Inorganic phosphorus and nitrogen modify composition and diversity of microbial communities in water of mesotrophic lake

Polish Journal of Microbiology

Volumn 58, Issue 1, 2009, Pages 77-90

  Chróst, Ryszard J ^a   Adamczewski, Tomasz ^a   Kalinowska, Krystyna ^b   Skowrońska, Agnieszka ^c  

^a UNIVERSITY OF WARSAW   (Poland)

^b CENTRE FOR ECOLOGICAL RESEARCH   (Poland)

^c UNIVERSITY OF WARMIA AND MAZURY IN OLSZTYN   (Poland)

Author keywords

Lake microbial community; Nitrogen; Phosphorus

Indexed keywords

CHLOROPHYLL A; LAKE WATER; NITROGEN; PHOSPHATE; PHOSPHORUS;

ALGAL BLOOM; ALPHAPROTEOBACTERIA; ARTICLE; BIOAVAILABILITY; BIOMASS; CONTROLLED STUDY; CYTOPHAGA; FLAVOBACTERIUM; FLUORESCENCE IN SITU HYBRIDIZATION; MESOCOSM; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; NONHUMAN; PHOTOSYNTHESIS; PROTISTAN COMMUNITY; SPECIES DIVERSITY; TAXONOMY; TURNOVER TIME;

ANIMALS; BACTERIA; BIODIVERSITY; BIOMASS; CELL MEMBRANE; CHLOROPHYLL; ECOSYSTEM; FRESH WATER; IN SITU HYBRIDIZATION, FLUORESCENCE; NITROGEN; PHOSPHORUS; PHOTOSYNTHESIS; PHYTOPLANKTON; PROTOZOA; WATER MICROBIOLOGY;

ALPHAPROTEOBACTERIA; BACTERIA (MICROORGANISMS); CILIOPHORA; CYTOPHAGA; FLAVOBACTERIUM; PROTISTA;

EID: 66649109357     PISSN: 17331331     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (76)

