Advertisement

Seaweed Acclimation to Salinity and Desiccation Stress

  • Ulf Karsten
Chapter
Part of the Ecological Studies book series (ECOLSTUD, volume 219)

Abstract

Physiological performance, distribution, and biodiversity of seaweeds are primarily controlled by various environmental factors such as salinity and drought. Fluctuating salinity and desiccation is typically a local rather than a global parameter and can be highly variable in coastal regions. This chapter focuses on the effects of changing salinities and desiccation on physiological processes in seaweeds such as growth, photosynthesis, and respiration as well as on osmotic acclimation. In addition, ultrastructural changes and the development of salinity ecotypes are discussed. Although the principal mechanisms of osmotic acclimation in seaweeds such as ion transport and biosynthesis of organic osmolytes are well understood, the underlying molecular expression and regulation patterns are still mainly unstudied. To overcome this gap in knowledge more genomes of model seaweeds are urgently needed to get a fundamental understanding of salinity and desiccation stress responses.

Keywords

Salinity Stress Salinity Tolerance Brown Seaweed Seaweed Species Organic Osmolytes 
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.

Notes

Acknowledgments

The author likes to thank many of his colleagues for excellent collaboration on salinity stress in seaweeds over the last two decades, particularly Robert King, Gunter Kirst, Annika Mostaert, John West, and Christian Wiencke, as well as the Deutsche Forschungsgemeinschaft for funding various projects.

