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Salinity Tolerance of the Chlorophyll b-synthesizing Cyanobacterium Prochlorothrix hollandica Strain SAG 10.89

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Abstract

Ecophysiological investigations on the salinity acclimation of the cyanobacterium Prochlorothrix hollandica SAG 10.89 led to significantly revised salinity tolerance limits. Besides potential effects of cultivation techniques, clear ion composition effects mainly explain formerly described hypersensitivity to NaCl-mediated salinity and lack of osmolyte detection. An extraordinarily broad plasticity of cellular chlorophyll a/b ratios occurred with variations of NaCl-induced salinity. Photosynthesis characteristics, pigment regulation, respiration, and biomass yield in growth medium with field-like ion composition indicated generally reduced acclimation pressure. A simultaneously significant increase in osmolyte (sucrose) accumulation indicated more efficient osmotic acclimation. Minor growth inhibition up to salinities of 10 practical salinity units enlarged the potential habitat of P. hollandica but at the most to about 300,000 km2 in the Baltic Sea. This supports probable observations of Prochlorothrix sp. in phytoplankton assemblages of open waters in Baltic Sea-monitoring studies. Brackish habitats differ from so far known habitats of Prochlorothrix spp. in turbidity, productivity, and plankton composition. Adjusted physiological features dispel fundamental doubts on the establishment of filamentous prochlorophytes in brackish waters.

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References

  1. Allakhverdiev SI, Nishiyama Y, Suzuki, I, Tasaka Y, Murata N (1999) Genetic engineering of the unsaturation of fatty acids in membrane lipids alters the tolerance of Synechocyctis to salt stress. Proc Natl Acad Sci USA 96:5862–5867

    Article  PubMed  CAS  Google Scholar 

  2. Allakhverdiev SI, Sakamoto A, Nishiyama Y, Inaba M, Murata N (2000) Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiol 123:1047–1056

    Article  PubMed  CAS  Google Scholar 

  3. Andrizhiyevskaya EG, Schwabe TME, Germano M, D’Haene S, Kruip J, van Grondelle R, Dekker JP (2002) Spectroscopic properties of PSI-IsiA supercomplexes from the cyanobacterium Synechococcus PCC 7942. Biochim Biophys Acta 1556:265–272

    Article  PubMed  CAS  Google Scholar 

  4. BACC (2006) Assessment of climate change for the Baltic Sea basin—the BACC project. Int Conf, 22–23 May 2006, Göteborg, Sweden. Chapter summaries, available at: http://dvsun3.gkss.de/ BACC/

  5. Bumba L, Prasil O, Vacha F (2005) Antenna ring around trimeric Photosystem I in chlorophyll b containing cyanobacterium Prochlorothrix hollandica. Biochim Biophys Acta 1708:1–5

    Article  PubMed  CAS  Google Scholar 

  6. Burger-Wiersma T, Veenhuis M, Korthals HJ, van der Wiel CCM, Mur LR (1986) A new prokaryote containing chlorophylls a and b. Nature 320:262–264

    Article  CAS  Google Scholar 

  7. Burger-Wiersma T, Stal LJ, 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 39:250–257

    Article  Google Scholar 

  8. Burger-Wiersma T, Post AF (1989) Functional analysis of the photosynthetic apparatus of Prochlorothrix hollandica (Prochlorales), a chlorophyll b containing prokaryote. Plant Physiol 91:770–774

    PubMed  CAS  Google Scholar 

  9. Burger-Wiersma T, Matthijs HCP (1990) The biology of the prochlorales. In: Codd GA (ed) Autotrophic microbiology and one-carbon metabolism. Kluwer, Dordrecht, pp 1–24

    Google Scholar 

  10. Chisholm SW, Olsen RJ, Zettler ER, Waterbury JB, Goericke, R, Welschmeyer N (1988) A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334:340–343

    Article  Google Scholar 

  11. Cunningham FX, Gantt E (1998) Genes and enzymes of carotenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 49:557–583

    Article  PubMed  CAS  Google Scholar 

  12. Demmig-Adams B (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24

    Article  CAS  Google Scholar 

  13. Erdmann N (1983) Organic osmoregulatory solutes in blue-green algae. Z Pflanzenphysiol 110:147–155

    CAS  Google Scholar 

  14. Erdmann N, Hagemann M, Berg C, Fulda S (1990) Basis of salt adaptation in cyanobacteria. Limnologica (Berlin) 20:57–60