1. Amann R.I., B.J. Binder, R.J. Olson, S.W. Chisholm, R. Devereux and D.A. Stahl. 1990. Combination of 16S-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 56: 1919-1925.
2. Arndt H. 1993. Rotifers as predators on components of the microbial food web (bacteria, heterotrophic flagellates, ciliates) - a review. Hydrobiologia 255/256: 231-246.
3. Arar E.J. and G.B. Collins. 1997. Method 445.0. In vitro determination of chlorophyll a and phaeophytin a in marine and freshwater algae by fluorescence. National Exposure Research Laboratory, Office of Research and Development, U.S.E.P.A.
4. Børsheim K.Y. and G. Bratbak. 1987. Cell volume to cell carbon conversion factors for a bacterivorous Monas sp. enriched from seawater. Mar. Ecol. Prog. Ser. 36: 171-175.
5. Carlson P., E. Graneli, P. Tester and L. Boni. 1995. Influences of riverine humic substances on bacteria, protozoa, phytoplankton, and copepods in a coastal plankton community. Mar. Ecol. Prog. Ser. 127:213-221.
6. Caron D.A., J.C. Goldman and M.R. Dennett. 1988. Experimental demonstration of the roles of bacteria and bacterivorous protozoa in plankton nutrient cycles. Hydrobiologia 159: 27-40.
7. Christoffersen K., B. Riemann, L.R. Hansen, A. Klysner and H.B. Sørensen. 1990. Qualitative importance of the microbial loop and plankton community structure in a eutrophic lake during a bloom of cyanobacteria. Microb. Ecol. 20: 253-272.
8. Chróst R.J. and M.A. Faust. 1999. Consequences of solar radiation on bacterial secondary production and growth rates in subtropical coastal water (Atlantic Coral Reef off Belize, Central America). Aquat. Microb. Ecol. 20: 39-48.
9. Chróst R.J., M. Koton and W. Siuda. 2000. Bacterial secondary production and bacterial biomass in four Mazurian lakes of differing trophic status. Pol. J. Environ. Stud. 9: 255-266.
10. Chróst R.J. and H. Rai. 1994. Bacterial secondary production, pp. 92-117. In: Overbeck J. and R.J. Chróst (eds). Microbial Ecology of Lake Plußsee. Springer Verlag, New York.
11. Chróst R.J. and W. Siuda. 2006. Microbial production, utilization and enzymatic degradation of organic matter in the upper trophogenic water layer in the pelagial zone of lakes along the eutrophication gradient. Limnol. Oceanogr. 51: 749-762.
12. Chrzanowski T.H. and J.P. Grover. 2001. Effects of mineral nutrients on the growth of bacterio- and phytoplankton in two southern reservoirs. Limnol. Oceanogr. 46: 1319-1330.
13. Chrzanowski T.H., R.W. Sterner and J.J. Elser. 1995. Nutrient enrichment and nutrient regeneration stimulate bacterioplankton growth. Microb. Ecol. 29: 221-230.
14. Corno G. and K. Jürgens. 2006. Direct and indirect effects of protist predation on population size structure of a bacterial strain with high phenotypic plasticity. Appl. Environ. Microbiol. 1: 78-86.
15. Coveney M.E. and R.G. Wetzel. 1992. Effects of nutrients on specific growth rate of bacterioplankton in oligotrophic lake water cultures. Appl. Environ. Microbiol. 58: 150-156.
16. Crump B.C., G.W. Kling, M. Bahr and J.E. Hobbie. 2003. Bacterioplankton community shifts in an Arctic lake correlate with seasonal changes in organic matter source. Appl. Environ. Microbiol. 69: 2253-2268.
17. Currie D.J. and J. Kalff. 1984. The relative importance of bacterioplankton and phytoplankton in phosphorus uptake in freshwater. Limnol. Oceanogr. 29: 311-321.
18. del Giorgio P.A, J.M. Gasol, D. Vaquè, P. Mura, S. Agostí and C.M. Duarte. 1996. Bacterioplankton community structure: protists control net production and the proportion of active bacteria in a coastal marine community. Limnol. Oceanogr. 41: 1169-1179.
