Virus-bacterium coupling driven by both turbidity and hydrodynamics in an Amazonian floodplain lake

Applied and Environmental Microbiology

Volumn 76, Issue 21, 2010, Pages 7194-7201

  Barros, Nathan ^a   Farjalla, Vinicius F ^b   Soares, Maria C ^a   Melo, Rossana C N ^a   Roland, Fábio ^a  

^a FEDERAL UNIVERSITY OF JUIZ DE FORA   (Brazil)

^b Laboratory of Limnology   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

AQUATIC ECOSYSTEM; BACTERIAL ABUNDANCE; BIOLOGICAL SUBSTRATES; CHLOROPHYLL A; CLOSE COUPLING; DISSOLVED ORGANIC CARBON; FLOODPLAIN LAKES; FRESHWATER ECOSYSTEM; HIGH WATER; INFECTED CELLS; LIGHT DISTRIBUTION; LOW WATER; PHYSICAL PROCESS; PLANKTONIC COMMUNITY; QUANTITATIVE ANALYSIS; TEM; VIRAL INFECTIONS; VIRUS-LIKE PARTICLES;

BACTERIA; BACTERIOLOGY; BACTERIOPHAGES; CHLOROPHYLL; LAKES; ORGANIC CARBON; PORPHYRINS; TRANSMISSION ELECTRON MICROSCOPY; TURBIDITY;

ECOSYSTEMS;

FRESH WATER;

ABUNDANCE; BACTERIUM; DISSOLVED ORGANIC CARBON; FLOODPLAIN; FRESHWATER ECOSYSTEM; HOST-PATHOGEN INTERACTION; HYDRODYNAMICS; INFECTIOUS DISEASE; LIGHT AVAILABILITY; PLANKTON; TURBIDITY; VIRUS;

ARTICLE; BACTERIOPHAGE; BACTERIUM; BRAZIL; ECOSYSTEM; HYDRODYNAMICS; MICROBIOLOGY; PHOTOMETRY; PHYSIOLOGY; RIVER; TRANSMISSION ELECTRON MICROSCOPY; VIROLOGY;

BACTERIA; BACTERIOPHAGES; BRAZIL; ECOSYSTEM; FRESH WATER; HYDRODYNAMICS; MICROSCOPY, ELECTRON, TRANSMISSION; NEPHELOMETRY AND TURBIDIMETRY; RIVERS; WATER MICROBIOLOGY;

AMAZONIA; BRAZIL; LAKE BATATA; PARA [BRAZIL];

BACTERIA (MICROORGANISMS);

EID: 78149424253     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01161-10     Document Type: Article

References (57)

