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Vertical heterogeneity in physiological characteristics of Ulva spp. mats

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Abstract

In eutrophic areas, green macroalgae are frequently and for long periods arranged in mats, resulting in a steep light gradient. This study investigates the effect of this gradient on physiological characteristics [tissue nitrogen content, maximal photosynthetic efficiency (F v/F m), glutathione levels and redox ratio, absorbance and absorption spectra] of the green macroalga Ulva spp. Mats were sampled during the build-up (June), stationary (July), and decomposing (September) phases of a macroalgal bloom in the Veerse Meer, a eutrophic brackish (salinity 15–20 psu) lake in the southwest Netherlands. Water samples were taken for nutrient analyses. At all three sampling dates, the mats were composed almost entirely of Ulva spp.; in September the mats were in decay and covered with silt and epiphytes. In June and July, total dissolved inorganic nitrogen concentration (DIN) of the water within the mat was significantly higher than outside the mat. Pronounced vertical differences were found in tissue N, F v/F m values, total glutathione levels, glutathione redox ratios, and absorbance. In June and July, tissue N decreased from over 2.2% dry weight (DW; N-sufficient) in the bottom layers to around 1% DW (minimum level for survival) in the top layers. Wide-band absorption increased with depth in the mat and throughout the season, probably due to higher Chl a and b and lutein contents. The shape of the absorption spectrum was similar for all layers. The absorption of the silt/epiphyte film on the top Ulva layer was highest; its absorption spectrum (high absorption in the 500–560 nm range) indicates that the film on the top layers of the macroalgal mats mainly consisted of diatoms. In June, F v/F m and the glutathione redox ratio of the algae increased with depth in the layer, while total glutathione decreased. Low F v/F m values in the bottom and middle layers in September reflect the bad condition of the algae; the mats were largely decaying. It is concluded that multiple growth-limiting gradients occur in macroalgal mats: upper layers suffer from nitrogen limitation and photoinhibition while bottom layers are light limited. The algae in the mat acclimatize to low light conditions by increasing their absorption through increased pigment contents and by higher photosynthetic efficiency during the build-up and stationary period. This study qualifies the glutathione redox ratio as a promising candidate for stress indicator in macroalgae and provides suggestions for its further development.

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References

  • Agrawal SB (1992) Effects of supplemental U.V.-B radiation on photosynthetic pigment, protein and glutathione contents in green algae. Environ Exp Bot 32:137–143

    CAS  Google Scholar 

  • Alscher RG (1989) Biosynthesis and antioxidant function of glutathione in plants. Physiol Plant 77:457–464

    CAS  Google Scholar 

  • Baker NR, Bowyer JR (eds) (1994) Photoinhibition of photosynthesis: from the molecular mechanisms to the field. BIOS Scientific, Oxford

    Google Scholar 

  • Barranguet C, Herman PMJ, Sinke JJ (1998) Microphytobenthos biomass and community composition studied by pigment biomarkers. Importance and fate in the carbon cycle of a tidal flat. J Sea Res 38:59–70

    Article  Google Scholar 

  • Bartoli M, Cattadori M, Giordani G, Viaroli P (1996) Benthic oxygen respiration, ammonium and phosphorus regeneration in surficial sediments of the Sacca di Goro (northern Italy) and two French coastal lagoons: a comparative study. Hydrobiologia 329:143–159

    CAS  Google Scholar 

  • Bischof K, Peralta G, Kräbs G, Poll WH van de, Pérez-Lloréns JL, Breeman AM (2002) Effects of solar UV-B radiation on canopy structure of Ulva communities from southern Spain. J Exp Bot 53:2411–2421

    Article  CAS  PubMed  Google Scholar 

  • Box GEP, Cox DR (1964) An analysis of transformations. J R Stat Soc B 26:211–243

    Google Scholar 

  • Brown VB, Davies SA, Synnot RN (1990) Long-term monitoring of the effects of sewage effluent on intertidal macroalgae. Bot Mar 33:85–98

    Google Scholar 

  • Brüggemann W, Beyel V, Brodka M, Poth H, Weil M, Stockhaus J (1999) Antioxidants and antioxidative enzymes in wild-type and transgenic Lycopersicon genotypes of different chilling tolerance. Plant Sci 140:145–154

    Article  Google Scholar 

  • Davey WM, Dekempeneer E, Keulemans J (2003) Rocket-powered high-performance liquid chromatographic analysis of plant ascorbate and glutathione. Anal Biochem 316:74–81

    Article  CAS  PubMed  Google Scholar 

  • Davison IR, Pearson GA (1996) Stress tolerance in intertidal seaweeds. J Phycol 32:197–211

