Predation impact of ciliated and flagellated protozoa during a summer bloom of brown sulfur bacteria in a meromictic coastal lake

FEMS Microbiology Ecology

Volumn 70, Issue 1, 2009, Pages 42-53

  Saccà, Alessandro ^a   Borrego, Carles M ^b   Renda, Rossella ^a   Triadó Margarit, Xavier ^b   Bruni, Vivia ^a   Guglielmo, Letterio ^a  

^a UNIVERSITY OF MESSINA   (Italy)

^b UNIVERSITY OF GIRONA   (Spain)

Author keywords

Anoxic environment; Bacteriochlorophyll; Grazing; Meromictic lake; Planktonic protozoa; Sulfur bacteria

Indexed keywords

ANOXIC CONDITIONS; BACTERIUM; BIOMASS; CARBON FLUX; CHLOROPHYLL A; CILIATE; GRAZING; GROWTH RATE; LAKE ECOSYSTEM; PHOTOSYNTHESIS; PREDATION; PRIMARY PRODUCTION; STRATIFICATION; TEMPORAL DISTRIBUTION; TROPHIC LEVEL;

ARTICLE; BLEPHARISMA; CHLOROBIUM; CILIATE; CONTROLLED STUDY; CRYPTOPHYTA; EUPLOTES; FLAGELLATE; GRAZING; HETEROTROPH; ITALY; LAKE; MICROBIAL BIOMASS; NONHUMAN; PHAGOTROPH; PHOTOTROPHIC BACTERIUM; PICOPLANKTON; PLANKTON; PREDATION; PRIORITY JOURNAL; PROTISTAN COMMUNITY; SULFUR BACTERIUM; SUMMER; TROPHIC LEVEL;

ANIMALS; BACTERIA; BACTERIOCHLOROPHYLLS; BIOMASS; FRESH WATER; PLANKTON; PROTOZOA; SICILY; WATER MICROBIOLOGY;

CHLOROBI; CILIOPHORA; MASTIGOPHORA (FLAGELLATES); PHOTOBACTERIA; PROTOZOA;

EID: 69949158817     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2009.00735.x     Document Type: Article

References (74)