1. Amado, A. M., J. B. Cotner, A. L. Suhett, F. Assis Esteves, R. L. Bozelli, and V. F. Farjalla. 2007. Contrasting interactions mediate dissolved organic matter decomposition in tropical aquatic ecosystems. Aquat. Microb. Ecol. 49: 25-34.
2. Amado, A. M., F. F. Vinicius, A. E. Francisco de, L. B. Reinaldo, R. Fábio, and E.-P. Alex. 2006. Complementary pathways of dissolved organic carbon removal pathways in clear-water Amazonian ecosystems: Photochemical degradation and bacterial uptake. FEMS Microbiol. Ecol. 56:8-17.
3. Ammann, A., H. Neve, A. Geis, and K. J. Heller. 2008. Plasmid transfer via transduction from Streptococcus thermophilus to Lactococcus lactis. J. Bacteriol. 190:3083-3087.
4. Amon, R. M. W., and R. Benner. 1996. Bacterial utilization of different size classes of dissolved organic matter. Limnol. Oceanogr. 41:41-51.
5. Anesio, A. M., P. C. Abreu, and F. D. Esteves. 1997. Influence of the hydrological cycle on the bacterioplankton of an impacted clear water Amazonian lake. Microb. Ecol. 34:66-73.
6. Bettarel, Y., M. Bouvy, C. Dumont, and T. Sime-Ngando. 2006. Virus-bacterium interactions in water and sediment of West African inland aquatic systems. Appl. Environ. Microbiol. 72:5274-5282.
7. Bozelli, R. L. 1996. The influence of bauxite tailings on the cladoceran populations of Lake Batata, Amazonia, Brazil. Int. Rev. Gesamten Hydrobiol. 81:621-634.
8. Bozelli, R. L. 1998. Influences of suspended inorganic matter on carbon ingestion and incorporation rates of two tropical cladocerans, Diaphanosoma birgei and Moina minuta. Arch. Hydrobiol. 142:451-465.
9. Bozelli, R. L. 1994. Zooplankton community density in relation to waterlevel fluctuations and inorganic turbidity in an Amazonian lake, Lago- Batata, state of Para, Brazil. Amazoniana-Limnol. Oecol. Region. Syst. Fluminis Amazonas 13:17-32.
10. Bozelli, R. L., A. Caliman, R. D. Guariento, L. S. Carneiro, J. M. Santangelo, M. P. Figueiredo-Barros, J. J. F. Leal, A. M. Rocha, L. B. Quesado, P. M. Lopes, V. F. Farjalla, C. C. Marinho, F. Roland, and F. A. Esteves. 2009. Interactive effects of environmental variability and human impacts on the long-term dynamics of an Amazonian floodplain lake and a South Atlantic coastal lagoon. Limnologica 39:306-313.
11. Bratbak, G., and M. Heldal. 2000. Viruses rule the waves-the smallest and most abundant members of marine ecosystems. Microbiol. Today 27:171-173.
12. Brussaard, C. P. D. 2004. Viral control of phytoplankton populations-a review. J. Eukaryot. Microbiol. 51:125-138.
13. Burnham, K. P., and D. Anderson. 2002. Model selection and multimodel inference: A practical information-theoretic approach, 2nd ed. Springer- Verlag, New York, NY.
14. Cotner, J. B., and B. A. Biddanda. 2002. Small players, large role: Microbial influence on biogeochemical processes in pelagic aquatic ecosystems. Ecosystems 5:105-121.
15. de Melo, S., and V. L. M. Huszar. 2000. Phytoplankton in an Amazonian flood-plain lake (Lago Batata, Brasil): Diel variation and species strategies. J. Plankton Res. 22:63-76.
16. Deng, L., and P. K. Hayes. 2008. Evidence for cyanophages active against bloom-forming freshwater cyanobacteria. Freshwater Biol. 53:1240-1252.
17. Evans, T. J., M. A. Crow, N. R. Williamson, W. Orme, N. R. Thomson, E. Komitopoulou, and G. P. C. Salmond. 2010. Characterization of a broadhost- range flagellum-dependent phage that mediates high-efficiency generalized transduction in, and between, Serratia and Pantoea. Microbiology 156:240-247.
18. Farjalla, V. F., D. A. Azevedo, F. A. Esteves, R. L. Bozelli, F. Roland, and A. Enrich-Prast. 2006. Influence of hydrological pulse on bacterial growth and DOC uptake in a clear-water Amazonian lake. Microb. Ecol. 52:334-344.
19. Farjalla, V. F., F. A. Esteves, R. L. Bozelli, and F. Roland. 2002. Nutrient limitation of bacterial production in clear water Amazonian ecosystems. Hydrobiologia 489:197-205.
20. Filippini, M., N. Buesing, Y. Bettarel, T. Sime-Ngando, and M. O. Gessner. 2006. Infection paradox: High abundance but low impact of freshwater benthic viruses. Appl. Environ. Microbiol. 72:4893-4898.
21. Fuhrman, J. A. 1999. Marine viruses and their biogeochemical and ecological effects. Nature 399:541-548.
22. Fuhrman, J. A., and R. T. Noble. 1995. Viruses and protists cause similar bacterial mortality in coastal seawater. Limnol. Oceanogr. 40:1236-1242.
23. Heissenberger, A., G. G. Leppard, and G. J. Herndl. 1996. Relationship between the intracellular integrity and the morphology of the capsular envelope in attached and free-living marine bacteria. Appl. Environ. Microbiol. 62:4521-4528.
24. Huszar, V. L. M., and C. S. Reynolds. 1997. Phytoplankton periodicity and sequences of dominance in an Amazonian flood-plain lake (Lago Batata, Pará, Brasil): Responses to gradual environmental change. Hydrobiologia 346:169-181.
25. Junk, W. J., P. B. Bayley, and R. E. Sparks. 1989. The flood pulse concept in river-floodplain system. Can. Spec. Publ. Fish Aquat. Sci. 106:110-127.
26. Kepner, R. L., R. A. Wharton, and C. A. Suttle. 1998. Viruses in antartic lakes. Limnol. Oceanogr. 43:1754-1761.