References

  1. Allakhverdiev SI, Murata N (2008) Salt stress inhibits photosystems II and I in cyanobacteria. Photosynth Res 98:529–539PubMedGoogle Scholar
  2. Anderson RJ, Velimirov B (1982) An experimental investigation of the palatability of kelp bed algae to the sea urchin Parechinus angulosus Leske. P.S.Z.N.I. Mar Ecol 3:357–373Google Scholar
  3. Asada K (1994) Production and action of active oxygen species in photosynthetic tissues. In: Foyer CH, Mullineaux PM (eds) Causes of photooxidative stress and amelioration of defence systems in plants. CRC, Boca Raton, pp 77–104Google Scholar
  4. Ballal A, Basu B, Apte SK (2007) The Kdp-ATPase system and its regulation. J Biosci 32:559–568PubMedGoogle Scholar
  5. Bartsch I, Wiencke C, Bischof K, Buchholz CM, Buck BH, Eggert A, Feuerpfeil P, Hanelt D, Jacobsen S, Karez R, Karsten U, Molis M, Roleda MY, Schubert H, Schumann R, Valentin K, Weinberger F, Wiese J (2008) The genus Laminaria sensu lato: recent insights and developments. Eur J Phycol 43:1–86Google Scholar
  6. Bird CJ, McLachlan J (1986) The effect of salinity on distribution of species of Gracilaria (Rhodophyta, Gigartinales): an experimental assessment. Bot Mar 29:231–238Google Scholar
  7. Bird NL, Chen LCM, McLachlan J (1979) Effects of temperature, light and salinity on growth in culture of Chondrus crispus, Furcellaria lumbricalis, Gracilaria tikvahiae (Gigartinales, Rhodophyta), and Fucus serratus (Fucales, Phaeophyta). Bot Mar 22:1–27Google Scholar
  8. Bischof K, Peralta G, Kräbs G, van den Poll WH, Perez-Llorens JL, Breeman AM (2002) Effects of solar UV-B radiation on canopy structure of Ulva communities from southern Spain. J Exp Bot 379:2411–2421Google Scholar
  9. Bisson MA, Gutknecht J (1975) Osmotic regulation in the marine alga, Codium decorticatum. I. Regulation of turgor pressure by control of ionic composition. J Membr Biol 37:85–98Google Scholar
  10. Bisson MA, Kirst GO (1983) Osmotic adaptations of charophyte algae in the Coorong, South Australia and other Australian lakes. Hydrobiology 105:45–51Google Scholar
  11. Bisson MA, Kirst GO (1995) Osmotic acclimation and turgor pressure regulation in algae. Naturwissenschaften 82:461–471Google Scholar
  12. Bolton JJ (1979) Estuarine adaptation in populations of Pilayella littoralis (L.) Kjellm. (Phaeophyta, Ectocarpales). Estuar Coast Mar Sci 9:273–280Google Scholar
  13. Brown AD, Simpson JR (1972) Water relations of sugar-tolerant yeasts: the role of intracellular polyols. J Gen Microb 72:589–591Google Scholar
  14. Choi TS, Kang EJ, Kim JH, Kim KY (2010) Effect of salinity on growth and nutrient uptake of Ulva pertusa (Chlorophyta) from an eelgrass bed. Algae 25:17–26Google Scholar
  15. Chudek JA, Foster R, Davison IR, Reed RH (1984) Altritol in the brown alga Himanthalia elongata. Phytochemistry 23:1081–1082Google Scholar
  16. Cock JM, Sterck L, Rouze P, Scornet D, Allen AA, Amoutzias G, Anthourad V, Artiguenave F, Aury JM, Badger JH et al (2010) The Ectocarpus genome and the independent evolution of multicellularity in the brown algae. Nature 465:617–621PubMedGoogle Scholar
  17. Craigie JS (1974) Storage products. In: Stewart WDP (ed) Algal physiology and biochemistry. Blackwell, Oxford, pp 206–235Google Scholar
  18. Dai YD, Zhao G, Jin SX, Ji LY, De LD, Man LW, Wang B (2004) Construction and characterization of a bacterial artificial chromosome library of marine macroalga Porphyra yezoensis (Rhodophyta). Plant Mol Biol Rep 22:375–386Google Scholar
  19. Davison IR, Reed RH (1985a) Osmotic adjustment in Laminaria digitata (Phaeophyta) with particular reference to seasonal changes in internal solute concentrations. J Phycol 21:41–50Google Scholar
  20. Davison IR, Reed RH (1985b) The physiological significance of mannitol accumulation in brown algae: the role of mannitol as a compatible cytoplasmic solute. Phycologia 24:449–457Google Scholar