    Google Scholar 

  • De Vos CHR, Vonk MJ, Vooijs R, Schat H (1992) Glutathione depletion due to copper induced phytochelatin synthesis in Silene cucubalis. Plant Physiol 98:853–858

    Google Scholar 

  • Duarte CM (1995) Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia 41:87–112

    Google Scholar 

  • Fahey RC, Newton GL (1987) Determination of low-molecular weight thiols using monobromobimane fluorescent labeling and high-performance liquid chromatography. Methods Enzymol 143:85–101

    CAS  PubMed  Google Scholar 

  • Fork DC, Larkum AWD (1989) Light harvesting in the green alga Ostreobium sp., a coral symbiont adapted to extreme shade. Mar Biol 103:381–385

    Google Scholar 

  • Fujita RM, Wheeler PA, Edwards RL (1989) Assessment of macroalgal nitrogen limitation in a seasonal upwelling region. Mar Ecol Prog Ser 53:293–303

    Google Scholar 

  • Geertz-Hansen O, Sand-Jensen K (1992) Growth rates and photon yield of growth in natural populations of a marine macroalga Ulva lactuca. Mar Ecol Prog Ser 81:179–183

    Google Scholar 

  • Hanelt D, Huppertz K, Nultsch W (1992) Photoinhibition of photosynthesis and its recovery in red algae. Bot Acta 105:278–284

    Google Scholar 

  • Hanelt D, Huppertz K, Nultsch W (1993) Daily course of photosynthesis and photoinhibition in marine macroalgae investigated in the laboratory and field. Mar Ecol Prog Ser 97:31–71

    Google Scholar 

  • Hanisak MD (1993) Nitrogen release from decomposing seaweeds: species and temperature effects. J Appl Phycol 5:175–181

    Google Scholar 

  • Henley WJ, Ramus J (1989a) Optimization of pigment content and the limits of photoacclimation for Ulva rotundata (Chlorophyta). Mar Biol 103:267–274

    CAS  Google Scholar 

  • Henley WJ, Ramus J (1989b) Photoacclimation of Ulva rotundata (Chlorophyta) under natural irradiance. Mar Biol 103:261–266

    Google Scholar 

  • Henley WJ, Levavasseur G, Franklin LA, Lindley ST, Ramus J, Osmond CB (1991a) Diurnal responses of photosynthesis and fluorescence in Ulva rotundata acclimated to sun and shade in outdoor culture. Mar Ecol Prog Ser 75:19–28

    Google Scholar 

  • Henley WJ, Levavasseur G, Franklin LA, Osmond CB, Ramus J (1991b) Photoacclimation and photoinhibition in Ulva rotundata as influenced by nitrogen availability. Planta 184:235–243

    CAS  Google Scholar 

  • Huisman J (1997) The struggle for light. PhD thesis, University of Groningen, The Netherlands

  • Ishikawa T, Sies H (1988) Glutathione as an antioxidant: toxicological aspects. In: Dolphin D, Poulson R (eds) Glutathione, part B. Wiley, New York, pp 85–109

  • Kageyama A, Yokohama Y, Shimura S, Ikawa T (1977) An efficient excitation energy transfer from a carotenoid, siphonaxanthin to chlorophyll a observed in a deep-water species of chlorophycean seaweed. Plant Cell Physiol 18:477–480

    CAS  Google Scholar 

  • Kocsy G, Galiba G, Brunold C (2001) Role of glutathione in adaptation and signalling during chilling and cold acclimation in plants. Physiol Plant 113:158–164

    CAS  Google Scholar 

  • Krause-Jensen D, McGlathery KJ, Rysgaard S, Christensen PB (1996) Production within dense mats of the filamentous macroalga Chaetomorpha linum in relation to light and nutrient availability. Mar Ecol Prog Ser 134:207–216

    Google Scholar 

  • Krause-Jensen D, Christensen PB, Rysgaard S (1999) Oxygen and nutrient dynamics within mats of the filamentous macroalga Chaetomorpha linum. Estuaries 22:31–38

    CAS  Google Scholar 

  • Kristensen E (1994) Decomposition of macroalgae, vascular plants and sediment detritus in seawater: use of stepwise thermogravimetry. Biogeochemistry 26:1–24

    Google Scholar 

  • Lapointe BE, Tenore KR (1981) Experimental outdoor studies with Ulva fasciata Delile I. Interactions of light and nitrogen on nutrient uptake, growth, and biochemical composition. J Exp Mar Biol Ecol 53:135–152

