Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-24T01:47:15.190Z Has data issue: false hasContentIssue false

Benefits and costs of the grazer-induced colony formation in Microcystis aeruginosa

Published online by Cambridge University Press:  21 August 2009

Zhen Yang
Affiliation:
State Key Laboratory of Lake Science Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, 73 East Beijing Road, 210008 Nanjing, China Graduate School of the Chinese Academy of Sciences, 100039 Beijing, China
Fanxiang Kong*
Affiliation:
State Key Laboratory of Lake Science Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, 73 East Beijing Road, 210008 Nanjing, China
Zhou Yang
Affiliation:
Jiangsu Key Laboratory for Biodiversity and Biotechnology, School of Biological Sciences, Nanjing Normal University, 1 Wenyuan Road, 210046 Nanjing, China
Min Zhang
Affiliation:
State Key Laboratory of Lake Science Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, 73 East Beijing Road, 210008 Nanjing, China
Yang Yu
Affiliation:
State Key Laboratory of Lake Science Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, 73 East Beijing Road, 210008 Nanjing, China
Shanqin Qian
Affiliation:
State Key Laboratory of Lake Science Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, 73 East Beijing Road, 210008 Nanjing, China Graduate School of the Chinese Academy of Sciences, 100039 Beijing, China
Get access

Abstract

Colonial Microcystis aeruginosa were obtained when the unicellular algae were exposed to flagellate Ochromonas sp. filtrate. To investigate the benefit of this morphological change, flagellates were added into cultures of unicellular and colonial M. aeruginosa, respectively. The clearance rates of flagellates on algae were markedly decreased when they were cultivated with induced colonial M. aeruginosa. This result indicated that colony formation in M. aeruginosa was a predator-induced defense, which could reduce predation risk from flagellate. The increased content of soluble extracellular polysaccharide (sEPS) and bound extracellular polysaccharide (bEPS) may play an important role in adhering M. aeruginosa cells together to form colonies. The decrease of ΦPS II and the increase of sinking rates of induced colonial M. aeruginosa showed that the costs of grazed-induced colony formation in M. aeruginosa may reflect in the photosystem II efficiency, and in the sinking rates.