  21. Dickson DMJ, Kirst GO (1986) The role of dimethylsulphoniopropionate, glycine betaine and homarine in the osmoacclimation of Platymonas subcordiformis. Planta 155:409–415Google Scholar
  22. Druehl LD (1967) Distribution of two species of Laminaria as related to environmental factors. J Phycol 3:103–108Google Scholar
  23. Eggert A, Karsten U (2010) Low molecular weight carbohydrates in red algae – an ecophysiological and biochemical perspective. In: Seckbach J, Chapman D, Weber A (eds) Cellular origins, life in extreme habitats and astrobiology red algae in the genomics age. Springer, Berlin, pp 445–456Google Scholar
  24. Eppley RW, Bovell CR (1958) Sulphuric acid in Desmarestia. Biol Bull 115:101–106Google Scholar
  25. Fork DC, Öquist G (1981) The effects of desiccation on excitation energy transfer at physiological temperatures between the two photosystems of the red alga Porphyra perforata. Z Pflanzenphysiol 104:385–393Google Scholar
  26. Gerard VA, Dubois K, Greene R (1987) Growth responses of two Laminaria saccharina populations to environmental variation. Hydrobiology 151(152):229–232Google Scholar
  27. Gessner F, Schramm W (1971) Salinity: plants. In: Kinne O (ed) Marine ecology, vol 1(2), Environmental factors. Wiley Interscience, London, pp 705–1083Google Scholar
  28. Gimmler H (2000) Primary sodium plasma membrane ATPases in salttolerant algae: facts and fictions. J Exp Bot 348:1171–1178Google Scholar
  29. Gimmler H, Kaaden R, Kirchner U, Weyand A (1984) The chloride sensitivity of Dunaliella parva enzymes. Z Pflanzenphysiol 114:131–50Google Scholar
  30. Gustavs L, Schumann R, Eggert A, Karsten U (2009) In vivo growth fluorometry: accuracy and limits of microalgal growth rate measurements in ecophysiological investigations. Aquat Microb Ecol 55:95–104Google Scholar
  31. Gutknecht J, Hastings DF, Bisson MA (1978) Ion transport and turgor pressure regulation in giant algal cells. In: Giebisch G, Tosteson DC, Ussing HH (eds) Membrane transport in biology, vol 3, Transport across biological membranes. Springer, Berlin, pp 25–74Google Scholar
  32. Hagemann M (2011) Molecular biology of cyanobacterial salt acclimation. FEMS Microbiol Rev 35:87–123PubMedGoogle Scholar
  33. Hanelt D, Tüg H, Bischof K, Groß C, Lippert H, Sawall T, Wiencke C (2001) Light regime in an Arctic fjord: a study related to stratospheric ozone depletion as a basis for determination of UV effects on algal growth. Mar Biol 138:649–658Google Scholar
  34. Inaba M, Sakamoto A, Murata N (2001) Functional expression in Escherichia coli of low-affinity and high-affinity Na+(Li+)/H+ antiporters of Synechocystis. J Bacteriol 183:1376–1384PubMedCentralPubMedGoogle Scholar
  35. Iwamoto K, Kawanobe H, Ikawa T, Shiraiwa Y (2003) Characterization of salt-regulated mannitol-1-phosphate dehydrogenase in the red alga Caloglossa continua. Plant Physiol 133:893–900PubMedCentralPubMedGoogle Scholar
  36. Jacob A, Kirst GO, Wiencke C, Lehmann H (1991) Physiological responses of the Antarctic green alga Prasiola crispa ssp. antarctica to salinity stress. J Plant Physiol 139:57–62Google Scholar
  37. Jacob A, Wiencke C, Lehmann H, Kirst GO (1992) Physiology and ultrastructure in the green alga Prasiola crispa from Antarctica. Bot Mar 35:297–303Google Scholar
  38. Jentsch TJ (2008) CLC chloride channels and transporters: from genes to protein structure, pathology and physiology. Crit Rev Biochem Mol 43:3–36Google Scholar
  39. Kain JM, Norton TA (1990) Marine ecology. In: Cole KM, Sheath RG (eds) Biology of the red algae. Cambridge University Press, Cambridge, pp 377–422Google Scholar
  40. Kaneko T, Sato S, Kotani H et al (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136PubMedGoogle Scholar
  41. Karsten U (1999) Seasonal variation in heteroside concentrations of field-collected Porphyra species (Rhodophyta) from different biogeographic regions. New Phytol 143:561–571Google Scholar
