Strong effects of amoebae grazing on the biomass and genetic structure of a Microcystis bloom (Cyanobacteria)

Environmental Microbiology

Volumn 12, Issue 10, 2010, Pages 2797-2813

  Van Wichelen, Jeroen ^a   van Gremberghe, Ineke ^a   Vanormelingen, Pieter ^a   Debeer, Ann Eline ^a   Leporcq, Bruno ^b   Menzel, Diana ^c   Codd, Geoffrey A ^c   Descy, Jean Pierre ^b   Vyverman, Wim ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF NAMUR   (Belgium)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FRESH WATER;

AMOEBA (LIFE CYCLE STAGE); ARTICLE; BACTERIAL GENOME; BIOMASS; CHEMISTRY; CLASSIFICATION; ECOSYSTEM; FOOD CHAIN; GENETICS; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; MICROCYSTIS;

AMOEBA; BIOMASS; ECOSYSTEM; FOOD CHAIN; FRESH WATER; GENOME, BACTERIAL; MICROCYSTIS; WATER MICROBIOLOGY;

AMOEBA (GENUS); CYANOBACTERIA; MICROCYSTIS; MICROCYSTIS AERUGINOSA; MICROCYSTIS VIRIDIS; PROTOZOA;

EID: 77957311651     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2010.02249.x     Document Type: Article

References (97)