1. Allali K, Dolan J Rassoulzadegan F (1994) Culture characteristics and orthophosphate excretion of a marine oligotrich ciliate, Strombidium sulcatum, fed heat-killed bacteria. Mar Ecol-Prog Ser 105 : 159 165. (Pubitemid 24430647)
2. Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol-Prog Ser 10 : 257 263.
3. Bettarel Y, Amblard C, Sime-Ngando T, Carrias J-F, Sargos D, Garabétian F Lavandier P (2003) Viral lysis, flagellate grazing potential, and bacterial production in Lake Pavin. Microb Ecol 45 : 119 127.
4. Bettarel Y, Sime-Ngando T, Amblard C Dolan J (2004) Viral activity in two contrasting lake ecosystems. Appl Environ Microb 70 : 2941 2951.
5. Biagini GA, Finlay BJ Lloyd D (1998) Protozoan stimulation of anaerobic microbial activity: enhancement of the rate of terminal decomposition of organic matter. FEMS Microbiol Ecol 27 : 1 8.
6. Bloem JM, Bär-Gilissen JB Cappenberg TE (1986) Fixation, counting, and manipulation of heterotrophic nanoflagellates. Appl Environ Microb 52 : 1266 1272.
7. Boenigk J, Matz C, Jürgens K Arndt H (2001) The influence of pre-culture conditions and food quality on the ingestion and digestion process of three species of heterotrophic nanoflagellates. Microb Ecol 42 : 168 176.
8. Borrego CM Garcia-Gil LJ (1994) Separation of bacteriochlorophyll homologues from green photosynthetic sulphur bacteria by reversed-phase HPLC. Photosynth Res 41 : 157 163.
9. Borrego CM, Garcia-Gil LJ, Vila XP, Figueras JB Abella CA (1997) Distribution of bacteriochlorophyll homologues in natural populations of brown-colored phototrophic sulfur bacteria. FEMS Microbiol Ecol 24 : 301 309.
10. Borrego CM, Arellano JB, Abellà CA, Gillbro T Garcia-Gil LJ (1999) The molar extinction coefficient of bacteriochlorophyll e and the pigment stoichiometry in Chlorobium phaeobacteroides. Photosynth Res 60 : 257 264.
11. Carlson RE (1977) A trophic state index for lakes. Limnol Oceanogr 22 : 361 369.
12. Carlson RE (1980) More complications in the chlorophyll-Secchi disk relationship. Limnol Oceanogr 25 : 378 382.
13. Caron DA (1983) Technique for enumeration of heterotrophic and phototrophic nanoplankton, using epifluorescence microscopy, and comparison with other procedures. Appl Environ Microb 46 : 491 498.
14. Chang KH Hanazato T (2004) Diel vertical migrations of invertebrate predators (Leptodora kindtii, Thermocyclops taihokuensis, and Mesocyclops sp.) in a shallow, Eutrophic lake. Hydrobiologia 528 : 249 259.
15. Choi DH, Hwang CY Cho BC (2003) Comparison of virus- and bacterivory-induced bacterial mortality in the eutrophic Masan Bay, Korea. Aquat Microb Ecol 30 : 117 125.
16. De Meester L Vyverman W (1997) Diurnal residence of the larger stages of the Calanoid Copepod Acartia tonsa in the Anoxic Monimolimnion of a tropical Meromictic Lake in New Guinea. J Plankton Res 19 : 425 434.
17. Dolan JR (1991) Microphagous ciliates in mesohaline Chesapeake Bay waters: estimates of growth rates and consumption by copepods. Mar Biol 111 : 303 309.
18. Dolan JR (1997) Phosphorus and ammonia excretion by planktonic protists. Mar Geol 139 : 109 122.
19. Eccleston-Parry JD Leadbeater BSC (1995) Regeneration of phosphorus and nitrogen by four species of heterotrophic nanoflagellates feeding on three nutritional states of a single bacterial strain. Appl Environ Microb 61 : 1033 1038.
20. Fenchel T Finlay BJ (1990) Anaerobic free-living protozoa: growth efficiencies and the structure of anaerobic communities. FEMS Microbiol Ecol 74 : 269 276.
21. Fenchel T Finlay BJ (1995) Ecology and Evolution in Anoxic Worlds. Oxford University Press, Oxford, UK.
22. Fenchel T, Kristensen LD Rasmussen L (1990) Water column anoxia: vertical zonation of planktonic protozoa. Mar Ecol-Prog Ser 62 : 1 10.
23. Fenchel T, King GM Blackburn TH (1998) Bacterial Biogeochemistry: The Ecophysiology of Mineral Cycling. Academic Press, New York.
24. Fuhrman J Noble R (1995) Viruses and protists cause similar bacterial mortality in coastal seawater. Limnol Oceanogr 40 : 1236 1242. (Pubitemid 3016468)
25. Genovese S Magazzù G (1969) Manuale d'Analisi per le Acque Salmastre. La Editrice Universitaria, Messina.
26. González J, Iriberri J, Egea L Barcina I (1990) Differential rates of digestion of bacteria by freshwater and marine phagotrophic protozoa. Appl Environ Microb 56 : 1851 1857.