  42. Karsten U, West JA (1993) Ecophysiological studies on six species of the mangrove red algal genus Caloglossa. Aust J Plant Physiol 20:729–739Google Scholar
  43. Karsten U, Wiencke C, Kirst GO (1991a) The effect of salinity changes upon the physiology of eulittoral green macroalgae from Antarctica and Southern Chile. I. Cell viability, growth, photosynthesis and dark respiration. J Plant Physiol 138:667–673Google Scholar
  44. Karsten U, Wiencke C, Kirst GO (1991b) The effect of salinity changes upon the physiology of eulittoral green macroalgae from Antarctica and Southern Chile. II. Intracellular inorganic ions and organic compounds. J Exp Bot 245:1533–1539Google Scholar
  45. Karsten U, Barrow KD, King RJ (1993a) Floridoside, L-isofloridoside, and D- isofloridoside in the red alga Porphyra columbina. Plant Physiol 103:485–491PubMedCentralPubMedGoogle Scholar
  46. Karsten U, West JA, Ganesan EK (1993b) Comparative physiological ecology of Bostrychia moritziana (Ceramiales, Rhodophyta) from freshwater and marine habitats. Phycologia 32:401–409Google Scholar
  47. Karsten U, West JA, Zuccarello G, Kirst GO (1994) Physiological ecotypes in the marine red alga Bostrychia radicans (Ceramiales, Rhodophyta) from the east coast of the USA. J Phycol 30:174–182Google Scholar
  48. Karsten U, Bock C, West JA (1995) Low molecular weight carbohydrate patterns in geographically different isolates of the eulittoral red alga Bostrychia tenuissima from Australia. Bot Acta 108:321–326Google Scholar
  49. Karsten U, Barrow KD, Nixdorf O, King RJ (1996a) The compability of unusual organic osmolytes from mangrove red algae with enzyme activity. Aust J Plant Physiol 23:577–582Google Scholar
  50. Karsten U, Koch S, West JA, Kirst GO (1996b) Physiological responses of the eulittoral macroalga Stictosiphonia hookeri (Rhodomelaceae, Rhodophyta) from Argentina and Chile: salinity, light and temperature acclimation. Eur J Phycol 31:361–368Google Scholar
  51. Karsten U, Barrow KD, Nixdorf O, West JA, King RJ (1997) Characterization of mannitol metabolism in the mangrove red alga Caloglossa leprieurii (Montagne) J. Agardh Planta 201:173–178Google Scholar
  52. Karsten U, West JA, Zuccarello GC, Nixdorf O, Barrow KD, King RJ (1999) Low molecular weight carbohydrate patterns in the Bangiophyceae (Rhodophyta). J Phycol 35:967–976Google Scholar
  53. Karsten U, Dummermuth A, Hoyer K, Wiencke C (2003a) Interactive effects of ultraviolet radiation and salinity on the ecophysiology of two Arctic red algae from shallow waters. Polar Biol 26:249–258Google Scholar
  54. Karsten U, West JA, Zuccarello GC, Engbrodt R, Yokoyama A, Hara Y, Brodie J (2003b) Low molecular weight carbohydrates of the Bangiophycidae (Rhodophyta). J Phycol 39:584–589Google Scholar
  55. Karsten U, Michalik D, Michalik M, West JA (2005) A new unusual low molecular weight carbohydrate in the red algal genus Hypoglossum (Delesseriaceae, Ceramiales) and its possible function as osmolyte. Planta 222:319–326PubMedGoogle Scholar
  56. Karsten U, Görs S, Eggert A, West JA (2007) Trehalose, digeneaside and floridoside in the Florideophyceae (Rhodophyta) – a re-evaluation of its chemotaxonomic value. Phycologia 46:143–150Google Scholar
  57. Kauss H (1987) Some aspects of calcium-dependent regulation in plant metabolism. Annu Rev Plant Physiol 38:47–72Google Scholar
  58. Kirst GO (1990) Salinity tolerance of eukaryotic marine algae. Annu Rev Plant Physiol Plant Mol Biol 41:21–53Google Scholar
  59. Kremer BP (1976) Distribution and biochemistry of alditols in the genus Pelvetia (Phaeophyceae, Fucales). Br Phycol J 11:239–243Google Scholar
  60. Kremer BP (1978) Patterns of photoassimilatory products in Pacific Rhodophyceae. Can J Bot 56:1655–1659Google Scholar
  61. Kremer BP, Kirst GO (1981) Biosynthesis of 2-O-D-glycerol-D-galactopyranoside (floridoside) in marine Rhodophyceae. Plant Sci Lett 23:349–357Google Scholar