    Google Scholar 

  15. Ferjani A, Mustardy L, Sulpice R, Marin K, Isuzuki I, Hagemann M, Murata N (2003) Glucosylglycerol, a compatible solute, sustains cell division under salt stress. Plant Physiol 131(4):1628–1637

    Article  PubMed  CAS  Google Scholar 

  16. Geiß U, Bergmann I, Blank M, Schumann R, Hagemann M, Schoor A (2003) Detection of Prochlorothrix in brackish waters by specific amplification of pcb genes. Appl Environ Microbiol 69:6243–6249

    Article  PubMed  CAS  Google Scholar 

  17. Golden SS, Morden CW, Greer KL (1993) Comparison of sequences and organization of photosynthesis genes among the prochlorophyte Prochlorothrix hollandica, cyanobacteria, and chloroplasts. In: Lewin RA (ed) Origins of plastids: symbiogenesis, prochlorophytes and the origins of chloroplasts. Chapman & Hall, New York, pp 141–158

    Google Scholar 

  18. Golecki JR, Jürgens UJ (1989) Ultrastructural studies on the membrane systems and cell inclusions of the filamentous prochlorophyte Prochlorothrix hollandica. Arch Microbiol 152:77–82

    Article  Google Scholar 

  19. Hagemann M, Fulda S, Schubert H (1994) DNA, RNA and protein synthesis in the cyanobacterium Synechocystis sp. PCC 6803 adapted to different salt concentrations. Cur Microbiol 28:201–207

    Article  CAS  Google Scholar 

  20. Hincha DK, Hagemann M (2004) Stabilization of model membranes during drying by compatible solutes involved in the stress tolerance of plants and microorganisms. Biochem J 383:277–283

    Article  PubMed  CAS  Google Scholar 

  21. Ihalainen JA, D’Haene S, Yeremenko N, van Roon H, Arteni AA, Boekema EJ, van Grondelle R, Matthijs HC, Dekker JP (2005) Aggregates of the chlorophyll-binding protein IsiA (CP43')dissipate energy in cyanobacteria. Biochemistry 44:10846–10853

    Article  PubMed  CAS  Google Scholar 

  22. Jakobsen TS, Hansen PB, Jeppesen E, Søndergaard M (2004) Cascading effect of three-spined stickleback Gasterosteus aculeatus on community composition, size, biomass and diversity of phytoplankton in shallow, eutrophic brackish lagoons. Mar Ecol Prog Ser 279:305–309

    Article  Google Scholar 

  23. Joset F, Jeanjean R, Hagemann M (1996) Dynamics of the response of cyanobacteria to salt stress: deciphering the molecular events. Physiol Plant 96:738–744

    Article  CAS  Google Scholar 

  24. Kirst GO (1979) Osmotische Adaptation der marinen Planktonalge Platymonas subcordiformis. Ber Deutsch Bot Ges 92:31–42

    CAS  Google Scholar 

  25. Lefort-Tran M, Pouphile M, Spath S, Packer L (1988) Cytoplasmic membrane changes during adaptation of the fresh water cyanobacterium Synechococcus 6311 to salinity. Plant Physiol 87:767–775

    Article  PubMed  CAS  Google Scholar 

  26. Lewin RA (1975) A marine Synechocystis (Cyanophyta, Chlorococcales) epizoic on ascidians. Phycol 14:153–169

    Google Scholar 

  27. Lewin RA (1976) Prochlorophyta as a proposed new division of algae. Nature 261:697–698

    Article  PubMed  CAS  Google Scholar 

  28. Lewin RA (1977) Prochloron, type genus of the Prochlorophyta. Phycologia 16:217

    Google Scholar 

  29. Mathews-Roth MM (1987) Photoprotection by carotenoids. Fed Proc 46:1890–1893

    PubMed  CAS  Google Scholar 

  30. Nishiyama Y, Los DA, Murata N (1999) PsbU, a protein associated with photosystem II, is required for the acquisition of cellular thermotolerance in Synechococcus sp. PCC 7002. Plant Physiol 120:176–182

