Filamentous green algae, extracellular alkaline phosphatases and some features of the phosphorus cycle in ponds
##plugins.themes.ibsscustom.article.main##
Google Scholar
##plugins.themes.ibsscustom.article.details##
Abstract
Filamentous green algae (FGA) may reach high biomass and play a very important functional role in productivity and nutrient cycling in the different water bodies. Their extracellular alkaline phosphatase activity may be an important player in the phosphorus cycle. Currently, there is intensive development of green algae in various freshwater and marine waterbodies, which creates problems for people's activities and necessitates its investigation. Filamentous green algae in four Chinese and Crimean (Russia) shallow freshwater ponds were in focus of this study. The dissolved phosphorus fraction in pond water, algal pigment level, activity and kinetic properties of alkaline phosphatase were evaluated in water column and cell membrane of filamentous green algae. Microalgal taxa were identified in the plankton samples. Species composition and density of FGA in the studied ponds were different. Two ponds had more than 50 % coverage of a water surface by FGA and its wet biomass more than 100 g∙m-2. Two others were with wet biomass less than 2 g∙m-2. In ponds with low FGA biomass, the soluble reactive phosphorus concentration exhibited considerably low level with less than 10 µg∙L-1, and the dissolved organic phosphorus comprised the largest phosphorus fraction, averaging 23.1 µg∙L-1 and ranged from 20.8 to 25.4 µg∙L-1. However, in ponds with high FGA biomass, particulate phosphorus was the major component, which contributes 45.8 % and 56.7 % of total phosphorus, respectively. Size fractionation of extracellular alkaline phosphatase activity in water column expressed spatial heterogeneity, which corresponded with biomass of FGA. The response of extracellular alkaline phosphatase activity to different phosphate concentration in water column was completely distinct from that in the cell membrane of FGA, the last of which represented the significantly inhibition effect to high phosphate concentration. The significant inhibition of alkaline phosphatase activity in cell membrane of FGA by phosphate in water may validate that FGA growth was limited by phosphorus. The contradiction between a low concentration of soluble reactive phosphorus and high FGA biomass may indicate that there was high speed nutrient cycling, probably, due to the alkaline phosphatase activity. Excreting exo-alkaline phosphatases, FGA, microalgae and bacteria accelerate phosphorus cycling through different mechanisms, and this may increase their development. In ponds with high FGA biomass, many of bacteria are responsible for regeneration of nutrients, which then consuming by FGA. Those bacteria also may concurrently restrict a microalgae development, such as unicellular Chlorophyta species. As an example, Cladophora provides habitat for different species of epibionts (bacteria and microalgae, primarily diatoms), and sustains of strong mutualistic alga-bacterium interactions. Therefore, the problem of excessive FGA growth should not be considered in isolation, but in a whole-ecosystem context.
Authors
References
Auer M.T., Canale R. Ecological studies and mathematical modeling of Cladophora in Lake Huron: 2 phosphorus uptake kinetics. Journal of Great Lakes Research, 1982, vol. 8, pp. 84–92.
Berman T. Alkaline phosphatase and phosphorus availability in Lake Kinneret. Limnology and Oceanography, 1970, vol. 15, pp. 663–674.
Brooks C., Grimm A., Shuchman R., Sayers M., Jessee N. A satellite-based multi-temporal assessment of the extent of nuisance Cladophora and related submerged aquatic vegetation for the Laurentian Great Lakes. Remote Sensing of Environment, 2015, vol. 157, pp. 58–71.
Canale R.P., Auer M.T. Ecological studies and mathematical modeling of Cladophora in Lake Huron: 7. Model verification and system response. Journal of Great Lakes Research, 1982, vol. 8, pp. 134–143.
Cao X., Song C., Zhou Y., Štrojsová A., Znachor P., Zapomělová E., Vrba J. Extracellular phosphatases produced by phytoplankton and other sources in shallow eutrophic lakes (Wuhan, China): taxon-specific versus bulk activity. Limnology, 2009, vol. 10, iss. 2, pp. 95–104.
Cao X., Song C., Zhou Y. Limitations of using extracellular alkaline phosphatase activities as a general indicator for describing P deficiency of phytoplankton in Chinese shallow lakes. Journal of Applied Phycology, 2010, vol. 22, iss. 1, pp. 33–41.