    CAS  Google Scholar 

  • Lavery PS, McComb AJ (1991a) Macroalgal-sediment nutrient interactions and their importance to macroalgal nutrition in a eutrophic lagoon. Estuar Coast Shelf Sci 32:281–295

    Google Scholar 

  • Lavery PS, McComb AJ (1991b) The nutritional eco-physiology of Chaetomorpha linum and Ulva rigida in Peel Inlet, Western Australia. Bot Mar 34:251–260

    CAS  Google Scholar 

  • Lavery PS, Lukatelich RJ, McComb AJ (1991) Changes in the biomass and species composition of macroalgae in a eutrophic estuary. Estuar Coast Shelf Sci 33:1–22

    Google Scholar 

  • Lowthion D, Soulsby PG, Houston M (1985) Investigation of a eutrophic tidal basin: part 1—factors affecting the distribution and biomass of macroalgae. Mar Environ Res 15:263–284

    Google Scholar 

  • Magnusson G (1997) Diurnal measurements of Fv/Fm used to improve productivity estimates in macroalgae. Mar Biol 130:203–208

    Article  Google Scholar 

  • Malta E (2000) Macroalgal mats in a eutrophic lagoon: dynamics and control mechanisms. PhD thesis, University of Nijmegen, The Netherlands

    Google Scholar 

  • Malta E, Verschuure JM (1997) Effects of environmental variables on between-year variation of Ulva growth and biomass in a eutrophic brackish lake. J Sea Res 38:71–84

    Article  Google Scholar 

  • Malta E, Draisma SGA, Kamermans P (1999) Free-floating Ulva in the southwest Netherlands: species or morphotypes? A morphological, molecular and ecological comparison. Eur J Phycol 34:443–454

    Article  Google Scholar 

  • Malta E, Verschuure JM, Nienhuis PH (2002) Regulation of spatial and seasonal variation of macroalgal biomass in a brackish, eutrophic lake. Helgol Mar Res 56:211–220

    Article  Google Scholar 

  • Markager S, Sand-Jensen K (1994) The physiology and ecology of light-growth relationship in macroalgae. In: Round FE, Chapman DE (eds) Progress in phycological research, vol 10. Biopress, Bristol, pp 209–298

  • McGlathery KJ, Krause-Jensen D, Rysgaard S, Christensen PB (1997) Patterns of ammonium uptake within dense mats of the filamentous macroalga Chaetomorpha linum. Aquat Bot 59:99–115

    Article  Google Scholar 

  • Mercado JM, Jiménez C, Niell FX, Figueroa FL (1996) Comparison of methods for measuring light absorption by algae and their application to the estimation of the package effect. Sci Mar 60:39–45

    Google Scholar 

  • Meuwly P, Rauser WE (1992) Alteration of thiol pools in roots and shoots of maize seedlings exposed to cadmium. Adaptation and developmental cost. Plant Physiol 99:8–15

    CAS  Google Scholar 

  • Nakano T, Watanabe M, Sato M, Takeuchi M (1995) Characterization of catalase from the seaweed Porphyra yezoensis. Plant Sci 104:127–133

    Article  CAS  Google Scholar 

  • Naldi M, Wheeler PA (1999) Changes in nitrogen pools in Ulva fenestrata (Chlorophyta) and Gracilaria pacifica (Rhodophyta) under nitrate and ammonium enrichment. J Phycol 35:70–77

    Article  CAS  Google Scholar 

  • Nieuwenhuize J, Maas YEM, Middelburg JJ (1994) Rapid analysis of organic carbon and nitrogen in particulate materials. Mar Chem 45:217–224

    CAS  Google Scholar 

  • Pedersen MF (1994) Vaekst og naeringsdynamik hos marine planter. PhD dissertation, University of Copenhagen, Denmark

  • Ramus J (1983) A physiological test of the theory of complementary chromatic adaptation II. Brown, green and red seaweeds. J Phycol 19:173–178

    CAS  Google Scholar 

  • Rijstenbil JW, Wijnholds JA (1996) HPLC analysis of nonprotein thiols in planktonic diatoms: pool size, redox state and response to copper and cadmium exposure. Mar Biol 127:45–54

    CAS  Google Scholar 

  • Rijstenbil JW, Haritonidis S, Malea P, Seferlis M, Wijnholds JA (1998) Thiol pools and glutathione redox ratios as possible indicators of copper toxicity in the green macroalgae Enteromorpha spp. from the Scheldt estuary (SW Netherlands, Belgium) and Thermaikos Gulf (Greece, N Aegean sea). Hydrobiologia 385:171–181

