Grazing and virus-induced mortality of microbial populations before and during the onset of annual hypoxia in Lake Erie

Aquatic Microbial Ecology

Volumn 51, Issue 2, 2008, Pages 117-128

  Gobler, Christopher J ^a   Davis, Timothy W ^a   Deonarine, Sarah N ^a   Saxton, Matthew A ^b   Lavrentyev, Peter J ^c   Jochem, Frank J ^d   Wilhelm, Steven W ^b  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

^c UNIVERSITY OF AKRON   (United States)

^d FLORIDA INTERNATIONAL UNIVERSITY   (United States)

Author keywords

Grazing; Great Lakes; Hypoxia; Microbial mortality; Viruses

Indexed keywords

ALGAE; BACTERIA (MICROORGANISMS); CILIOPHORA; CYANOBACTERIA; EUKARYOTA; PROKARYOTA; ROTIFERA;

EID: 46949087412     PISSN: 09483055     EISSN: None     Source Type: Journal    
DOI: 10.3354/ame01180     Document Type: Article

References (53)

1. Baines SB, Pace ML (1991) The production of dissolved organic carbon by phytoplankton and its importance to bacteria - patterns across marine and fresh-water systems. Limnol Oceanogr 36:1078-1090
2. Bark AW, Goodfellow JG (1985) Studies on ciliated protozoa in eutrophic lakes. 2. Field and laboratory studies on the effects of oxygen and other chemical gradients on the ciliate distribution. Hydrobiologia 124:167-188
3. Bettarel Y, Amblard C, Sime-Ngando T, Carries JF, Sargos D, Garabetian F, Lavandier P (2003) Viral lysis, flagellate grazing potential, and bacterial production in Lake Pavin. Microb Ecol 45:119-127
4. Binder B (1999) Reconsidering the relationship between virally induced bacterial mortality and frequency of infected cells. Aquat Microb Ecol 18:207-215
5. Calbet A, Landry MR (2004) Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol Oceanogr 49:51-57
6. Carrick HJ, Fahnenstiel GL, Taylor WD (1992) Growth and production of planktonic protozoa in Lake Michigan: in situ and in vitro comparisons and importance to food web dynamics. Limnol Oceanogr 37:1221-1235
7. Charlton MN (1980) Oxygen depletion in Lake Erie: Has there been any change? Can J Fish Aquat Sci 37:72-81
8. 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
9. Colombet J, Sime-Ngando T, Cauchie HM, Fonty G, Hoffmann L, Demeure G (2006) Depth-related gradients of viral activity in Lake Pavin. Appl Environ Microbiol 72:4440-4445
10. DeBruyn JM, Leigh-Bell JA, McKay RML, Bourbonniere RA, Wilhelm SW (2004) Microbial distributions and the impact of phosphorus on bacterial activity in Lake Erie. J Gt Lakes Res 30:166-183
11. Detmer AE, Giesenhagen HC, Trenkel VM, Auf dem Venne H, Jochem FJ (1993) Phototrophic and heterotrophic pico-and nanoplankton in anoxic waters of the central Baltic Sea. Mar Ecol Prog Ser 99:197-203
12. Fahnenstiel GL, Krause AE, McCormick MJ, Carrick HJ (1998) The structure of the planktonic food-web in the St. Lawrence Great Lakes. J Gt Lakes Res 24:531-554
13. Fuhrman JA, Noble RT (1995) Viruses and protists cause similar bacterial mortality in coastal seawater. Limnol Oceanogr 40:1236-1242
14. Gardner WS, Lavrentyev PJ, Cavaletto JF, McCarthy MJ, Eadie BJ, Johengen TH, Cotner JB (2004) Distribution and dynamics of nitrogen and microbial plankton in southern Lake Michigan during spring transition 1999-2000. J Geophys Res 109(C3):C03007
15. Gobler CJ, Hutchins DA, Fisher NS, Cosper EM, Sanudo-Wilhelmy SA (1997) Cycling and bioavailablity of C, N, P, Fe and Se released by viral lysis of a marine chrysophyte. Limnol Oceanogr 42:1492-1504