27. Lapa, R. P. 2000. A bauxita e o rejeito de bauxita, p. 25-36. In F. R. Bozelli, F. A. Esteves, and F. Roland (ed.), Lago Batata: Impacto e recuperação de um ecossistema amazǒnico. IB-UFRJ/ Sociedade Brasileira de Limnologia, Rio de Janeiro, RJ, Brazil.
28. 2 uptake and bacterioplankton production in experimental microcosms with sediment-water interface of an Amazonian lake impacted by bauxite tailings. Int. Rev. Hydrobiol. 88: 167-178.
29. Lorenzen, C. J. 1967. Determination of chlorophyll and phaeopigments: Spectrophotometric equations. Limnol. Oceanogr. 12:342-345.
30. Madan, N. J., W. A. Marshall, and J. Laybourn-Parry. 2005. Virus and microbial loop dynamics over an annual cycle in three contrasting Antarctic lakes. Freshwater Biol. 50:1291-1300.
31. Maranger, R., and D. F. Bird. 1995. Viral abundance in aquatic systems-a comparison between marine and fresh-waters. Mar. Ecol. Progr. Ser. 121: 217-226.
32. Maranger, R., D. F. Bird, and S. K. Juniper. 1994. Viral and bacterial dynamics in arctic sea-ice during the spring algal bloom near Resolute, NWT, Canada. Mar. Ecol. Progr. Ser. 111:121-127.
33. Maranger, R., P. A. del Giorgio, and D. F. Bird. 2002. Accumulation of damaged bacteria and viruses in lake water exposed to solar radiation. Aquat. Microb. Ecol. 28:213-227.
34. Mathias, C. B., A. K. T. Kirschner, and B. Velimirov. 1995. Seasonal-variations of virus abundance and viral control of the bacterial production in a backwater system of the Danube River. Appl. Environ. Microbiol. 61:3734-3740.
35. Melo, R. C. N., L. A. Spencer, S. A. C. Perez, I. Ghiran, A. M. Dvorak, and P. F. Weller. 2005. Human eosinophils secrete preformed, granule-stored interleukin-4 through distinct vesicular compartments. Traffic 6:1047-1057.
36. Noble, R. T., and J. A. Fuhrman. 1998. Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat. Microb. Ecol. 14:113-118.
37. Noble, R. T., and J. A. Fuhrman. 1997. Viral decay and its causes in coastal waters. Appl. Environ. Microbiol. 63:77-83.
38. Patel, A., R. T. Noble, J. A. Steele, M. S. Schwalbach, I. Hewson, and J. A. Fuhrman. 2007. Virus and prokaryote enumeration from planktonic aquatic environments by epifluorescence microscopy with SYBR Green I. Nat. Protoc. 2:269-276.
39. Peduzzi, P., and F. Schiemer. 2004. Bacteria and viruses in the water column of tropical freshwater reservoirs. Environ. Microbiol. 6:707-715.
40. Proctor, L. M., and J. A. Fuhrman. 1992. Mortality of marine bacteria in response to enrichments of the virus size fraction from seawater. Mar. Ecol. Progr. Ser. 87:283-293.
41. Proctor, L. M., A. Okubo, and J. A. Fuhrman. 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.
42. Rangel, T. F. L. V. B., J. A. F. Diniz-Filho, and L. M. Bini. 2006. Towards an integrated computational tool for spatial analysis in macroecology and biogeography. Global Ecol. Biogeogr. 15:321-327.
43. Roland, F., and F. D. Esteves. 1998. Effects of bauxite tailing on PAR attenuation in an Amazonian crystalline water lake. Hydrobiologia 377:1-7.
44. Roland, F., F. D. Esteves, and F. A. R. Barbosa. 2002. Relationship between antropogenically caused turbidity and phytoplankton production in a clear Amazonian floodplain lake. Amazoniana-Limnol. Oecol. Region. Syst. Fluminis Amazonas 17:65-77.
45. Roland, F., L. M. Lobão, L. O. Vidal, E. Jeppesen, R. Paranhos, and V. Huszar. 2010. Relationships between pelagic bacteria and phytoplankton abundances in contrasting tropical freshwaters. Aquat. Microb. Ecol. 60:261-272.
46. Säwström, C., W. Graneli, J. Laybourn-Parry, and A. M. Anesio. 2007. High viral infection rates in Antarctic and Arctic bacterioplankton. Environ. Microbiol. 9:250-255.
47. Sioli, H. 1984. The Amazon. D. W. J. Publishers, Dordrecht, Netherlands.
48. Suttle, C. A. 1994. The significance of viruses to mortality in aquatic microbial communities. Microb. Ecol. 28:237-243.
49. Suttle, C. A. 2005. Viruses in the sea. Nature 437:356-361.
50. Weinbauer, M. G. 2004. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 28:127-181.
51. Weinbauer, M. G., and M. G. Hofle. 1998. Size-specific mortality of lake bacterioplankton by natural virus communities. Aquat. Microb. Ecol. 15: 103-113.
52. Weinbauer, M. G., and C. A. Suttle. 1997. Comparison of epifluorescence and transmission electron microscopy for counting viruses in natural marine waters. Aquat. Microb. Ecol. 13:225-232.
53. Wetzel, R. G., and G. E. Likens. 1991. Limnological analyses, 2nd ed. Springer- Verlag, New York, NY.
54. Wilhelm, S. W., and R. E. H. Smith. 2000. Bacterial carbon production in Lake Erie is influenced by viruses and solar radiation. Can. J. Fish. Aquat. Sci. 57:317-326.
55. Wilhelm, S. W., and C. A. Suttle. 1999. Viruses and nutrient cycles in the sea-viruses play critical roles in the structure and function of aquatic food webs. Bioscience 49:781-788.
56. Wilhelm, S. W., M. G. Weinbauer, C. A. Suttle, and W. H. Jeffrey. 1998. The role of sunlight in the removal and repair of viruses in the sea. Limnol. Oceanogr. 43:586-592.
57. Wommack, K. E., R. T. Hill, T. A. Muller, and R. R. Colwell. 1996. Effects of sunlight on bacteriophage viability and structure. Appl. Environ. Microbiol. 62:1336-1341.