ALGAE

The Korean Society of Phycology (한국조류학회(藻類))
권호 표지
DOI QR코드

DOI QR Code

Physiological responses to salt stress by native and introduced red algae in New Zealand

  • Gambichler, Vanessa (Institute of Biological Sciences, Applied Ecology and Phycology, University of Rostock) ;
  • Zuccarello, Giuseppe C. (School of Biological Sciences, Victoria University of Wellington) ;
  • Karsten, Ulf (Institute of Biological Sciences, Applied Ecology and Phycology, University of Rostock)
  • Received : 2021.03.15
  • Accepted : 2021.06.10
  • Published : 2021.06.15
Download PDF
⟨ Previous Next ⟩

Abstract

Intertidal macroalgae are regularly exposed to hypo- or hypersaline conditions which are stressful. However, red algae in New Zealand are generally poorly studied in terms of salinity tolerance. Consequently, two native (Bostrychia arbuscula W. H. Harvey [Ceramiales], Champia novae-zelandiae [J. D. Hooker & Harvey] Harvey [Rhodymeniales]) and one introduced red algal taxon (Schizymenia spp. J. Agardh [Nemastomatales]) were exposed for 5 days in a controlled salt stress experiment to investigate photosynthetic activity and osmotic acclimation. The photosynthetic activity of B. arbuscula was not affected by salinity, as reflected in an almost unchanged maximum quantum yield (Fv/Fm). In contrast, the Fv/Fm of C. novae-zelandiae and Schizymenia spp. strongly decreased under hypo- and hypersaline conditions. Treatment with different salinities led to an increase of the total organic osmolyte concentrations with rising salt stress in B. arbuscula and Schizymenia spp. In C. novae-zelandiae the highest organic osmolyte concentrations were recorded at SA 38, followed by declining amounts with further hypersaline exposure. In B. arbuscula, sorbitol was the main organic osmolyte, while the other taxa contained floridoside. The data presented indicate that all three red algal species conspicuously differ in their salt tolerance. The upper intertidal B. arbuscula exhibited a wide salinity tolerance as reflected by unaffected photosynthetic parameters and strong sorbitol accumulation under increasing salinities, and hence can be characterized as euryhaline. In contrast, the introduced Schizymenia spp. and native C. novae-zelandiae, which preferentially occur in the mid-intertidal, showed a narrower salinity tolerance. The species-specific responses reflect their respective vertical positions in the intertidal zone.

Keywords

Acknowledgement

Vanessa Gambichler thanks the DAAD for a PROMOS Scholarship supporting her research stay in New Zealand. We thank Maren Preuss for her help collecting samples for this study, and all her intellectual input, as well as Ken Ryan, John van der Sman and Neville Higgison for their technical support. We also thank Julianne Müller for her support with the HPLC.