1. Anderson OR. Annual abundances, diversity and growth potential of Gymnamoebae in a shallow freshwater pond. J Eukaryot Microbiol 1997, 44:393-398.
2. Anderson OR. A seasonal study of the carbon content of planktonic naked amoebae in the Hudson Estuary and in a productive freshwater pond with comparative data for ciliates. J Eukaryot Microbiol 2007, 54:388-391.
3. Arndt H. A critical review of the importance of rhizopods (naked and testate amoebae) and actinopods (Heliozoa) in lake plankton. Mar Microb Food Webs 1993, 7:3-29.
4. Bailey-Watts AE, Lund JWG. Observations on a diatom bloom in Loch Leven, Scotland. Biol J Linn Soc 1973, 5:235-253.
5. Bottrell H, Duncan A, Gliwicz ZM, Grygierek E, Herzig A, Hillbricht-Ilkowska A. A review of some problems in zooplankton production studies. Norw J Zool 1976, 24:419-456.
6. Briand E, Yepremian C, Humbert JF, Quiblier C. Competition between microcystin- and non-microcystin-producing Planktothrix agardhii (Cyanobacteria) strains under different environmental conditions. Environ Microbiol 2008, 10:3337-3348.
7. Briand E, Escoffier N, Straub C, Sabart M, Quiblier C, Humbert JF. Spatiotemporal changes in the genetic diversity of a bloom-forming Microcystis aeruginosa (Cyanobacteria) population. ISME J 2009, 3:419-429.
8. Caiola MG, Pellegrini S. Lysis of Microcystis aeruginosa (Kütz.) by Bdellovibrio-like bacteria. J Phycol 1984, 20:471-475.
9. Canter HM, Lund JWG. The importance of Protozoa in controlling abundance of planktonic algae in lakes. Proc Linn Soc Lond 1968, 179:203-219.
10. Canter HM, Heaney SI, Lund JWG. The ecological significance of grazing on planktonic populations of Cyanobacteria by the ciliate Nassula. New Phytol 1990, 114:247-263.
11. Carrillo E, Ferrero LM, Alonso-Andicoberry C, Basanta A, Martin A, Lopez-Rodas V, Costas E. Interstrain variability in toxin production in populations of the cyanobacterium Microcystis aeruginosa from water-supply reservoirs of Andalusia and lagoons of Doñana National Park (Southern Spain). Phycologia 2003, 42:269-274.
12. Choi HJ, Kim BH, Kim JD, Han MS. Streptomyces neyagawaensis as a control for the hazardous biomass of Microcystis aeruginosa (Cyanobacteria) in eutrophic freshwaters. Biol Control 2005, 33:335-343.
13. Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management 1999, Chorus IBartram J. eds, London, UK, E & FN Spon
14. Codd GA, Morrison LF, Metcalf JS. Cyanobacterial toxins: risk management for health protection. Toxicology Appl Pharmacology 2005, 203:264-272.
15. Cook WL, Ahearn DG. Natural control of Anabaena blooms by the amoeba Asterocaelum anabaenophilum sp. nov. The Distributional History of the Biota of the Southern Appalachians. Part IV. Algae and Fungi. Biogeography, Systematics, and Ecology 1976, 71-80. Parker BC, Roane MK. eds, Charlottesville, VA, USA, University Press of Virginia, pp.
16. Cottingham KL. Nutrients and zooplankton as multiple stressors of phytoplankton communities: evidence from size structure. Limnol Oceanogr 1999, 44:810-827.
17. Davis PA, Dent M, Parker J, Reynolds CS, Walsby AE. The annual cycle of growth rate and biomass change in Planktothrix spp. in Blelham Tarn, English Lake District. Freshw Biol 2003, 48:852-867.
18. De Bruin A, Ibelings BW, Kagami M, Mooij WM, Van Donk E. Adaptation of the fungal parasite Zygorhizidium planktonicum during 200 generations of growth on homogeneous and heterogeneous populations of its host, the diatom Asterionella formosa. J Eukaryot Microbiol 2008, 55:69-74.
19. Decaestecker E, Gaba S, Raeymaekers JAM, Stoks R, Van Kerckhoven L, Ebert D, De Meester L. Host-parasite 'Red Queen' dynamics archived in pond sediment. Nature 2007, 450:870-873.
20. Dejenie T, Asmelash T, Rousseaux S, Gebregiorgis T, Gebrekidan A, Gebrehiwot M. Impact of the fish Garra on the ecology of reservoirs and the occurrence of Microcystis blooms in semi-arid tropical highlands: an experimental assessment using enclosures. Freshw Biol 2009, 54:1605-1615.
21. Demott WR. Foraging strategies and growth inhibition in five daphnids feeding on mixtures of a toxic cyanobacterium and a green alga. Freshw Biol 1999, 42:263-274.
22. Standard Methods for the Examination of Water and Wastewater 2005, Eaton AClesceri LSRice EWGreenberg AE. eds, 21th, edn., Washington, DC, USA, American Public Health Association, American Water Works Association, Water Environment Federation
23. Fialkowska E, PajdakStos A. Inducible defence against a ciliate grazer, Pseudomicrothorax dubius, in two strains of Phormidium (Cyanobacteria). Proc R Soc Lond B Biol Sci 1997, 264:937-941.