Chrost R.J., Siuda W., Halemejko G.Z. Longterm studies on alkaline phosphatase activity (APA) in a lake with fish-aquaculture in relation to lake eutrophication and phosphorus cycle. Archiv Fur Hydrobiologie, 1984, vol. 70, pp. 1–32.
Curiel D., Rismondo A., Bellemo G., Marzocchi M. Macroalgal biomass and species variations in the Lagoon of Venice (Northern Adriatic Sea, Italy): 1981–1998. Scientia Marina, 2004, vol. 68, pp. 57–67.
Dodds W.K., Gudder D.A. The ecology of Cladophora. Journal of Phycology, 1992, vol. 28, pp. 415–427.
Dondajewska R., Frankowski T., Wojak P. Changes in the vegetation of filamentous green algae in the Antoninek preliminary reservoir. Oceanological and Hydrobiological Studies, 2007, vol. 36, pp. 121–128.
El-Shahed A.M., Ibrahim H., Abd-Elnaeim M. Isolation and characterization of phosphatase enzyme from the freshwater macroalga Cladophora glomerata Kützing (Chlorophyta). Pakistan Journal of Biological Sciences, 2006, vol. 9, pp. 2456–2461.
Golterman H.L., Clymo R.S., Ohmstad M.A.M. 1978. Methods for physical and chemical analysis of Fresh waters. Oxford: Blackwell Scientific Publications, 1978, 214 p.
Gordon D.M., McComb A.J. Growth and production of the green alga Cladophora montagneana in a eutrophic Australian estuary and its interpretation using a computer program. Water Research, 1989, vol. 23, iss. 5, pp. 633–645.
Gubelit Y. I., Berezina N. A. The causes and consequences of algal blooms: the Cladophora glomerata bloom and the Neva estuary (eastern Baltic Sea). Marine Pollution Bulletin, 2010, vol. 61, iss. 4-6, pp. 183–188.
Higgins S. N., Pennuto C. M., Howell E. T., Lewis T. W., Makarewicz J. C. Urban influences on Cladophora blooms in Lake Ontario. Journal of Great Lakes Research, 2012, vol. 38, pp. 116–123.
Kwon H. K., Oh S. J., Yang H. S. Ecological significance of alkaline phosphatase activity and phosphatase-hydrolyzed phosphorus in the northern part of Gamak Bay, Korea. Marine pollution bulletin, 2011 vol. 62, iss. 11, pp. 2476–2482.
Labry C., Delmas D., Herbland A. Phytoplankton and bacterial alkaline phosphatase activities in relation to phosphate and DOP availability within the Gironde plume waters (Bay of Biscay). Journal of Experimental Marine Biology and Ecology, 2005, vol. 318, iss. 2, 213–225.
Lapointe B.E., O’Connell J. Nutrient-enhanced growth of Cladophora prolifera in Harrington Sound, Bermuda: Eutrophication of a confined, phosphorus-limited marine ecosystem. Estuarine Coastal and Shelf Science, 1989, vol. 28, pp. 347–360.
Lembi C.A. Control of nuisance algae. In: Freshwater algae of North America:Ecology and classification. New York: Academic Press, 2003, pp. 805–834.
Lin C.K. Accumulation of water soluble phosphorus and hydrolysis of polyphosphates by Cladophora glomerata (Chlorophyceae). Journal of Phycology, 1977, vol. 13, pp. 46–51.
Malkin S.Y., Guildford S.J., Hecky R.E. Modeling the growth response of Cladophora in a Laurentian Great Lake to the exotic invader Dreissena and to lake warming. Limnology and Oceanography, 2008, vol. 53, pp. 1111–1124.
Mantai K.E. The response of Cladophora glomerata to changes in soluble orthophosphate concentrations in Lake Erie. Verhandlungen des Internationalen Verein Limnologie, 1978, vol. 20, pp. 347–351.
Murphy J., Riley P. A modified single solution method of the determination of phosphate in natural waters. Analytica Chimica Acta, 1962, vol. 27, pp. 1–36.
Okada H., Watanabe Y. Effect of physical factors on the distribution of filamentous green algae in the Tama River. Limnology, 2002, vol. 3, pp. 121–126.