19. Ejsmont-Karabin J., Z. Gorelysheva, K. Kalinowska and T. Wȩgleńska. 2004. Role of zooplankton (Ciliata, Rotifera and Crustacea) in phosphorus removal from cycling: lakes of the river Jorka watershed (Masuria Lakeland, Poland). Pol. J. Ecol. 52: 275-284.
20. Fenchel T. 1986. The ecology of heterotrophic microflagellates. Adv. Microb. Ecol. 9: 57-97.
21. Fisher M.M., J.L. Klug, G. Lauster, M. Newton and E.W. Triplett. 2000. Effects of resources and trophic interactions on freshwater bacterioplankton diversity. Microb. Ecol. 40: 125-138.
22. Foissner W., H. Berger, H. Blatterer and F. Kohmann. 1995. Taxonomische und ökologische Revision der Ciliaten des Saprobiensystems. Band I-IV. Bayer. Landesamt für Wasserwirtschaft, München.
23. Gasol J.M., P.A. del Giorgio, R. Massana and C.M. Duarte. 1995. Active versus inactive bacteria: size-dependence in a coastal marine plankton community. Mar. Ecol. Prog. Ser. 128: 91-97.
24. Golterman H.L. 1969. Methods for Chemical Analyses of Fresh Waters. Blackwell Scientific Publications, Oxford.
25. Hahn M.W. and M.G. Höfle. 2001. Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol. Ecol. 35: 113-121.
26. Hahn M.W., E.R.B. Moore and M.G. Höfle. 1999. Bacterial filament formation, a defense mechanism against flagellate grazing, is growth rate-controlled in bacteria of different phyla. Appl. Environ. Microbiol. 65: 25-35.
27. Jardillier L., M. Basset, I. Domaizon, A. Belan, C. Amblard, M. Richardot and D. Debroas. 2004. Bottom-up and top-down control of bacterial community composition in the euphotic zone of a reservoir. Aquat. Microb. Ecol. 35: 259-273.
28. Joint I., P. Henriksen, G.A. Fonnes, D. Bourne, T.F. Thingstad and B. Riemann. 2002. Competition for inorganic nutrients between phytoplankton and bacterioplankton in nutrient manipulated mesocosms. Aquat. Microb. Ecol. 29: 45-159.
29. Jürgens K., J. Pernthaler, S. Schalla and R. Amman. 1999. Morphological and compositional changes in a planktonic bacterial community in response to enhanced protozoan grazing. Appl. Environ. Microbiol. 65: 1241-1250.
30. Jürgens K. and G. Stolpe. 1995. Seasonal dynamics of crustacean zooplankton, heterotrophic nanoflagellates and bacteria in a shallow, eutrophic lake. Freshwat. Biol. 33: 27-38.
31. Kivi K., S. Kaitala, H. Kuosa, J. Kuparinen, E. Leskinen, R. Lignell, B. Marcussen and T. Tamminen. 1993. Nutrient limitation and grazing control of the Baltic plankton community during annual succession. Limnol. Oceanogr. 38: 893-905.
32. Koton-Czarnecka M. and R.J. Chróst. 2003. Protozoans prefer large and metabolically active bacteria. Pol. J. Environ. Stud. 12: 325-334.
33. Lebaron P., P. Servais, M. Troussellier, C. Courties, G. Muyzer, L. Bernard, H. Schäfer, R. Pukall, E. Stackebrandt, T. Guindulain and J. Vives-Rego. 2001. Microbial community dynamics in Mediterranean nutrient-enriched seawater mesocosms: changes in abundances, activity and composition. FEMS Microbiol. Ecol. 34: 255-266.
34. Lee S. and J.A. Fuhrman. 1987. Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl. Environ. Microbiol. 53: 1298-1303.
35. Lindström E.S. 2000. Bacterioplankton community composition in five lakes differing in trophic status and humic content. Microb. Ecol. 40: 104-113.
36. Manz W., R. Amann, W. Ludwig, M. Wagner and K.H. Schleifer. 1992. Phylogenetic oligonucleotide probes fort the major subclasses of Proteobacteria: Problems and solutions. Syst. Appl. Microbiol. 15: 593-600.
37. Manz W., R. Amann, M. Vancanneyt and K.H. Schleifer. 1996. Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum Cytophaga-Flavobacter-Bacteroides in the natural environment. Microbiology 140: 2849-2858.
38. Morris D.P. and Jr. W.M. Lewis. 1992. Nutrient limitation of bacterioplankton growth in Lake Dilon, Colorado. Limnol. Oceanogr. 37: 1179-1192.