  62. Lindberg B (1955) Low-molecular carbohydrates in algae. XI. Investigation of Porphyra umbilicalis. Acta Chem Scand 9:1097–1099Google Scholar
  63. Lüning K (1990) Seaweeds: their environment, biogeography, and ecophysiology. Wiley, New YorkGoogle Scholar
  64. Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann Bot 84:123–133Google Scholar
  65. Matsuda N, Kobayashi H, Katoh H, Ogawa T, Futatsugi L, Nakamura T, Bakker EP, Uozumi N (2004) Na+-dependent K+ uptake Ktr system from the cyanobacterium Synechocystis sp. PCC 6803 and its role in the early phases of cell adaptation to hyperosmotic shock. J Biol Chem 279:54952–54962PubMedGoogle Scholar
  66. Meng J, Rosell KG, Srivastava LM (1987) Chemical characterization of floridosides from Porphyra perforata. Carbohyd Res 161:171–180Google Scholar
  67. Mostaert AS, King RJ (1993) The cell wall of the halotolerant red alga Caloglossa leprieurii (Montagne) J. agardh (Ceramiales, Rhodophyta) from freshwater and marine habitats: effect of changing salinity. Crypt Bot 4:40–46Google Scholar
  68. Nygard CA, Dring MJ (2008) Influence of salinity, temperature and dissolved inorganic carbon and nutrient concentration on the photosynthesis and growth on Fucus vesiculosus from Baltic and Irish Seas. Eur J Phycol 43:253–262Google Scholar
  69. Reed RH (1983) The osmotic response of Polysiphonia lanosa from marine and estuarine sites: evidence for incomplete recovery of turgor. J Exp Mar Biol Ecol 68:69–93Google Scholar
  70. Reed RH (1984) The effects of extreme hyposaline stress upon Polysiphonia lanosa (L.) Tandy from marine and estuarine sites. J Exp Mar Biol Ecol 76:131–144Google Scholar
  71. Reed RH (1990) Solute accumulation and osmotic adjustment. In: Cole KM, Sheath RG (eds) Biology of the red algae. Cambridge University Press, Cambdrige, pp 147–170Google Scholar
  72. Remane A (1940) Einführung in die zoologische Ökologie der Nord- und Ostsee. In: Grimpe G, Wagler E (eds) Die Tierwelt der Nord- und Ostsee, 1a. – Akademische Verlagsgesellschaft Leipzig, pp 1–238Google Scholar
  73. Rietema H (1993) Ecotypic differences between baltic and north-sea populations of Delesseria sanguinea and Membranoptera alata. Bot Mar 36:15–21Google Scholar
  74. Ritchie RJ (1988) The ionic relations of Ulva lactuca. J Plant Physiol 33:183–192Google Scholar
  75. Roberts MF (2005) Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Systems 1:5. doi: 10.1186/1746-1448-1-5 PubMedCentralPubMedGoogle Scholar
  76. Rousvoal S, Groisillier A, Dittami SM, Michel G, Boyen C, Tonon T (2011) Mannitol-1-P dehydrogenase activity in Ectocarpus siliculosus, a key role for mannitol synthesis in brown algae. Planta 233:261–273PubMedGoogle Scholar
  77. Rueness J, Kornfeldt RA (1992) Ecotypic differentiation in salinity responses of Ceramium strictum (Rhodophyta) from Scandinavian waters. Sarsia 77:207–212Google Scholar
  78. Russell G (1985) Recent evolutionary changes in the algae of the Baltic Sea. Br Phycol J 20:87–104Google Scholar
  79. Russell G (1987) Salinity and seaweed vegetation. In: Crawford RMM (ed) The physiological ecology of amphibious and intertidal plants. Blackwell, Oxford, pp 35–52Google Scholar
  80. Ryther JH, Menzel DW, Corwin N (1967) Influence of the Amazon river outflow on the ecology of the western tropical Atlantic. I. Hydrography and nutrient chemistry. J Mar Res 25:69–83Google Scholar
  81. Satoh K, Smith CM, Fork DC (1983) Effects of salinity on primary processes of photosynthesis in the red alga Porphyra perforata. Plant Physiol 73:643–647PubMedCentralPubMedGoogle Scholar
  82. Schramm W, Nienhuis PH (1996) Marine benthic vegetation. Recent changes and the effects of eutrophication. Ecol Stud Anal Synth 123:1–470Google Scholar
  83. Smith CM, Satoh K, Fork DC (1986) The effects of osmotic tissue dehydration and air drying in morphology and energy transfer in two species of Porphyra. Plant Physiol 80:843–847PubMedCentralPubMedGoogle Scholar