24. Fogg GE, Stewart WDP, Fay P, Walsby AE. The Blue-Green Algae 1973, London, UK, Academic Press
25. Fulton RS, Paerl HW. Toxic and inhibitory effects of the blue-green-alga Microcystis-aeruginosa on herbivorous zooplankton. J Plankton Res 1987, 9:837-855.
26. Geng H, Xie P. Experimental studies on the effects of toxic Microcystis aeruginosa pcc7820 on the survival and reproduction of two freshwater rotifers Brachionus calyciflorus and Brachionus rubens. Ecotoxicology 2008, 17:709-715.
27. van Gremberghe I, Van Wichelen J, Van der Gucht K, Vanormelingen P, D'hondt S, Boutte C. Covariation between zooplankton community composition and cyanobacterial community dynamics in Lake Blaarmeersen (Belgium). FEMS Microbiol Ecol 2008, 63:222-237.
28. van Gremberghe I, Vanormelingen P, Van der Gucht K, Souffreau C, Vyverman W, De Meester L. Priority effects in experimental populations of the cyanobacterium Microcystis. Environ Microbiol 2009a, 11:2564-2573.
29. van Gremberghe I, Vanormelingen P, Vanelslander B, Van der Gucht K, D'hondt S, De Meester L, Vyverman W. Genotype-dependent interactions among sympatric Microcystis strains mediated by Daphnia grazing. OIKOS 2009b, 118:1647-1658.
30. Guillard RRL, Lorenzen CL. Yellow-green algae with chlorophyllide C. J Phycol 1972, 8:10-14.
31. Gumbo RJ, Ross G, Cloete ET. Biological control of Microcystis dominated harmful algal blooms. Afr J Biotechnol 2008, 7:4765-4773.
32. Haande S, Ballot A, Rohrlack T, Fastner J, Wiedner C, Edvardsen B. Diversity of Microcystis aeruginosa isolates (Chroococcales, Cyanobacteria) from East-African water bodies. Arch Microbiol 2007, 188:15-25.
33. Haney JF, Hall DJ. Sugar-coated Daphnia- preservation technique for Cladocera. Limnol Oceanogr 1973, 18:331-333.
34. Heinbokel JF. Studies on functional role of tintinnids in Southern-California Bight .2. Grazing rates of field populations. Mar Biol 1978, 47:191-197.
35. Hillebrand H, Dürselen CD, Kirschtel D, Pollingher U, Zohary T. Biovolume calculation for pelagic and benthic microalgae. J Phycol 1999, 35:403-424.
36. Holfeld H. Fungal infections of the phytoplankton: seasonality, minimal host density, and specificity in a mesotrophic lake. New Phytol 1998, 138:507-517.
37. Honjo M, Matsui K, Ueki M, Nakamura R, Fuhrman JA, Kawabata Z. Diversity of virus-like agents killing Microcystis aeruginosa in a hyper-eutrophic pond. J Plankton Res 2006, 28:407-412.
38. Huss VAR, Frank C, Hartmann EC, Hirmer M, Kloboucek A, Seidel BM. Biochemical taxonomy and molecular phylogeny of the genus Chlorella sensu lato (Chlorophyta). J Phycol 1999, 35:587-598.
39. Imai H, Chang KH, Kusaba M, Nakano S. Temperature-dependent dominance of Microcystis (Cyanophyceae) species: M. aeruginosa and M. wesenbergii. J Plankton Res 2009, 31:171-178.
40. Janse I, Meima M, Kardinaal WEA, Zwart G. High-resolution differentiation of cyanobacteria by using rRNA-internal transcribed spacer denaturing gradient gel electrophoresis. Appl Environ Microbiol 2003, 69:6634-6643.
41. Jöhnk KD, Huisman J, Sharples J, Sommeijer B, Visser PM, Stroom JM. Summer heatwaves promote blooms of harmful cyanobacteria. Global Change Biol 2008, 14:495-512.
42. Joung S-H, Kim C-H, Ahn C-J, Jang K-Y, Min Boo S, Oh H-M. Simple method for a cell count of the colonial cyanobacterium, Microcystis sp. J Microbiol 2006, 44:562-565.
43. Kardinaal WEA, Tonk L, Janse I, Hol S, Slot P, Huisman J, Visser PM. Competition for light between toxic and nontoxic strains of the harmful cyanobacterium Microcystis. Appl Environ Microbiol 2007a, 73:2939-2946.
44. Kardinaal WEA, Janse I, Kamst-van Agterveld M, Meima M, Snoek J, Mur LR. Microcystis genotype succession in relation to microcystin concentrations in freshwater lakes. Aquat Microb Ecol 2007b, 48:1-12.
45. Karling JS. Chytridiomycetarum Iconographia 1977, Vaduz, Liechtenstein, J. Cramer, Monticello, NY, USA, Lubrecht & Cramer
46. Lampert W. Laboratory studies on zooplankton-cyanobacteria interactions. NZ J Mar Fresh Res 1987, 21:483-490.
47. Laybourn-Parry J, Jones K, Holdich JP. Grazing by Mayorella sp. (Protozoa: Sarcodina) on Cyanobacteria. Funct Ecol 1987, 1:99-104.
48. Mackey MD, Mackey DJ, Higgins HW, Wright SW. CHEMTAX - a program for estimating class abundances from chemical markers: application to HPLC measurements of phytoplankton. Mar Ecol Prog Ser 1996, 144:265-283.