16. Gobler CJ, Deonarine SN, Leigh-Bell J, Downes Gastlich M, Anderson OR, Wilhelm SW (2004) Ecology of phytoplankton communities dominated by Aureococcus anophagefferens: the role of viruses, nutrients, and microzooplankton grazing. Harmful Algae 3:471-483
17. Hasle GR (1978) The inverted microscope method. UNESCO Monogr Oceanogr Method 6:88-96
18. Hwang SJ, Heath RT (1997a) The distribution of protozoa across a trophic gradient, factors controlling their abundance and importance in the plankton food web. J Plankton Res 19:491-518
19. Hwang SJ, Heath RT (1997b) Bacterial productivity and protistan bacterivory in coastal and offshore communities of Lake Erie. Can J Fish Aquat Sci 54:788-799
20. Hwang SJ, Heath RT (1999) Zooplankton bacterivory at coastal and offshore sites of Lake Erie. J Plankton Res 21:699-719
21. Jacquet S, Domazon I, Personnic S, Ram ASP, Hedal M, Duhamel S, Sime-Ngano T (2005) Estimates of protozoan-and viral-mediated mortality of bacterioplankton in Lake Bourget (France). Freshw Biol 50:627-645
22. Jochem FJ (2001) Morphology and DNA content of bacterioplankton in the northern Gulf of Mexico: analysis by epifluorescence microscopy and flow cytometry. Aquat Microb Ecol 25:179-194
23. Johannsson O, Dermott R, Graham DM, Dahl JA, Millard ES, Myles DD, LeBlanc J (2000) Benthic and pelagic secondary production in Lake Erie after the invasion of Dreissena spp. with implications for fish production. J Gt Lakes Res 26:31-54
24. Landry MR, Kirshtein J, Constantinou J (1995) A refined dilution technique for measuring the community grazing impact of microzooplankton, with experimental tests in the central equatorial Pacific. Mar Ecol Prog Ser 120:53-63
25. Lavrentyev PJ, Gardner WS, Cavaletto JF, Beaver JR (1995) Effects of the zebra mussel (Dreissena polymorpha Pallas) on protozoa and phytoplankton in Saginaw Bay, Lake Huron. J Gt Lakes Res 21:545-557
26. Lavrentyev PJ, McCarthy MJ, Klarer DM, Jochem FJ, Gardner WS (2004) Estuarine microbial food web patterns in a Lake Erie coastal wetland. Microb Ecol 48:567-577
27. Lee S, Fuhrman J (1987) Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl Environ Microbiol 53:1298-1303
28. Miller CA, Penry DL, Gilbert PM (1995) The impact of trophic interactions on rates of nitrogen regeneration and grazing in Chesapeake Bay. Limnol Oceanogr 40:1005-1011
29. Nagata T, Kirchman DL (1992) Release of macromolecular organic complexes by heterotrophic marine flagellates. Mar Ecol Prog Ser 83:233-240
30. Noble RT, Middelboe M, Fuhrman JA (1999) Effects of viral enrichment on the mortality and growth of heterotrophic bacterioplankton. Aquat Microb Ecol 18:1-13
31. North RL, Guildford SJ, Smith REH, Havens SM, Twiss MR (2007) Evidence for phosphorus, nitrogen, and iron colimitation of phytoplankton communities in Lake Erie. Limnol Oceanogr 52:315-328
32. Olson RJ, Zettler ER, Chisholm SW, Dusenberry JA (1991) Advances in oceanography through flow cytometry. In: Demers S (ed) Particle analysis in oceanography. Springer-Verlag, Berlin, p 351-399
33. Proctor LM, Okubo A, Fuhrman JA (1993) Calibrating estimates of phage-induced mortality in marine bacteria: ultrastructural studies of marine bacteriophage development from one-step growth experiments. Microb Ecol 25:161-182
34. Reckermann M, Veldhuis MJW (1997) Trophic interactions between picophytoplankton and micro- and nanozooplankton in the western Arabian Sea during the NE monsoon 1993. Aquat Microb Ecol 12:263-273