  84. Sung MS, Hsu YT, Hsu YT, Wu TM, Lee TM (2009) Hypersalinity and hydrogen peroxide upregulation of gene expression of antioxidant enzymes in Ulva fasciata against oxidative stress. Mar Biotechnol 11:199–209PubMedGoogle Scholar
  85. Tazawa M, Shimmen T, Mimura T (1987) Membrane control in the Characeae. Annu Rev Plant Physiol 38:95–117Google Scholar
  86. Thomas DN, Kirst GO (1991) Salt tolerance of Ectocarpus siliculosus (Dillw.) Lyngb.: comparison of gametophytes, sporophytes and isolates of different geographic origin. Bot Acta 104:26–36Google Scholar
  87. Thomas DN, Collins JC, Russell G (1988) Interactive effects of temperature and salinity upon net photosynthesis of Cladophora glomerata and C. rupestris. Bot Mar 31:73–77Google Scholar
  88. Törnroth-Horsefield S, Wang Y, Hedfalk K, Johanson U, Karlsson M, Tajkhorshid E, Neutze R, Kjellbom P (2006) Structural mechanism of plant aquaporin gating. Nature 439:688–694PubMedGoogle Scholar
  89. Turesson G (1922) The genotypical response of the plant species to the habitat. Hereditas 3:211–350Google Scholar
  90. Verret F, Wheeler G, Taylor AR, Farnham G, Brownlee C (2010) Calcium channels in photosynthetic eukaryotes: implications for evolution of calcium-based signalling. New Phytol 187:23–43PubMedGoogle Scholar
  91. Wendler S, Zimmermann U, Bentrup FW (1983) Relationship between cell turgor pressure, electrical membrane potential, and chloride efflux in Acetabularia mediterranea. J Membr Biol 72:75–84Google Scholar
  92. Wiangnon K, Raksajit W, Incharoensakdi A (2007) Presence of a Na+-stimulated P-type ATPase in the plasma membrane of the alkaliphilic halotolerant cyanobacterium Aphanothece halophytica. FEMS Microbiol Lett 270:139–145PubMedGoogle Scholar
  93. Wickberg B (1958) Synthesis of 1-glyceritol D-galactopyranosides. Acta Chem Scand 12:1187–1201Google Scholar
  94. Wiencke C (1982) Effect of osmotic stress on thylakoid fine structure in Porphyra umbilicalis. Protoplasma 111:215–220Google Scholar
  95. Wiencke C, Läuchli A (1980) Growth, cell volume, and fine structure of Porphyra umbilicalis in relation to osmotic tolerance. Planta 150:303–311PubMedGoogle Scholar
  96. Wiencke C, Läuchli A (1983) Tonoplast fine structure and osmotic regulation in Porphyra umbilicalis. Planta 159:342–346PubMedGoogle Scholar
  97. Wiencke C, Stelzer R, Läuchli A (1983) Ion compartmentation in Porphyra umbilicalis determined by electron-probe X-ray microanalysis. Planta 159:336–341PubMedGoogle Scholar
  98. Wiltens J, Schreiber U, Vidaver W (1978) Chlorophyll fluorescence induction: an indicator of photosynthetic activity in marine algae undergoing desiccation. Can J Bot 56:2787–2794Google Scholar
  99. Wright PJ, Clayton MN, Chudek JA, Foster R, Reed RH (1987) Low molecular weight carbohydrates in marine brown algae from the southern hemisphere: the occurrence of altritol in Bifurcariopsis capensis, Hormosira banksii, Notheia anomala and Xiphophora chondrophylla. Phycologia 26:429–434Google Scholar
  100. Wright DG, Pawlowicz R, McDougall TJ, Feistel R, Marion GM (2010) Absolute salinity, “density salinity” and the reference-composition salinity scale: present and future use in the seawater standard TEOS-10. Ocean Sci Discuss 7:1559–1625Google Scholar
  101. Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830PubMedGoogle Scholar
  102. Young AJ, Collins JC, Russell G (1987) Solute regulation in the euryhaline marine alga Enteromorpha prolifera (O.F. Mull) J. Ag. J Exp Bot 38:1298–1308Google Scholar
  103. Zimmermann U, Steudle E (1978) Physical aspects of water relations of plant cells. Adv Bot Res 6:45–117Google Scholar
  104. Zuccarello GC, West JA, Karsten U, King RJ (1999) Molecular relationships within Bostrychia tenuissima (Rhodomelaceae, Rhodophyta). Phycol Res 47:81–85Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Institute of Biological Sciences, Applied EcologyUniversity of RostockRostockGermany

Personalised recommendations