49. Mathes J, Arndt H. Annual cycle of protozooplankton (ciliates, flagellates and sarcodines) in relation to phytozooplankton and metazooplankton in Lake Neumühler See (Mecklenburg, Germany). Archiv Hydrobiol 1995, 134:337-358.
50. Menden-Deuer S, Lessard EJ. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol Oceanogr 2000, 45:569-579.
51. Metcalf JS, Codd GA. Microwave oven and boiling waterbath extraction of hepatotoxins from cyanobacterial cells. FEMS Microbiol Lett 2000, 184:241-246.
52. Metcalf JS, Bell SG, Codd GA. Production of novel polyclonal antibodies against the cyanobacterial toxin microcystin-LR and their application for the detection and quantification of microcystins and nodularin. Water Res 2000, 34:2761-2769.
53. Moisander PH, Lehman PW, Ochiai M, Corum S. Diversity of Microcystis aeruginosa in the Klamath River and San Francisco Bay delta, California, USA. Aquat Microb Ecol 2009, 57:19-31.
54. Murzov SA, Caron DA. Sporadic high abundances of naked amoebae in Black Sea plankton. Aquat Microb Ecol 1996, 11:161-169.
55. Muyzer G, Dewaal EC, Uitterlinden AG. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16s rRNA. Appl Environ Microbiol 1993, 59:695-700.
56. Nishibe Y, Kawabata Z, Nakano S. Grazing on Microcystis aeruginosa by the heterotrophic flagellate Collodictyon triciliatum in a hypertrophic pond. Aquat Microb Ecol 2002, 29:173-179.
57. Nishibe Y, Manage PM, Kawabata Z, Nakano S. Trophic coupling of a testate amoeba and Microcystis species in a hypertrophic pond. Limnology 2004, 5:71-76.
58. O'Kelly CJ, Peglar MT, Black MND, Sawyer TK, Nerad TA. Korotnovella hemistylolepis N. Sp. and Korotnevella monacantholepis N. Sp. (Paramoebidae), two new scale-covered mesohaline amoebae. J Eukaryot Microbiol 2001, 48:655-662.
59. Otsuka S, Suda S, Li RH, Watanabe M, Oyaizu H, Matsumoto S, Watanabe MM. Phylogenetic relationships between toxic and non-toxic strains of the genus Microcystis based on 16S to 23S internal transcribed spacer sequence. FEMS Microbiol Lett 1999, 172:15-21.
60. Otsuka S, Suda S, Shibata S, Oyaizu H, Matsumoto S, Watanabe MM. A proposal for the unification of five species of the cyanobacterial genus Microcystis Kutzing ex Lemmermann 1907 under the Rules of the Bacteriological Code. Int J Syst Evol Microbiol 2001, 51:873-879.
61. Paerl HW, Huisman J. Climate - blooms like it hot. Science 2008, 320:57-58.
62. Reynolds CS, Jaworski GHM, Cmiech HA, Leedale GF. On the annual cycle of the blue-green alga Microcystis aeruginosa Kütz. Emend. Elenkin. Phylosophical Trans R Soc Lond B 1981, 239:419-477.
63. Rinta-Kanto JM, Konopko EA, DeBruyn JM, Bourbonniere RA, Boyer GL, Wilhelm SW. Lake Erie Microcystis: relationship between microcystin production, dynamics of genotypes and environmental parameters in a large lake. Harmful Algae 2009, 8:665-673.
64. Rogerson A, Gwaltney C. High numbers of naked amoebae in the planktonic waters of a mangrove stand in Southern Florida, USA. J Eukaryot Microbiol 2000, 47:235-241.
65. Rogerson A, Anderson OR, Vogel C. Are planktonic naked amoebae predominately floc associated or free in the water column? J Plankton Res 2003, 25:1359-1365.
66. Rohrlack T, Dittmann E, Börner T, Christoffersen K. Effects of cell-bound microcystins on survival and feeding of Daphnia spp. Appl Environ Microbiol 2001, 67:3523-3529.
67. Rothhaupt KO. The influence of toxic and filamentous blue-green algae on feeding and population-growth of the rotifer Brachionus rubens. Int Revue ges Hydrobiol 1991, 76:67-72.
68. Rudi K, Skulberg OM, Larsen F, Jakobsen KS. Strain characterization and classification of oxyphotobacteria in clone cultures on the basis of 16S rRNA sequences from the variable regions V6, V7, and V8. Appl Environ Microbiol 1997, 63:2593-2599.
69. Sarmento H, Descy J-P. Use of marker pigments and functional groups for assessing the status of phytoplankton assemblages in lakes. J Appl Phycol 2008, 20:1001-1011.
70. Sarnelle O, Wilson AE. Local adaptation of Daphnia pulicaria to toxic cyanobacteria. Limnol Oceanogr 2005, 50:1565-1570.
71. Schembri MA, Neilan BA, Saint CP. Identification of genes implicated in toxin production in the cyanobacterium Cylindrospermopsis raciborskii. Environ Toxicol 2001, 16:413-421.
72. Shapiro J. The role of carbon dioxide in the initiation and maintenance of blue-green dominance in lakes. Freshw Biol 1997, 37:307-323.
73. Sherr EB, Sherr BF. Preservation and Storage of Samples for Enumeration of Heterotrophic Protists. Handbook of Methods in Aquatic Microbial Ecology 1993, 207-212. Kemp PF, Sherr BFSherr EBCole JJ. eds, Boca Raton, FL, USA, CRC Press, pp.