Painter D.S., Kamaitis G. Reduction of Cladophora biomass and tissue phosphorus in Lake Ontario, 1972-83. Canadian Journal of Fisheries and Aquatic Sciences, 1987, vol. 44, pp. 2212–2215.
Parker J.E., Maberly S.C. Biological response to lake remediation by phosphate stripping: Control of Cladophora. Freshwater Biology, 2000, vol. 44, pp. 303–309.
Planas D., Maberly S.C., Parker J.E. Phosphorus and nitrogen relationships of Cladophora glomerata in two lake basins of different trophic status. Freshwater Biology, 1996, vol. 35, pp. 609–622.
Power M.E. Hydrologic and trophic controls of seasonal algal blooms in northern California rivers. Archiv fur Hydrobiologie, 1992, vol. 125, pp. 385–410.
Prazukin A.V., Bobkova A.N., Evsigneeva I.K., Tankovska I.N., Shadrin N.V. Structure and seasonal dynamics of the phytocomponent of bioenert system marine hypersaline lakeon of cape of Chersonessus (Crimea). Morskoy Ekologicheskiyj Zhurnal, 2008, vol. 7, pp. 61–79. (in Russ.).
Ren L., Wang P., Wang C., Peng Z., Hu B., Wang R. Contribution of alkaline phosphatase to phosphorus cycling in natural riparian zones in the Wangyu River running into Lake Taihu. Desalination and Water Treatment, 2016, vol. 57, iss. 44, pp. 20970–20984.
Scott N.H., Robert E.H., Stephanie J.G. Environmental controls of Cladophora growth dynamics in eastern Lake Erie: Application of the Cladophora growth model (CGM). Journal of Great Lakes Research, 2006, vol. 32, pp. 629–644.
Scott N.H., Sairah Y.M., Todd H., Stephanie J.G., Linda C., Veronique H., Robert E.H. An ecological review of Cladophora Glomerata (Chlorophyte) in the Laurentian great lakes. Journal of Phycology, 2008, vol. 44, pp. 839–854.
Sharma K., Inglett P.W., Reddy K.R., Ogram A.V. Microscopic examination of photoautotrophic and phosphatase-producing organisms in phosphorus-limited Everglades periphyton mats. Limnology and Oceanography, 2005, vol. 50, pp. 2057–2062.
Valiela I., Mcclelland J., Hauxwell J., Behr P. J., Hersh D., Foreman K. Macroalgal blooms in shallow estuaries: Controls and ecophysiological and ecosystem consequences. Limnology and Oceanography, 1997, vol. 42, pp. 1105–1118.
Vollenweider R.A. A manual on methods for measuring primary production in aquatic environments. 2nd ed. Oxford: Blackwell Sc. Publ., 1974, 225 p. (IBP Handbook; no. 12).
Watson S. B., Miller C., Arhonditsis G., Boyer G. L., Carmichael W., Charlton M. N., Matisoff G. The re-eutrophication of Lake Erie: Harmful algal blooms and hypoxia. Harmful Algae, 2016, vol. 56, pp. 44–66.
Wellburn A.R. The spectral determination of chlorophylls a and b, as well as total carotenoids using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology, 1994, vol. 144, pp. 307–313.
Young E. B., Tucker R. C., Pansch L. A. Alkaline phosphatase in freshwater Cladophora – epiphyte assemblages: regulation in response to phosphorus supply and localization. Journal of Phycology, 2010, vol. 46, iss. 1, pp. 93–101.
Zulkifly S. B., Graham J. M., Young E. B., Mayer R. J., Piotrowski M. J., Smith I., Graham L. E. The genus Cladophora Kützing (Ulvophyceae) as a globally distributed ecological engineer. Journal of Phycology, 2013, vol. 49, iss. 1, pp. 1–17.
Zulkifly S., Hanshew A., Young E. B., Lee P., Graham M. E., Graham M. E., Piotrowski M., Graham L. E. The epiphytic microbiota of the globally widespread macroalga Cladophora glomerata (Chlorophyta, Cladophorales). American Journal of Botany, 2012, vol. 99, no. 9, pp. 1541–1552.
