Dynamics of natural prokaryotes, viruses, and heterotrophic nanoflagellates in alpine karstic groundwater

MicrobiologyOpen

Volumn 2, Issue 4, 2013, Pages 633-643

  Wilhartitz, Inés C ^a   Kirschner, Alexander K T ^b,c   Brussaard, Corina P D ^d,e   Fischer, Ulrike R ^b   Wieltschnig, Claudia ^b   Stadler, Hermann ^f   Farnleitner, Andreas H ^c,g  

^a SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c Interuniversity Cooperation Center Water and Health   (Austria)

^d ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

^e UNIVERSITY OF AMSTERDAM   (Netherlands)

^f JOANNEUM RESEARCH   (Austria)

^g Institute of Biochemical Engineering   (Austria)

Author keywords

Alpine karst; Groundwater; Heterotrophic nanoflagellates; Prokaryotes; Viruses

Indexed keywords

GROUND WATER;

AQUATIC ENVIRONMENT; ARTICLE; FLAGELLATE; HETEROTROPHY; HYDROLOGY; MICROBIAL BIOMASS; MICROBIAL COMMUNITY; MICROBIOLOGY; MORPHOTYPE; NONHUMAN; POPULATION ABUNDANCE; POPULATION DYNAMICS; PRIORITY JOURNAL; PROKARYOTE; VIRUS; WATER ANALYSIS; WATER QUALITY;

ALPINE KARST; GROUNDWATER; HETEROTROPHIC NANOFLAGELLATES; PROKARYOTES; VIRUSES;

BACTERIAL LOAD; BIOTA; GROUNDWATER; PARASITE LOAD; SEASONS; VIRAL LOAD;

PROKARYOTA;

EID: 84897115217     PISSN: None     EISSN: 20458827     Source Type: Journal    
DOI: 10.1002/mbo3.98     Document Type: Article

References (62)