39. Neef A. 1997. Einzelzell-identifizierung von Bakterien zur Populationsanalyse in Komplexen Mikrobiellen Biozonosen. Ph.D. Thesis. Technische Universitat München, Munich, Germany
40. Oda Y., S.J. Slagman, W.G. Meijer, L.J. Forney and J.C. Gottschal. 2000. Influence of growth rate and starvation on fluorescent in situ hybridization of Rhodopseudomonas palustris. FEMS Microbiol. Ecol. 32: 205-213.
41. Pace M.L., J.E. Glasser and L.R. Pomeroy. 1984. A stimulation analysis of continental shelf food webs. Mar. Biol. 82: 47-63.
42. Pace M.L. 1993. Heterotrophic microbial processes. pp. 253-277. In: Carpenter S.R. and J.F. Kitchel (eds). The Trophic Cascade in Lakes. Cambridge University Press, New York.
43. Pace M.L. and J.J. Cole. 1996. Regulation of bacteria by resources and predation tested in whole-lake experiments. Limnol. Oceanogr. 41: 1448-1460.
44. Pace M.L. and E. Funke. 1991. Regulation of planktonic microbial communities by nutrients and herbivores. Ecology 72: 904-914.
45. Pearce D.A., C.J. van der Gast, K. Woodward and K.K. Newsham. 2005. Significant changes in the bacterioplankton community structure of a maritime Antarctic freshwater lake following nutrient enrichment. Microbiology 151: 3237-3248.
46. Pernthaler J., F.O. Glöckner, W. Schonhuber and R. Amann. 2001. Fluorescence in situ hybridization (FISH) with rRNA-targeted oligonucleotide probes. Methods Microbiol. 30: 207-226.
47. Pernthaler A., C.M. Preston, J. Pernthaler, E.F. DeLong and R. Amann. 2002. Comparison of fluorescently labeled oligonucleotide and polynucleotide probes for the detection of pelagic marine bacteria and Arachaea. Appl. Environ. Microbiol. 68: 661-667.
48. Pernthaler J., B. Sattler, K. Šimek, A. Schwarzenbacher and R. Psenner. 1996. Top-down effects on the size-biomass distribution of a freshwater bacterioplankton community. Aquat. Microb. Ecol. 10: 255-263.
49. Pernthaler J., E. Zollner, F. Warnecke and K. Jürgens. 2005. Bloom of filamentous bacteria in a mesotrophic lake: identity and potential controlling mechanism. Appl. Environ. Microbiol. 70: 6272-6281.
50. Pinhassi J., F. Azam, J. Hemphalä, R.A. Long, J. Martinez, U.L. Zweifel and Å. Hagström. 1999. Coupling between bacterioplankton species composition, population dynamics, and organic matter degradation. Aquat. Microb. Ecol. 17: 13-26.
51. Pinhassi J. and Å. Hagström. 2000. Seasonal succession in marine bacterioplankton. Aquat Microb. Ecol. 21: 245-256.
52. Porter K.G. and Y.S. Feig. 1980. The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr. 25: 943-948.
53. Psenner R. 1993. Determination of size and morphology of aquatic bacteria by automated image analysis. pp. 339-345. In: Kemp P.F., B.F. Sherr, E.B. Sherr and J.J. Cole (eds). Handbook of Methods in Aquatic Microbial Ecology. Lewis Publ., Boca Raton.
54. Putt M. and D.K. Stoecker. 1989. An experimentally determined carbon: volume ratio for "oligotrichous" ciliates from estuarine and coastal waters. Limnol. Oceanogr. 34: 1097-1103.
55. Redfield A.C., B.H. Ketchum and F.A. Richards. 1963. The influence of organisms on the composition of sea water. pp. 26-77. In: Hill M.N. (ed). The Sea. Vol.2. Wiley-Liss, New York.
56. Richardot M., D. Debroas, A. Thouvenot, D. Sargos, I.L. Berthon and J. Devaux. 2001. Influence of cladoceran grazing activity on dissolved organic matter, enzymatic hydrolysis and bacterial growth. J. Plankton Res. 23: 1249-1261.
57. Sanders R.W., K.G. Porter, S.J. Bennett and A.E. DeBiase. 1989. Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community. Limnol. Oceanogr. 34: 673-687.