    Article  Google Scholar 

  31. Oren A (1999) Bioenergetic aspects of halophilism. Microbiol Mol Biol Rev 63:334–348

    PubMed  CAS  Google Scholar 

  32. Partensky F, Hess WR, Vaulot D (1999) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63:106–127

    PubMed  CAS  Google Scholar 

  33. Pinevich AV, Skulberg OM, Matthijs HCP, Schubert H, Willen E, Gavrilova OV, Velichko, NV (1999) Characterisation of a novel Chlorophyll b-containing Prochlorothrix species (Prochlorophyta) and its photosynthetic apparatus. Microbios 100:159–174

    CAS  Google Scholar 

  34. Platt T, Gallegos CL, Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687–701

    Google Scholar 

  35. Post AF, Arieli B (1997) Photosynthesis of Prochlorothrix hollandica under sulfide-rich anoxic conditions. Appl Environ Microbiol 63:3507–3511

    PubMed  CAS  Google Scholar 

  36. Provasoli L (1968) Media and prospect for the cultivation of marine algae. In: Watanabe A, Hattori A (eds) Cultures and collections of algae. Proceedings of US–Japan Conference, Hakone, Sept. 1966. The Japanese Society of Plant Physiologists, Hakone, Japan, pp 63–75

    Google Scholar 

  37. Reed RH, Stewart WDP (1985) Osmotic adjustment and organic solute accumulation in unicellular cyanobacteria from freshwater and marine habitats. Mar Biol 88:1–9

    Article  CAS  Google Scholar 

  38. Reed RH, Stewart WDP (1988) The responses of cyanobacteria to salt stress. In: Rogers LJ, Gallon JR (eds) Biochemistry of the algae and cyanobacteria, vol. 12. Clarendon, Oxford, pp 217–231

    Google Scholar 

  39. Rippka R, Deruelles J, Waterbury JB, Herdmann M, Stainer RY (1979) Generic asignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  40. Scanlan DJ, West NJ (2002) Molecular ecology of the marine cyanobacterial genera Prochlorococcus and Synechococcus. FEMS Microbiol Ecol 40(1):1–12

    Article  CAS  PubMed  Google Scholar 

  41. Schoor A, Erdmann N, Effmert U, Mikkat S (1995) Determination of the cyanobacterial osmolyte glycosylglycerol by high-performance liquid chromatography. J Chromatogr A 704:89–97

    Article  CAS  Google Scholar 

  42. Schoor A, Hagemann M, Erdmann N (1999) Glucosylglycerol-phosphate synthase: target for ion-mediated regulation of osmolyte synthesis in the cyanobacterium Synechocystis sp. strain PCC 6803. Arch Microbiol 171:101–106

    Article  PubMed  CAS  Google Scholar 

  43. Schubert H, Fulda S, Hagemann M (1993) Effects of adaptation to different salt concentrations on photosynthesis and pigmentation of the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 142:291–295

    CAS  Google Scholar 

  44. van den Hoek C, Jahns HM, Mann DG (eds) (1993) Algen. Thieme, Stuttgart, pp 15–34

  45. van der Staay GWM, Brouwer A, Baard RL, van Mourik F, 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 1102:220–228

    Article  Google Scholar 

  46. Walsby AE (1997) Numerical integration of phytoplankton photosynthesis through time and depth in a water column. New Phytol 136:189–209

    Article  CAS  Google Scholar 

  47. Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Plant Physiol 144:307–313

    CAS  Google Scholar 

  48. Wolfstein K, Hartig P (1998) The photosynthetic light dispensation system: application to microphytobenthic primary production measurements. Mar Ecol Prog Ser 166:63–71

    Article  Google Scholar 

  49. Yeremenko N, Kouril R, Ihalainen JA, D’Haene S, van Oosterwijk N, Andrizhiyevskaya EG, Keegstra W, Dekker HL, Hagemann M, Boekema EJ, Matthijs HC, Dekker JP (2004) Supramolecular organization and dual function of the IsiA chlorophyll-binding protein in cyanobacteria. Biochemistry 43:10308–10313

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank S. Görs for a chromatographic verification of sucrose accumulation. The detailed and helpful suggestions of an anonymous reviewer are kindly acknowledged. This work was partially supported by a grant of the Deutsche Forschungsgemeinschaft (DFG).

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Correspondence to Arne Schoor.

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Bergmann, I., Geiß-Brunschweiger, U., Hagemann, M. et al. Salinity Tolerance of the Chlorophyll b-synthesizing Cyanobacterium Prochlorothrix hollandica Strain SAG 10.89. Microb Ecol 55, 685–696 (2008). https://doi.org/10.1007/s00248-007-9311-5

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