27. González J, Sherr E Sherr B (1993) Differential feeding by marine flagellates on growing versus starving and on motile versus non-motile bacterial prey. Mar Ecol-Prog Ser 102 : 257 267. (Pubitemid 24417246)
28. Guhl BE Finlay BJ (1993) Anaerobic predatory ciliates track seasonal migrations of planktonic photosynthetic bacteria. FEMS Microbiol Lett 107 : 313 316.
29. Hahn MW Höfle MG (1999) Flagellate predation on a bacterial model community: interplay of size-selective grazing, specific bacterial cell size, and bacterial community composition. Appl Environ Microb 65 : 4863 4872.
30. Hahn MW, Moore ERB Höfle MG (1999) Bacterial filament formation, a defense mechanism against flagellate grazing, is growth rate controlled in bacteria of different phyla. Appl Environ Microb 65 : 25 35.
31. John EH Davidson K (2001) Prey selectivity and the influence of prey carbon : nitrogen ratio on microflagellate grazing. J Exp Mar Biol Ecol 260 : 93 111.
32. Jürgens K Güde H (1994) The potential importance of grazing-resistant bacteria in planktonic systems. Mar Ecol-Prog Ser 112 : 169 188.
33. Kirchman DL (2000) Uptake and regeneration of inorganic nutrients by marine heterotrophic bacteria. Microbial Ecology of the Oceans (Kirchman DL, ed), pp. 261 288. Wiley-Liss, New York.
34. Kisand V Zingel P (2000) Dominance of ciliate grazing on bacteria during spring in a shallow eutrophic lake. Aquat Microb Ecol 22 : 135 142.
35. Kršinić F, Carić M, Viličić D Ciglenečki I (2000) The Calanoid Copepod Acartia italica Steuer, phenomenon in the small saline lake Rogoznica (Eastern Adriatic Coast). J Plankton Res 22 : 1441 1464.
36. Landry MR (1994) Methods and controls for measuring the grazing impact of planktonic protists. Mar Microb Food Webs 8 : 37 57.
37. Landry MR, Lehner-Fournier JM, Sundstrom JA, Fagerness VL Selph KE (1991) Discrimination between living and heat-killed prey by a marine zooflagellate Paraphysomonas vestita (Stokes). J Exp Mar Biol Ecol 146 : 139 151.
38. Lee S Fuhrman JA (1987) Relationship between biovolume and biomass of naturally derived marine bacterioplankton. Appl Environ Microb 53 : 1298 1303.
39. Massana R Pedrós-Alió C (1994) Role of anaerobic ciliates in planktonic food webs: abundance, feeding, and impact on bacteria in the field. Appl Environ Microb 60 : 1325 1334.
40. Matz C Jürgens K (2003) Interaction of nutrient limitation and protozoan grazing determines the phenotypic structure of a bacterial community. Microb Ecol 45 : 384 398.
41. Matz C Kjelleberg S (2005) Off the hook - how bacteria survive protozoan grazing. Trends Microbiol 13 : 302 307.
42. Matz C, Deines P Jürgens K (2002) Phenotypic variation in Pseudomonas sp. CM10 determines microcolony formation and survival under protozoan grazing. FEMS Microbiol Ecol 39 : 57 65.
43. McManus GB Okubo A (1991) On the use of surrogate food particles to measure protistan ingestion. Limnol Oceanogr 36 : 613 617.
44. Menden-Deuer S Lessard E (2000) Carbon to volume relationships for dinoflagellates, diatoms and other protist plankton. Limnol Oceanogr 45 : 569 579.
45. Monger BC, Landry MR Brown SL (1999) Feeding selection of heterotrophic marine nanoflagellates based on the surface hydrophobicity of their picoplankton prey. Limnol Oceanogr 44 : 1917 1927.
46. Norland S (1993) The relationship between biomass and volume of bacteria. Handbook of Methods in Aquatic Microbial Ecology (Kemp PF, Sherr BF, Sherr EB Cole J, eds), pp. 303 307. Lewis Publishers, Boca Raton, FL.
47. Norland S, Heldal M Tumyr O (1987) On the relation between dry matter and volume of bacteria. Microb Ecol 13 : 95 101.
48. Pace ML, McManus GB Findlay SEG (1990) Planktonic community structure determines the fate of bacterial production in a temperate lake. Limnol Oceanogr 35 : 795 808.
49. Pelegrì SP, Christaki U, Dolan J Rassoulzadegan F (1999) Particulate and dissolved organic carbon production by the heterotrophic nanoflagellates Pteridomonas danica. Microb Ecol 37 : 276 284.
50. Pfennig N (1989) Ecology of phototrophic purple and green sulphur bacteria. Autotrophic Bacteria (Schlegel HG Bowien B, eds), pp. 97 116. Springer-Verlag, New York.
51. Pfister G Arndt H (1998) Food selectivity and feeding behaviour in omnivorous filter-feeding ciliates: a case study for Stylonychia. Eur J Protistol 34 : 446 457.
