King J and Chisholm SW (1998) Characterization of phycoerythrin genes in the chlorophyll a 2/b 2containing procaryote, Prochlorococcus sp. MIT9303. In: Garab G (ed) Photosynthesis: Mechanisms and Effects, Vol 1, pp 225-228. Kluwer Academic Publishers, DordrechtGoogle Scholar
  164. Ting CS, Rocap G, King J and Chisholm SW (2001) Phyeobiliprotein genes of the marine photosynthetic prokaryote Prochlorococcus: Evidence for rapid evolution of genetic heterogeneity. Microbiology 147: 3171–3182PubMedGoogle Scholar
  165. Tomitani A, Okada K, Miyashita H, Matthijs HCP, Ohno T and Tanaka A (1999) Chlorophyll b and phycobilins in the common ancestor of cyanobacteria and chloroplasts. Nature 400: 159–162PubMedGoogle Scholar
  166. Trissl H-W and Wilhelm C (1993) Why do thylakoids form grana stacks? Trends Biochem Sci 18: 415–419PubMedGoogle Scholar
  167. Turner S, Burger-Wiersma T, Giovannoni SJ, Mur LR and Pace NR (1989) The relationship of a prochlorophyte Prochlorothrix hollandica to green chloroplasts. Nature 337: 380–382PubMedGoogle Scholar
  168. Turner S, Pryer KM, Miao VPW and Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Euk Microbiol 46: 327–338PubMedGoogle Scholar
  169. Urbach E, Robertson DL and Chisholm SW (1992) multiple evolutionary origins of prochlorophytes within the cyanobacterial radiation. Nature 355: 267–270PubMedGoogle Scholar
  170. Urbach E, Scanlan DJ, Distel DL, Waterbury JB and Chisholm SW (1998) Rapid diversification of marine picophytoplankton with dissimilar light-harvesting structures inferred from sequences of Prochlorococcus and Synechococcus (Cyanobacteria). J Mol Evol 46: 188–201PubMedGoogle Scholar
  171. van der Staay GWM and Partensky F (1999) The 21 kDa protein associated with Photosystem I in Prochlorococcus marinus is the PsaF protein (AJ131438)(PGR99-067). Plant Physiol 120: 339Google Scholar
  172. van der Staay GWM and Staehelin LA (1994) Biochemical characterization of protein composition and protein phosphorylation patterns in stacked and unstacked thylakoid membranes of the prochlorophyte Prochlorothrix hollandica. J Biol Chem 269: 24834–24844PubMedGoogle Scholar
  173. van der Staay GWM, Matthijs HCP and Muur LR (1989) Phosphorylation and dephosphorylation of membrane proteins from the prochlorophyte Prochlorothrix hollandica in fixed redox states. Biochim Biophys Acta 975: 317–324Google Scholar
  174. van der Staay GWM, Brouwer A, Baard RL, van Mourik F and Matthijs HCP (1992) Separation of Photosystems I and II from the oxychlorobacterium (prochlorophyte) Prochlorothrix hollandica and association of chlorophyll b binding antennae with Photosystem II. Biochim Biophys Acta 1102: 220–228Google Scholar
  175. van der Staay GWM, Boekema EJ, Dekker JP and Matthijs HCP (1993) Characterization of trimeric Photosystem I particles from the prochlorophyte Prochlorothrix hollandica by electron microscopy and image analysis. Biochim Biophys Acta 1142: 189–193Google Scholar
  176. van der Staay GWM, Moon-van der Staay SY, Garczarek L and Partensky F (1998a) Characterization of the Photosystem I subunits Psal and PsaL from two strains of the marine oxyphototrophic prokaryote Prochlorococcus. Photosynth Res 57: 183–191Google Scholar
  177. van der Staay GWM, Yurkova N and Green BR (1998b) The 38 kDa chlorophyll a/b protein of the prokaryote Prochlorothrix hollandica is encoded by a divergent pcb gene. Plant Mol Biol 36: 709–716PubMedGoogle Scholar
  178. van der Staay GWM, Moon-van der Staay SY, Garczarek L and Partensky F (2000) Rapid evolutionary divergence of Photosystem I core subunits PsaA and PsaB in the marine prokaryote Prochlorococcus. Photosynth Res 65: 131–139PubMedGoogle Scholar
  179. Veldhuis MJW and Kraay GW (1990) Vertical distribution and pigment composition of a picoplanktonic prochlorophyte in the subtropical North-Atlantic: A combined study of HPLCanalysis of pigments and flow cytometry. Mar Ecol Prog Ser 68: 121–127Google Scholar
  180. West NJ and Scanlan DJ (1999) Niche-partitioning of Prochlorococcus populations in a stratified water column in the eastern north Atlantic occan. Appl Environ Microbiol 65: 2585–2591PubMedGoogle Scholar
  181. Whatley JM (1977) The fine structure of Prochloron. New Phytol 79: 309–313Google Scholar
  182. Wilmotte A (1994) Molecular evolution and taxonomy of Cyanobacteria. In: Bryant DA (ed) The Molecular Biology of Cyanobacteria, pp 1-25. Kluwer Academic Publishers, DordrechtGoogle Scholar
  183. Withers NW, Alberte RS, Lewin RA and Thornber JP (1978) Photosynthetic unit size, carotenoids and chlorophyll-protein composition of Prochloron sp., a prokaryotic green alga. Proc Natl Acad Sci USA 75: 2301–2305PubMedGoogle Scholar
  184. Wood AM (1979) Chlorophyll a:b ratios in marine planktonic algae. J Phycol 15: 330–3Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2003

Authors and Affiliations

  1. 1.Station BiologiqueCentre National de la Recherche Scientifique et Université Pierre et Marie CurieRoscoff CxFrance

Personalised recommendations