58. Schäfer H., L. Bernard, C. Courties, P. Lebaron, P. Servais, R. Pukall, E. Stackebrandt, M. Troussellier, T. Guindulain, J. Vives-Rego and G. Muyzer. 2001. Microbial community dynamics in Mediterranean nutrient-enriched seawater mesocosms: changes in the genetic diversity of bacterial populations. FEMS Microbiol. Ecol. 34: 243-253.
59. Schumann R., U. Schiewer, U. Karoten and T. Rieling. 2003. Viability of bacteria from different aquatic habitats. II. Cellular fluorescent markers for membrane integrity and metabolic activity. Aquat. Microb. Ecol. 32: 137-150.
60. Solórzano L. 1969. Determination of ammonia in natural waters by the phenylhypochlorite method. Limnol. Oceanogr. 14: 799-800.
61. Stockner J.G. and K.S. Shortreed. 1989. Algal picoplankton production and contribution to food-webs in oligotrophic British Columbia lakes. Hydrobiologia 173: 151-166.
62. Šimek K. and T.H. Chrzanowski. 1992. Direct and indirect evidence of size-selective grazing on pelagic bacteria by freshwater nanoflagellates. Appl. Environ. Microbiol. 58: 3715-3720.
63. Šimek K., J. Jezbera, K. Hornak, J. Vrba and J. Sedá. 2004. Role of diatom-attached choanoflagellates of the genus Salpingoeca as pelagic bacterivores. Aquat. Microb. Ecol. 36: 257-269.
64. Šimek K., K. Jürgens, J. Nedoma, M. Comerma and J. Armengol. 2000. Ecological role and bacterial grazing of Halteria spp.: small oligotrichs as dominant pelagic ciliate bacterivores. Aquat. Microb. Ecol. 22: 43-56.
65. Šimek K., P. Kojecká, J. Nedoma, P. Hartman, J. Vrba and J.R. Dolan. 1999. Shifts in bacterial community composition associated with different microzooplankton size fractions in a eutrophic reservoir. Limnol. Oceanogr. 44: 1634-1644.
66. Šimek K., J. Pernthaler, M.G. Weinbauer, K. Hornák, J.R. Dolan, J. Nedoma, M. Mašin and R. Amann. 2001. Changes in bacterial community composition, dynamics, and viral mortality rates associated with enhanced flagellate grazing in a mesoeutrophic reservoir. Appl. Environ. Microbiol. 67: 2723-2733.
67. Šimek K., K. Hornák, J. Jezbera, M. Mašin, J. Nedoma, J.M. Gasol and M. Schauer. 2005. Influence of top-down and bottom-up manipulations on the R-BT065 subclaster of β-Proteobacteria, an abundant group in bacterioplankton of a freshwater reservoir. Appl. Environ. Microbiol. 71: 2381-2390.
68. Thingstad T.F. and F. Rasoulzadegan. 1995. Nutrient limitation, microbial food webs and biological C-pump: suggested interactions in a P-limited Mediterranean. Mar. Ecol. Prog. Ser. 117: 299-306.
69. Vadstein O. and A. Jensen. 1988. Growth and phosphorus status of limnetic phytoplankton and bacteria. Limnol. Oceanogr. 33: 489-503.
70. Vadstein O., Y. Olsen and H. Reinertsen. 1993. The role of planktonic bacteria in phosphorus cycling in lakes-Sink and link. Limnol. Oceanogr. 38: 1539-1544.
71. Vrede K., T. Vrede, A. Isaksson, and A. Karlsson. 1999. Effects of nutrients (phosphorus, nitrogen, and carbon) and zooplankton on bacterioplankton and phytoplankton - a seasonal study. Limnol. Oceanogr. 44: 1616-1624.
72. Wallner G., R. Amann, and W. Beisker. 1993. Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14: 136-143.
73. Weisse T. 1991. The microbial food web and its sensitivity to eutrophication and contaminant enrichment: a cross-system overview. Int. Rev. Ges. Hydrobiol. 76: 327-337.
74. Wetzel R.G. 1975. Limnology. Saunders, Ann Arbor.
75. Wright R.T. 1988. Methods for evaluating the interaction of substrate and grazing as factors controlling planktonic bacteria. Arch. Hydrobiol. Ergebn. Limnol. 31: 229-242.
76. Wright R.T. and R.B. Coffin. 1984. Measuring microzooplankton grazing on planktonic marine bacteria by its impact on bacterial production. Microb. Ecol. 10: 137-149.