74. Sigee DC, Glenn R, Andrews MJ, Bellinger EG, Butler RD, Epton HAS, Hendry RD. Biological control of cyanobacteria: principles and possibilities. Hydrobiologia 1999, 395/396:161-172.
75. Sigee DC, Selwyn A, Gallois P, Dean AP. Patterns of cell death in freshwater colonial cyanobacteria during the late summer bloom. Phycologia 2007, 46:284-292.
76. Sims GP, Aitken R, Rogerson A. Identification and phylogenetic analysis of morphologically similar naked amoebae using small subunit ribosomal RNA. J Eukaryot Microbiol 2002, 49:478-484.
77. Smirnov AV, Goodkov AV. An illustrated list of basic morphotypes of Gymnamoebia (Rhizopoda, Lobosea). Protistology 1999, 1:20-29.
78. Sommer U, Gliwicz ZM, Lampert W, Duncan A. The PEG-model of seasonal succession of planktonic events in fresh waters. Archiv Hydrobiol 1986, 106:433-471.
79. Streble H, Krauter D. Das Leben Im Wassertropfen 1981, Stuttgart, Germany, Kosmos, Franckh'sche Verslagshandlung, W. Keller & Co
80. Takamura N, Watanabe M. Seasonal changes in the biomass of four species of Microcystis spp. Jap J Limnol 1987, 48:139-144.
81. Tarutani K, Nagasaki K, Yamaguchi M. Viral impacts on total abundance and clonal composition of the harmful bloom-forming phytoplankton Heterosigma akashiwo. Appl Environ Microbiol 2000, 66:4916-4920.
82. Tillmanns AR, Wilson AE, Pick FR, Sarnelle O. Meta-analysis of cyanobacterial effects on zooplankton population growth rate: species-specific responses. Fundam Appl Limnol 2008, 171:285-295.
83. Tucker S, Pollard P. Identification of cyanophage Ma-LBP and infection of the cyanobacterium Microcystis aeruginosa from an Australian subtropical lake by the virus. Appl Environ Microbiol 2005, 71:629-635.
84. Van Wichelen J, Muylaert K, Van der Gucht K, Vyverman W. Observations on little studied protists (chytrids and an amoeba), affecting phytoplankton populations in the upper reaches of the Schelde Estuary (Belgium). Belgian J Botany 2006, 139:153-166.
85. Vanormelingen P, Vyverman W, De Bock D, Van der Gucht K, Demeester L. Local genetic adaptation to grazing pressure of the green algae Desmodesmus armatus in a strongly connected pond system. Limnol Oceanogr 2008, 54:503-511.
86. Vezie C, Rapala J, Vaitomaa J, Seitsonen J, Sivonen K. Effect of nitrogen and phosphorus on growth of toxic and nontoxic Microcystis strains and on intracellular microcystin concentrations. Microb Ecol 2002, 43:443-454.
87. Visser PM, Ibelings BW, Mur LR, Walsby AE. The ecophysiology of the harmful cyanobacterium Microcystis. Aquatic Ecology Series 3: Harmful Cyanobacteria 2005, 109-142. Huisman J, Matthijs HC, Visser PM, eds, Dordrecht, The Netherlands, Springer, pp.
88. Weisse T, Müller H. Planktonic protozoa and the microbial food web in Lake Constance. Spec Issues Advanc Limnol 1998, 53:223-254.
89. Wilson AE, Sarnelle O, Neilan BA, Salmon TP, Gehringer MM, Hay ME. Genetic variation of the bloom-forming cyanobacterium Microcystis aeruginosa within and among lakes: implications for harmful algal blooms. Appl Environ Microbiol 2005, 71:6126-6133.
90. Wright SJL, Redhead K, Maudsley H. Acanthamoeba castellanii, a predator of cyanobacteria. J Gen Microbiol 1981, 125:293-300.
91. Wright SW, Jeffrey SW, Mantoura RFC, Llewellyn CA, Bjornland T, Repeta D, Welschmeyer N. Improved HPLC method for the analysis of chlorophylls and carotenoids from marine phytoplankton. Mar Ecol Prog Ser 1991, 77:183-196.
92. Yagi O, Ohkubo N, Tomioka N, Okada M. Effect of irradiance and temperature on photosynthetic activity of the cyanobacterium Microcystis spp. Environ Technol 1994, 15:389-394.
93. Yoshida M, Yoshida T, Satomi M, Takashima Y, Hosoda N, Hiroishi S. Intra-specific phenotypic and genotypic variation in toxic cyanobacterial Microcystis strains. J Appl Microbiol 2008, 105:407-415.
94. Yoshida T, Jones LE, Ellner SP, Fussmann GF, Hairston NG. Rapid evolution drives ecological dynamics in a predator-prey system. Nature 2003, 424:303-306.
95. Yoshida T, Ellner SP, Jones LE, Bohannan BJM, Lenski RE, Hairston NG. Cryptic population dynamics: rapid evolution masks trophic interactions. PLoS Biol 2007, 5:1868-1879.
96. Zhang X, Hu HY, Hong Y, Yang J. Isolation of a Poterioochromonas capable of feeding on Microcystis aeruginosa and degrading microcystin-LR. FEMS Microbiol Lett 2008, 288:241-246.
97. Zwart G, Huismans R, van Agterveld MP, Van de Peer Y, De Rijk P, Eenhoorn H. Divergent members of the bacterial division Verrucomicrobiales in a temperate freshwater lake. FEMS Microbiol Ecol 1998, 25:159-169.