References

  1. Adams, N. M. 1994. Seaweeds of New Zealand: an illustrated guide. Canterbury University Press, Christchurch, NZ, 360 pp.
  2. Angell, A. R., Mata, L., de Nys, R. & Paul, N. A. 2015. Indirect and direct effects of salinity on the quantity and quality of total amino acids in Ulva ohnoi (Chlorophyta). J. Phycol. 51:536-545. https://doi.org/10.1111/jpy.12300
  3. Ben-Amotz, A. & Avron, M. 1983. Accumulation of metabolites by halotolerant algae and its industrial potential. Annu. Rev. Microbiol. 37:95-119. https://doi.org/10.1146/annurev.mi.37.100183.000523
  4. Bischof, K., Gomez, I., Molis, M., Hanelt, D., Karsten, U., Luder, U., Roleda, M. Y., Zacher, K. & Wiencke, C. 2006. Ultraviolet radiation shapes seaweed communities. Rev. Environ. Sci. Biotechnol. 5:141-166. https://doi.org/10.1007/s11157-006-0002-3
  5. Bollen, M., Pilditch, C. A., Battershill, C. N. & Bischof, K. 2016. Salinity and temperature tolerance of the invasive alga Undaria pinnatifida and native New Zealand kelps: implications for competition. Mar. Biol. 163:194. https://doi.org/10.1007/s00227-016-2954-3
  6. Broderick, M. E. & Dawes, C. J. 1998. Seasonal photosynthetic and respiratory responses of the red alga Bostrychia tenella (Ceramiales, Rhodophyta) from a salt marsh and mangal. Phycologia 37:92-99. https://doi.org/10.2216/i0031-8884-37-2-92.1
  7. Brown, M. T. 1987. Effects of desiccation on photosynthesis of intertidal algae from a southern New Zealand shore. Bot. Mar. 30:121-127. https://doi.org/10.1515/botm.1987.30.2.121
  8. D'Archino, R., Nelson, W., Yang, M. Y. & Kim, M. S. 2015. New record of Hypnea flexicaulis in New Zealand and description of Calliblepharis psammophilus sp. nov. Bot. Mar. 58:485-497. https://doi.org/10.1515/bot-2015-0053
  9. D'Archino, R., Nelson, W. A. & Zuccarello, G. C. 2007. Invasive marine red alga introduced to New Zealand waters: first record of Grateloupia turuturu (Halymeniaceae, Rhodophyta). N. Z. J. Mar. Freshw. Res. 41:35-42. https://doi.org/10.1080/00288330709509894
  10. D'Archino, R. & Zuccarello, G. C. 2014. First record of Schizymenia apoda (Schizymeniaceae, Rhodophyta) in New Zealand. N. Z. J. Mar. Freshw. Res. 48:155-162. https://doi.org/10.1080/00288330.2013.847849
  11. D'Archino, R. & Zuccarello, G. C. 2020. Schizymenia dubyi (Chauvin ex Duby) J. Agardh collected in Whairepo Lagoon, Wellington Harbour. N. Z. Mar. Exot. Species Note 113:5.
  12. D'Archino, R. & Zuccarello, G. C. 2021. Two red macroalgae newly introduced into New Zealand: Pachymeniopsis lanceolata (K. Okamura) Y. Yamada ex S. Kawabata and Fushitsunagia catenata Filloramo et G. W. Saunders. Bot. Mar. Advanced online publication. https://doi.org/10.1515/bot-2021-0013.
  13. Davison, I. R. & Pearson, G. A. 1996. Stress tolerance in intertidal seaweeds. J. Phycol. 32:197-211. https://doi.org/10.1111/j.0022-3646.1996.00197.x
  14. Diehl, N., Michalik, D., Zuccarello, G. C. & Karsten, U. 2019. Stress metabolite pattern in the eulittoral red alga Pyropia plicata (Bangiales) in New Zealand: mycosporinelike amino acids and heterosides. J. Exp. Mar. Biol. Ecol. 510:23-30. https://doi.org/10.1016/j.jembe.2018.10.002
  15. Eggert, A. & Karsten, U. 2010. Low molecular weight carbohydrates in red algae: an ecophysiological and biochemical perspective. In Seckbach, J. & Chapman, D. J. (Eds.) Red Algae in the Genomic Age. Vol. 13. Cellular Origin, Life in Extreme Habitats and Astrobiology. Springer, Dordrecht, pp. 445-456.
  16. Eggert, A., Nitschke, U., West, J. A., Michalik, D. & Karsten, U. 2007. Acclimation of the intertidal red alga Bangiopsis subsimplex (Stylonematophyceae) to salinity changes. J. Exp. Mar. Biol. Ecol. 343:176-186. https://doi.org/10.1016/j.jembe.2006.11.015
  17. Fredersdorf, J., Muller, R., Becker, S., Wiencke, C. & Bischof, K. 2009. Interactive effects of radiation, temperature and salinity on different life history stages of the Arctic kelp Alaria esculenta (Phaeophyceae). Oecologia 160:483-492. https://doi.org/10.1007/s00442-009-1326-9
  18. Gabriel, D., Schils, T., Parente, M. I., Draisma, S. G. A., Neto, A. I. & Fredericq, S. 2011. Taxonomic studies in the Schizymeniaceae (Nemastomatales, Rhodophyta): on the identity of Schizymenia sp. in the Azores and the generic placement of Nemastoma confusum. Phycologia 50:109-121. https://doi.org/10.2216/09-67.1