35. Richmond C, Marcus NH, Sedlacek C, Miller GA, Oppert C (2006) Hypoxia and seasonal temperature: short-term effects and long-term implications for Acartia tonsa Dana. J Exp Mar Biol Ecol 328:177-196
36. Roman MR, Gauzens AL, Rhinehard WK, White JR (1993) Effect of low oxygen waters on Chesapeake Bay zooplankton. Limnol Oceanogr 38:1603-1614
37. Scavia D, Laird GA (1987) Bacterioplankton in Lake Michigan: dynamics, controls, and significance to carbon flux. Limnol Oceanogr 32:1017-1033
38. Scavia D, Lang GA, Kitchell JF (1988) Dynamics of Lake Michigan plankton: a model evaluation of nutrient loading, competition and predation. Can J Fish Aquat Sci 45:165-177
39. Setala O (1991) Ciliates in the anoxic deep-water layer of the Baltic. Arch Hydrobiol 122:483-492
40. Sherr EB, Sherr BF (2002) Significance of predation by protests in aquatic microbial food webs. Antonie Leeuwenhoek 81:293-308
41. Sherr EB, Caron DA, Sherr BF (1993) Staining of heterotrophic protists for visualization via epifluorescence microscopy. In: Kemp PF, Sherr BF, Sherr EB, Cole JJ (eds) Aquatic microbial ecology. Lewis Publishers, Boca Raton, FL, p 213-227
42. Šimek K, Pernthaler J, Weinbauer MG, Hornak K and others (2001) Changes in bacterial community composition and dynamics and viral mortality rates associated with enhanced flagellate grazing in a mesoeutrophic reservoir Appl Environ Microbiol 67: 2723-2733
43. Twiss MR, Campbell PGC, Auclair JC (1996) Regeneration, recycling, and trophic transfer of trace metals by microbial food-web organisms in the pelagic surface waters of Lake Erie. Limnol Oceanogr 41:1425-1437
44. Weinbauer MG, Höfle MG (1998) Significance of viral lysis and flagellate grazing as controlling factors of bacterioplankton production in a eutrophic lake. Appl Environ Microbiol 64:431-438
45. Weinbauer MG, Suttle CA (1996) Potential significance of lysogeny to bacteriophage production and bacterial mortality in coastal waters of the Gulf of Mexico. Appl Environ Microbiol 62:4374-4380
46. Weinbauer MG, Winter C, Höfle MG (2002) Reconsidering transmission electron microscopy based estimates of viral infection of bacterioplankton using conversion factors derived from natural communities. Aquat Microb Ecol 27:103-110
47. Weinbauer MG, Hornak K, Jezbera J, Nedoma J, Dolan JR, Šimek K (2007) Synergistic and antagonistic effects of viral lysis and protistan grazing on bacterial biomass, production and diversity. Environ Microbiol 9:777-788
48. Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39:1985-1992
49. Wilhelm SW, Smith REH (2000) Bacterial carbon production in Lake Erie is influenced by viruses and solar radiation. Can J Fish Aquat Sci 57:317-326
50. Wilhelm SW, Suttle CA (1999) Viruses and nutrient cycles in the sea. Bioscience 49:781-788
51. Wilhelm SW, Weinbauer MG, Suttle CA, Jeffrey WH (1998) The role of sunlight in the removal and repair of viruses in the sea. Limnol Oceanogr 43:586-592
52. Wilhelm SW, Jeffrey WH, Dean AL, Meador J, Pakulski JD, Mitchell DL (2003) UV radiation induced DNA damage in marine viruses along a latitudinal gradient in the southeastern Pacific Ocean. Aquat Microb Ecol 31:1-8
53. Wilhelm SW, Bullerjahn GS, Eldridge ML, Rinta-Kanto JM, Poorvin L, Bourbonniere RA (2006) Seasonal hypoxia and the genetic diversity of prokaryote populations in the central basin hypolimnion of Lake Erie: evidence for abundant cyanobacteria and photosynthesis. J Gt Lakes Res 32:657-671