    CAS  Google Scholar 

  • Rüegsegger A, Brunold C (1992) Effect of cadmium on γ-glutamylcysteine synthesis in maize seedlings. Plant Physiol 99:428–433

    Google Scholar 

  • Ruiz JM, Blumwald E (2002) Salinity-induced glutathione synthesis in Brassica napus. Planta 214:965–969

    Article  CAS  PubMed  Google Scholar 

  • Salles S, Aguilera J, Figueroa FL (1996) Light field in algal canopies: changes in spectral light ratios and growth of Porphyra leucostica Thur. in le Jol. Sci Mar 60:29–38

    Google Scholar 

  • Schramm W, Nienhuis PH (eds) (1996) Marine benthic vegetation. Recent changes and the effect of eutrophication. (Ecological studies, vol 123) Springer, Berlin Heidelberg New York

  • Sfriso A, Pavoni B, Marcomini A, Orio AA (1992) Macroalgae, nutrient cycles, and pollutants in the Lagoon of Venice. Estuaries 15:517–528

    CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. Freeman, New York

  • Soulsby PG, Lowthion D, Houston M, Montgomery HAC (1985) The role of sewage effluent in the accumulation of macroalgal mats on intertidal mudflats in two basins in southern England. Neth J Sea Res 19:257–263

    Google Scholar 

  • Spjøtvoll E, Stoline MR (1973) An extension of the T-method of multiple comparison to include the cases with unequal sample sizes. J Am Stat Assoc 68:976–978

    Google Scholar 

  • StatSoft (1997) STATISTICA for Windows (Computer program manual). StatSoft, Tulsa, Okla.

  • Thybo-Christensen M, Rasmussen MB, Blackburn H (1993) Nutrient fluxes and growth of Cladophora sericea in a shallow Danish bay. Mar Ecol Prog Ser 100:273–281

    Google Scholar 

  • Vergara JJ, Pérez-Lloréns JL, Peralta G, Hernández I, Niell FX (1997) Seasonal variation of photosynthetic performance and light attenuation in Ulva canopies from Palmones river estuary. J Phycol 33:773–779

    Google Scholar 

  • Vergara JJ, Sebastián M, Pérez-Lloréns JL, Hernández I (1998) Photoacclimation of Ulva rigida and U. rotundata (Chlorophyta) arranged in canopies. Mar Ecol Prog Ser 165:283–292

    Google Scholar 

  • Wheeler PA, Bjornsater BR (1992) Seasonal fluctuations in tissue nitrogen, phosphorus, and N:P for 5 macroalgal species common to the Pacific northwest coast. J Phycol 28:1–6

    CAS  Google Scholar 

  • Wright SW, Jeffrey SW, Mantoura RFC, Llewellyn CA, Bjørnland T, Repeta D, Welschmeyer N (1991) Improved HPLC method for the analysis of chlorophylls and carotenoids from marine phytoplankton. Mar Ecol Prog Ser 77:183–196

    CAS  Google Scholar 

  • Yokohama Y (1981) Distribution of the green light-absorbing pigments siphonaxanthin and siphonein in marine green algae. Bot Mar 24:637–640

    CAS  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Drs. P.H. Nienhuis, P. Kamermans, and two anonymous referees for their comments on earlier drafts of this manuscript. Thanks are due to J. Nieuwenhuize, Y. Maas, and P. van Breugel for carrying out the C:N analyses and to J. Sinke for carrying out the pigments analyses. Anita Wijnholds and Tanja Poortvliet kindly assisted with the glutathione analysis. Jan Peene, Ko Verschuure, and Monique de Bie provided invaluable assistance in collecting the algae. This study is carried out in the framework of the EUMAC project, which is funded by the Environment and Climate Programme of the European Commission (no. EV5V-CT93-0290). This is publication no. 3158 of the NIOO-KNAW, Netherlands Institute of Ecology.

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  1. E. Malta

    Present address: Área de Ecología, Facultad de Ciencias del Mar, Universidad de Cádiz, 11510, Puerto Real, Cádiz, Spain

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  1. Centre for Estuarine and Coastal Ecology, Netherlands Institute of Ecology, P.O. Box 140, 4400, AC Yerseke, The Netherlands

    E. Malta, J. W. Rijstenbil, P. E. M. Brouwer & J. C. Kromkamp

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Communicated by S.A. Poulet, Roscoff

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Malta, E., Rijstenbil, J.W., Brouwer, P.E.M. et al. Vertical heterogeneity in physiological characteristics of Ulva spp. mats. Marine Biology 143, 1029–1038 (2003). https://doi.org/10.1007/s00227-003-1134-4

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