  19. Gambichler, V., Zuccarello, G. C. & Karsten, U. 2021. Seasonal changes in stress metabolites of native and introduced red algae in New Zealand. J. Appl. Phycol. 33:1157-1170. https://doi.org/10.1007/s10811-020-02365-0
  20. Garbary, D. J., D'Archino, R., Flack, B., Hepburn, C. D., Nelson, W. A., Pritchard, D. & Sutherland, J. E. 2020. First record of Bonnemaisonia hamifera (Bonnemaisoniales, Rhodophyta) in the South Pacific, from the South Island of New Zealand. N. Z. J. Mar. Freshw. Res. 54:167-176. https://doi.org/10.1080/00288330.2019.1661260
  21. Guiry, M. D. & Guiry, G. M. 2020. AlgaeBase: World-wide electronic publication, National University of Ireland, Galway. Available from: https://www.algaebase.org. Accessed Jan 20, 2020.
  22. Gunnarsson, K., Russell, S. & Brodie, J. 2020. Schizymenia jonssonii sp. nov. (Nemastomatales, Rhodophyta): a relict or an introduction into the North Atlantic after the last glacial maximum? J. Phycol. 56:324-333. https://doi.org/10.1111/jpy.12957
  23. Hurd, C. L., Nelson, W. A., Falshaw, R. & Neill, K. F. 2004. History, current status and future of marine macroalgal research in New Zealand: taxonomy, ecology, physiology and human uses. Phycol. Res. 52:80-106. https://doi.org/10.1111/j.1440-1835.2004.tb00318.x
  24. Hutchinson, G. E. 1957. Concluding remarks. Cold Spring Harb. Symp. Quant. Biol. 22:415-427. https://doi.org/10.1101/SQB.1957.022.01.039
  25. Karsten, U. 2012. Seaweed acclimation to salinity and desiccation stress. In Wiencke, C. & Bischof, K. (Eds.) Seaweed Biology: Novel Insights into Ecophysiology, Ecology and Utilization. Vol. 219. Springer, Berlin, pp. 87-107.
  26. Karsten, U., Barrow, K. D., Nixdorf, O. & King, R. J. 1996a. The compability with enzyme activity of unusual organic osmolytes from mangrove red algae. Aust. J. Plant Physiol. 23:577-582. https://doi.org/10.1071/PP9960577
  27. Karsten, U., Barrow, K. D., Nixdorf, O., West, J. A. & King, R. J. 1997. Characterization of mannitol metabolism in the mangrove red alga Caloglossa leprieurii (Montagne) J.Agardh. Planta 201:173-178.
  28. Karsten, U., Bock, C. & West, J. A. 1995. Low molecular weight carbohydrate patterns in geographically different isolates of the eulittoral red alga Bostrychia tenuissima from Australia. Bot. Acta 108:321-326. https://doi.org/10.1111/j.1438-8677.1995.tb00501.x
  29. Karsten, U., Gors, S., Eggert, A. & West, J. A. 2007. Trehalose, digeneaside, and floridoside in the Florideophyceae (Rhodophyta): a reevaluation of its chemotaxonomic value. Phycologia 46:143-150. https://doi.org/10.2216/06-29.1
  30. Karsten, U. & Kirst, G. O. 1989. Incomplete turgor pressure regulation in the "terrestial" red alga, Bostrychia scorpioides (Huds.) Mont. Plant Sci. 61:29-36. https://doi.org/10.1016/0168-9452(89)90115-5
  31. Karsten, U., Koch, S., West, J. A. & Kirst, G. O. 1996b. Physiological responses of the eulittoral macroalga Stictosiphonia hookeri (Rhodomelaceae, Rhodophyta) from Argentina and Chile: salinity, light and temperature acclimation. Eur. J. Phycol. 31:361-368. https://doi.org/10.1080/09670269600651591
  32. Karsten, U., Michalik, D., Michalik, M. & West, J. A. 2005. A new unusual low molecular weight carbohydrate in the red algal genus Hypoglossum (Delesseriaceae, Ceramiales) and its possible function as an osmolyte. Planta 222:319-326. https://doi.org/10.1007/s00425-005-1527-3
  33. Kirst, G. O. 1990. Salinity tolerance of eukaryotic marine algae. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41:21-53. https://doi.org/10.1146/annurev.pp.41.060190.000321
  34. Kirst, G. O. & Bisson, M. A. 1979. Regulation of turgor pressure in marine algae: ions and low-molecular-weight organic compounds. Aust. J. Plant Physiol. 6:539-556.
  35. Lamare, M. D., Lesser, M. P., Barker, M. F., Barry, T. M. & Schimanski, K. B. 2004. Variation in sunscreen compounds (mycosporine-like amino acids) for marine species along a gradient of ultraviolet radiation transmission within doubtful sound, New Zealand. N. Z. J. Mar. Freshw. Res. 38:775-793. https://doi.org/10.1080/00288330.2004.9517277
  36. Luning, K. 1990. Seaweeds: Their environment, biogeography, and ecophysiology. John Wiley & Sons, New York, 527 pp.