52. Porter KG Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25 : 943 948.
53. Psenner R Schlott-Idl K (1985) Trophic relationships between bacteria and protozoa in the hypolilmnion of a meromictic mesotrophic lake. Hydrobiologia 121 : 111 120.
54. Rassoulzadegan F (1993) Protozoan patterns in the Azam-Ammerman's bacteria-phytoplankton mutualism. Trends in Microbial Ecology (Guerrero R Pedros-Alio C, eds), pp. 435 439. Spanish Society for Microbiology, Barcelona.
55. Rassoulzadegan F Sheldon RW (1986) Predator-prey interactions of nanozooplankton and bacteria in an oligotrophic marine environment. Limnol Oceanogr 31 : 1010 1021.
56. Saccà A, Guglielmo L Bruni V (2008) Vertical and temporal microbial community patterns in a meromictic coastal lake influenced by the Straits of Messina upwelling system. Hydrobiologia 600 : 89 104.
57. Sanders RW, Caron DA Berninger UG (1992) Relationship between bacteria and heterotrophic nanoplankton in marine and fresh waters: an inter-ecosystem comparison. Mar Ecol-Prog Ser 86 : 1 14.
58. Shannon PS, Chrzanowski TH Grover JP (2007) Prey food quality affects flagellate ingestion rates. Microb Ecol 53 : 66 73.
59. Sherr BF, Sherr EB Fallon RD (1987) Use of monodispersed, fluorescently labelled bacteria to estimate in situ protozoan bacterivory. Appl Environ Microb 53 : 958 965.
60. Sherr BF, Sherr EB Rassoulzadegan F (1988) Rates of digestion of bacteria by marine phagotrophic protozoa: temperature dependence. Appl Environ Microb 54 : 1091 1095.
61. Sherr EB Sherr BF (1993) Protistan grazing rates via uptake of fluorescently labeled prey. Handbook of Methods in Aquatic Microbial Ecology (Kemp PF, Sherr BF, Sherr EB Cole JJ, eds), pp. 695 701. Lewis Publishers, Boca Raton, FL.
62. Šimek K, Kojecká P, Nedoma J, Hartman P, Vrba J Dolan JR (1999) Shifts in bacterial community composition associated with different microzooplankton size fractions in a eutrophic reservoir. Limnol Oceanogr 44 : 1634 1644.
63. Šimek K, Pernthaler J, Weinbauer MG et al 2001) Changes in bacterial community composition and dynamics and viral mortality rates associated with enhanced flagellate grazing in a mesoeutrophic reservoir. Appl Environ Microb 67 : 2723 2733.
64. Simon M Azam F (1989) Protein content and protein synthesis rates of planktonic marine bacteria. Mar Ecol-Prog Ser 51 : 201 213.
65. Smith JHC Benitez A (1955) Chlorophylls: analysis in plant materials. Moderne Methoden der Pflanzenanalyse, Vol. 4 (Peach K Tracey MV, eds), pp. 142 196. Springer-Verlag, Berlin.
66. Šolić M Krstulović N (1994) Role of predation in controlling bacterial and heterotrophic nanoflagellate standing stocks in the coastal Adriatic Sea: seasonal patterns. Mar Ecol-Prog Ser 114 : 219 235.
67. Sorokin YI Donato N (1975) On the carbon and sulphur metabolism in the meromictic Lake Faro (Sicily). Hydrobiologia 47 : 241 252.
68. Trüper HG Genovese S (1968) Characterization of photosynthetic sulfur bacteria causing red water in Lake Faro (Messina, Sicily). Limnol Oceanogr 13 : 225 232.
69. Turley C (1993) Direct estimates of bacterial numbers in seawater sampler without incurring in cell loss due to sample storage. Handbook of Methods in Acquatic Microbial Ecology (Kemp PF, Sherr BF, Sherr EB Cole JJ, eds), pp. 143 147. Lewis Publishers, Boca Raton, FL.
70. Utermöhl H (1958) Zur Vervollkommung der quantitativen Phytoplankton Methodik. Mitt int Ver Theor Angew Limnol 9 : 1 38.
71. van Gemerden H Mas J (1995) Ecology of phototrophic sulfur bacteria. Anoxygenic Photosynthetic Bacteria (Blankenship RE, Madigan MT Bauer CE, eds), pp. 49 85. Kluwer Academic, Dordrecht.
72. Vaqué D, Gasol JM Marrasé C (1994) Grazing rates on bacteria: the significance of methodology and ecological factors. Mar Ecol-Prog Ser 109 : 263 274.
73. Verity PG Sieracki ME (1993) Use of color image analysis and epifluorescence microscopy to measure plankton biomass. Handbook of Methods in Aquatic Microbial Ecology (Kemp PF, Sherr BF, Sherr EB Cole JJ, eds), pp. 327 337. Lewis Publishers, Boca Raton, FL.
74. Vila X, Abella CA, Figueras JB Hurley JP (1998) Vertical models of phototrophic bacterial distribution in the metalimnetic microbial communities of several freshwater North-American kettle lakes. FEMS Microbiol Ecol 25 : 287 299.