Type
Research Article
Copyright
© EDP Sciences, 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agrawal A.A., 1998. Algal defense, grazers, and their interactions in aquatic trophic cascades. Acta Oecol., 19, 331–337.
Bienfang, P.K., 1981. SETCOL – a technically simple and reliable method for measuring phytoplankton sinking. Can. J. Fish. Aquat. Sci. , 38, 12891294. CrossRef
Bolch, C.J.S. and Blackburn, S.I., 1996. Isolation and purification of Australian isolates of the toxic cyanobacterium Microcystis aeruginosa Kütz. J. Appl. Phycol. , 8, 513. CrossRef
Brookes, J. and Ganf, G.G., 2001. Variations in the buoyancy response of Microcystis aeruginosa to nitrogen, phosphorus and light. J. Plankton Res. , 23, 13991411. CrossRef
De Philippis R. and Vincenzini M., 1998. Exocellular polysaccharides from cyanobacteria and their possible applications. FEMS Microbiol. Rev., 22, 151–175.
Dodson S.I., 1989. The ecological role of chemical stimuli for the zooplankton, predator-induced morphology in Daphnia. Oecologia, 78, 361–367.
Fulton, R.S. and Paerl, H.W., 1987. Toxic and inhibitory effects of the blue-green alga M. aeruginosa on herbivorous zooplankton. J. Plankton Res. , 9, 837855. CrossRef
Geel, C., Versluis, W. and Snel, J.F.H., 1997. Estimation of oxygen evolution by marine phytoplankton from measurement of the efficiency of photosystem II electron flow. Phot. Res. , 51, 6170. CrossRef
Genty, B., Briantais, J.M. and Baker, N.R., 1989. The relationship between the quantum yield of photosynthesis electron transport and quenching of chlorophyll fluorescence. Biochem. Biophys. Acta , 990, 8792. CrossRef
Herbert D., Phipps P.J. and Strange R.E., 1971. Chemical analysis of microbial cells, Academic Press, London, UK, 209 p.
Hessen D.O. and van Donk E., 1993. Morphological changes in Scenedesmus induced by substances released from Daphnia. Arch. Hydrobiol., 127, 129–140.
Hofstraat, J.W., Peeters, J.H.C., Snel, J.H.F. and Geel, C., 1994. Simple determination of photosynthetic efficiency and photoinhibition of Dunaliella tertiolecta by saturating pulse fluorescence measurements. Mar. Ecol. Prog. Ser. , 103, 187196. CrossRef
Jang M.H., Ha K., Joo G.J. and Takamura N., 2003. Toxin production of cyanobacteria is increased by exposure to zooplankton. Freshwater Biol., 48, 1540–1550.
Jungmann, D., 1992. Toxic compounds isolated from Microcystis PCC7806 that are more active against Daphnia than 2 microcystins. Limnol. Oceanogr. , 37, 17771793. CrossRef
Kolber, Z. and Falkowski, P.G., 1993. Use of active fluorescence to estimate phytoplankton photosynthesis in situ. Limnol. Oceanogr. , 38, 16461665. CrossRef
Lampert, W., Rothhaupt, K.O. and von Elert, E., 1994. Chemical induction of colony formation in a green alga (Scenedesmus acutus) by grazers (Daphnia). Limnol. Oceanogr. , 39, 15431550. CrossRef
Lürling M., 2003. Effects of microcystin-free and Microcystin containing strains of the cyanobacterium Microcystis aeruginosa on growth of the grazer Daphnia magna. Environ. Toxicol., 18, 202–210.
Lürling M. and van Donk E., 1996. Zooplankton-induced unicell-colony transformation in Scenedesmus acutus and its effect on growth of herbivore Daphnia. Oecologia, 108, 432–437.
Lürling M. and van Donk E., 2000. Grazer-induced colony formation in Scenedesmus: are there costs to being colonial? Oikos, 88, 111–118.
Marinone M.C. and Zaragese H.E., 1991. A field and laboratory study on factors affecting polymorphism in the rotifer Keratella tropica. Oecologia, 86, 372–377.
Mole, S., 1994. Trade-offs and constraints in plant-herbivore defense theory: a life-history perspective. Oikos , 71, 312. CrossRef
Oliver, R.L., 1994. Floating and sinking in gas-vacuolate cyanobacteria. J. Phycol. , 30, 161173. CrossRef
Ou, D.Y., Song, L.R., Gan, N.Q. and Chen, W., 2005. Effects of microcystins and toxin degradation by Poterioochromonas sp. Environ. Toxicol. , 20, 373380. CrossRef
Pajdak-Stós, A., Fialkowska, E. and Fyda, J., 2001. Phormidium autumnale (Cyanobacteria) defense against three ciliate grazer species. Aquat. Microb. Ecol. , 23, 237244. CrossRef
Peters R.H., 1984. Methods for the study of feeding, grazing and assimilation by zooplankton, Blackwell, Oxford, UK.
Reynolds C.S., 1984. The ecology of freshwater phytoplankton, Cambridge University Press, Cambridge, UK.
Reynolds, C.S. and Walsby, A.E., 1975. Water blooms. Biol. Rev. , 50, 437481. CrossRef
Reynolds, C.S., Jaworski, G., Cmiech, H. and Leedale, G., 1981. On the annual cycle of the blue-green alga M. aeruginosa Kütz. Philos. T. R. Soc. B. , 293, 419477. CrossRef
Reynolds, C.S., Oliver, R.L. and Walsby, A.E., 1987. Cyanobacterial dominance: the role of buoyancy regulation in dynamic lake environments. N. Z. J. Mar. Freshwater Res. , 21, 379390. CrossRef
Rippka, R., Deruelles, J., WaterburyJ., Herdman M. and Stanier R., 1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. , 111, 161.
Tang, K.W., 2003. Grazing and colony size development in Phaeocystis globosa (Prymnesiophyceae): the role of a chemical signal. J. Plankton Res. , 25, 831842. CrossRef
Thornton, D.C.O., 2002. Diatom aggregation in the sea: mechanisms and ecological implications. Eur. J. Phycol. , 37, 149161. CrossRef
Tollrian R. and Dodson S.I., 1999. Inducible defenses in cladacera: contraints, costs, and multipredator environments, Princeton University Press, Princeton, USA.
Valério E., Faria N., Paulino S. and Pereira P., 2008. Seasonal variation of phytoplankton and cyanobacteria composition and associated microcystins in six Portuguese freshwater reservoirs. Ann. Limnol. - Int. J. Lim., 44, 189–196.
van Holthoon, F.L., van Beek, T.A., Lürling, M., van Donk, E. and De Groot, A., 2003. Colony formation in Scenedesmus: a literature overview and further steps towards the chemical characterisation of the Daphnia kairomone. Hydrobiologia , 491, 241254. CrossRef
van Rijssel M., Janse I., Noordkamp D.J.B. and Gieskes W.W.C., 2000. An inventory of factors that affect polysaccharide production by Phaeocystis globosa. J. Sea Res., 43, 297–306.
Wicklow, B.J., 1997. Signal-induced defensive phenotypic changes in ciliated protists: morphological and ecological implications for predator and prey. J. Eukar. Microbiol. , 44, 176188. CrossRef
Yan R., Kong F.X. and Han X.B., 2004. [Analysis of the recruitment of the winter survival algae on the sediments of Lake Taihu by fluorometry]. J. Lake Sci., 16, 163–168 (in Chinese with English abstract).
Yang, Z., Kong, F.X., Cao, H.S. and Shi, X.L., 2005. Observation on colony formation of Microcystis aeruginosa induced by filtered lake water under laboratory conditions. Ann. Limnol. - Int. J. Lim. , 41, 169173. CrossRef
Yang, Z., Kong, F.X., Shi, X.L. and Cao, H.S., 2006. Morphological response of M. aeruginosa to grazing by different sorts of zooplankton. Hydrobiologia , 563, 225230. CrossRef
Yang, Z., Kong, F.X., Shi, X.L., Xing, P. and Cao, H.S., 2008. Changes in the morphology and polysaccharide content of Microcystis aeruginosa (cyanobacteria) during flagellate grazing. J. Phycol. , 44, 716720. CrossRef
Yang Z., Kong F.X., Zhang M., Yang Z., Yu Y. and Qian S.Q., 2009. Effect of filtered cultures of flagellate Ochromonas sp. on colony formation in Microcystis aeruginosa. Int. Rev. Hydrobiol., 94, 143–152.
Zhang, X.M. and Watanabe, M.M., 1996. Light and electron microscopy of grazing by Poterioochromonas malhamensis (Chrysophyceae) on a range of phytoplankton taxa. J. Phycol. , 32, 3746. CrossRef