  37. Lv, Y., Sun, P., Zhang, Y., Xuan, W., Xu, N. & Sun, X. 2019. Response of trehalose, its degrading enzyme, sucrose, and floridoside/isofloridoside under abiotic stresses in Gracilariopsis lemaneiformis (Rhodophyta). J. Appl. Phycol. 31:3861-3869. https://doi.org/10.1007/s10811-019-01869-8
  38. Marcelino, V. R. & Verbruggen, H. 2015. Ecological niche models of invasive seaweeds. J. Phycol. 51:606-620. https://doi.org/10.1111/jpy.12322
  39. Maxwell, K. & Johnson, G. N. 2000. Chlorophyll fluorescence: a practical guide. J. Exp. Bot. 51:659-668. https://doi.org/10.1093/jexbot/51.345.659
  40. Muangmai, N., Preuss, M. & Zuccarello, G. C. 2015. Comparative physiological studies on the growth of cryptic species of Bostrychia intricata (Rhodomelaceae, Rhodophyta) in various salinity and temperature conditions. Phycol. Res. 63:300-306. https://doi.org/10.1111/pre.12101
  41. Nelson, W. A. 1994. Distribution of macroalgae in New Zealand: an archipelago in space and time. Bot. Mar. 37:221-233. https://doi.org/10.1515/botm.1994.37.3.221
  42. Nelson, W. A. 2013. New Zealand seaweeds: an illustrated guide. Te Papa Press, Wellington, 328 pp.
  43. Nelson, W. A., Dalen, J. & Neill, K. F. 2013. Insights from natural history collections: analysing the New Zealand macroalgal flora using herbarium data. PhytoKeys 30:1-21. https://doi.org/10.3897/phytokeys.30.5889
  44. Ramirez, M. E., Nunez, J. D., Ocampo, E. H., Matula, C. V., Suzuki, M., Hashimoto, T. & Cledon, M. 2012. Schizymenia dubyi (Rhodophyta, Schizymeniaceae), a new introduced species in Argentina. N. Z. J. Bot 50:51-58. https://doi.org/10.1080/0028825X.2011.642887
  45. Ritchie, R. J. 1988. The ionic relations of Ulva lactuca. J. Plant Physiol. 133:183-192. https://doi.org/10.1016/S0176-1617(88)80135-4
  46. Russell, G. 1987. Salinity and seaweed vegetation. In Crawford, R. M. M. (Ed.) Plant Life in Aquatic and Amphibious Habitats. Blackwell, Oxford, pp. 35-52.
  47. Saunders, G. W., Birch, T. C. & Dixon, K. R. 2015. A DNA barcode survey of Schizymenia (Nemastomatales, Rhodophyta) in Australia and British Columbia reveals overlooked diversity including S. tenuis sp. nov. and Predaea borealis sp. nov. Botany 93:859-871. https://doi.org/10.1139/cjb-2015-0122
  48. Scherner, F., Ventura, R., Barufi, J. B. & Horta, P. A. 2013. Salinity critical threshold values for photosynthesis of two cosmopolitan seaweed species: providing baselines for potential shifts on seaweed assemblages. Mar. Environ. Res. 91:14-25. https://doi.org/10.1016/j.marenvres.2012.05.007
  49. Schweikert, K., Sutherland, J. E. S., Hurd, C. L. & Burritt, D. J. 2011. UV-B radiation induces changes in polyamine metabolism in the red seaweed Porphyra cinnamomea. Plant Growth Regul. 65:389-399. https://doi.org/10.1007/s10725-011-9614-x
  50. Shetty, P., Gitau, M. M. & Maroti, G. 2019. Salinity stress responses and adaptation mechanisms in eukaryotic green microalgae. Cells 8:1657. https://doi.org/10.3390/cells8121657
  51. Simon-Colin, C., Bessieres, M. -A. & Deslandes, E. 2002. An alternative HPLC method for the quantification of floridoside in salt-stressed cultures of the red alga Grateloupia doryphora. J. Appl. Phycol. 14:123-127. https://doi.org/10.1023/A:1019539225950
  52. Sudhir, P. & Murthy, S. D. S. 2004. Effects of salt stress on basic processes of photosynthesis. Photosynthetica 42:481-486. https://doi.org/10.1007/S11099-005-0001-6
  53. Underwood, A. J. 1997. Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge, pp. 140-197.
  54. van Ginneken, V. 2018. Some mechanism seaweeds employ to cope with salinity stress in the harsh euhaline oceanic environment. Am. J. Plant Sci. 9:1191-1211. https://doi.org/10.4236/ajps.2018.96089
  55. West, J. A. & McBride, D. L. 1999. Long-term and diurnal carpospore discharge patterns in the Ceramiaceae, Rhodomelaceae and Delesseriaceae (Rhodophyta). Hydrobiologia 398/399:101-113. https://doi.org/10.1023/A:1017025815001
  56. Wiencke, C. & Lauchili, A. 1981. Inorganic ions and floridoside as osmotic solutes in Porphyra umbilicalis. Z. Pflanzenphysiol. 103:247-258. https://doi.org/10.1016/S0044-328X(81)80157-2
  57. Yancey, P. H. 2005. Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J. Exp. Biol. 208:2819-2830. https://doi.org/10.1242/jeb.01730