1. Baltar, F., J. Aristegui, J. M. Gasol, and G. J. Herndl . 2012. Microbial functioning and community structure variability in the mesopelagic and epipelagic waters of the subtropical northeast atlantic ocean. Appl. Environ. Microbiol. 78:3309-3316.
2. Blenkinsopp, S. A., and M. A. Lock . 1994. The impact of storm flow on river biofilm architecture. J. Phycol. 30:807-818.
3. Borsheim, 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.
4. Bouvier, T., and C. F. Maurice . 2011. A Single-Cell Analysis of Virioplankton Adsorption, Infection, and Intracellular Abundance in Different Bacterioplankton Physiologic Categories. Microbial Ecol. 62:669-678.
5. Brancelj, A., and H. J. Dumont . 2007. A review of the diversity, adaptations and groundwater colonization pathways in Cladocera and Calanoida (Crustacea), two rare and contrasting groups of stygobionts. Fundam. Appl. Limnol. 168:3-17.
6. Brussaard, C. P. D. 2004. Optimization of procedures for counting viruses by flow cytometry. Appl. Environ. Microbiol. 70:1506-1513.
7. Brussaard, C. P. D., S. W. Wilhelm, F. Thingstad, M. G. Weinbauer, G. Bratbak, M. Heldal, et al. 2008. Global-scale processes with a nanoscale drive: the role of marine viruses. ISME J. 2:575-578.
8. Chen, F., J. R. Lu, B. J. Binder, Y. C. Liu, and R. E. Hodson . 2001. Application of digital image analysis and flow cytometry to enumerate marine viruses stained with SYBR gold. Appl. Environ. Microbiol. 67:539-545.
9. Cho, J. C., and S. J. Kim . 2000. Increase in bacterial community diversity in subsurface aquifers receiving livestock wastewater input. Appl. Environ. Microbiol. 66:956-965.
10. D'Amore, F., G. Scandiffio, and C. Panichi . 1983. Some observations on the chemical classification of ground water. Geothermics 12:141-148.
11. Deng, L., A. Gregory, S. Yilmaz, B. T. Poulos, P. Hugenholtz, and M. B. Sullivan . 2012. Contrasting life strategies of viruses that infect photo- and heterotrophic bacteria, as revealed by viral tagging. MBio. 3:e00373-12.
12. Drew, D., and H. Hötzl . 1999. Karst hydrogeology and human activities: impacts, consequences and implications. Vol. 20. IAH International Contributions to Hydrogeology, Brookfield, VT.
13. Farnleitner, A. H., G. Ryzinska-Paier, G. H. Reischer, M. M. Burtscher, S. Knetsch, S. Rudnicki, et al. 2010. Escherichia coli and enterococci are sensitive and reliable indicators for human, livestock, and wild life faecal pollution in alpine mountainous water resources. J. Appl. Microbiol. 109:1599-1608.
14. Farnleitner, A. H., I. Wilhartitz, A. K. T. Kirschner, H. Stadler, M. M. Burtscher, R. Hornek, et al. 2005. Bacterial dynamics in spring water of alpine karst aquifers indicates the presence of stable autochthonous microbial endokarst communities. Environ. Microbiol. 7:1248-1259.
15. Fischer, U. R., A. K. T. Kirschner, and B. Velimirov . 2005. Optimization of extraction and estimation of viruses in silty freshwater sediments. Aquat. Microb. Ecol. 40:207-216.
16. Ford, D. C., and P. W. Williams . 1996. Karst geomorphology and hydrology. Chapman and Hall, London.
17. Ford, D. C., and P. W. Williams . 2007. Karst geomorphology and hydrology. Chapman and Hall, London.
18. Galassi, D. M. P., F. Stoch, B. Fiasca, T. Di Lorenzo, and E. Gattone . 2009. Groundwater biodiversity patterns in the Lessinian Massif of northern Italy. Freshw. Biol. 54:830-847.
19. Gasol, J. M. 1994. A framework for the assessment of top-down vs bottom-up control of heterotrophic nanoflagellate abundance. Mar. Ecol. Prog. Ser. 113:291-300.
20. Gasol, J. M., C. Pedrós-Alió, and D. Vaqué . 2002. Regulation of bacterial assemblages in oligotrophic plancton systems: results from experimental and empirical approaches. Antonie Van Leeuwenhoek 81:435-452.
21. Gibert, J., and D. C. Culver . 2009. Assessing and conserving groundwater biodiversity: an introduction. Freshw. Biol. 54:639-648.
22. Gibert, J., D. C. Culver, M. J. Dole-Olivier, F. Malard, M. C. Christman, and L. Deharveng . 2009. Assessing and conserving groundwater biodiversity: synthesis and perspectives. Freshw. Biol. 54:930-941.
23. Goddard, V. J., A. C. Baker, J. E. Davy, D. G. Adams, M. M. De Ville, S. J. Thackeray, et al. 2005. Temporal distribution of viruses, bacteria and phytoplankton throughout the water column in a freshwater hypereutrophic lake. Aquat. Microb. Ecol. 39:211-223.
24. Gordon, C., and S. Toze . 2003. Influence of groundwater characteristics on the survival of enteric viruses. J. Appl. Microbiol. 95:536-544.
25. Hobbie, J. E., R. J. Daley, and S. Jasper . 1977. Use of nucleopore filters for counting bacteria by fluorescence microscopy. Appl. Environ. Microbiol. 33:1225-1228.
26. Husman, A. M. D. R., W. J. Lodder, S. A. Rutjes, J. F. Schijven, and P. F. M. Teunis . 2009. Long-term inactivation study of three enteroviruses in artificial surface and groundwaters, using PCR and cell culture. Appl. Environ. Microbiol. 75:1050-1057.
27. John, D. E., and J. B. Rose . 2005. Review of factors affecting microbial survival in groundwater. Environ. Sci. Technol. 39:7345-7356.
28. Kjelleberg, S. 1993. Starvation in bacteria. Plenum Press, New York, NY.
29. Lehman, R. M., F. S. Colwell, and G. A. Bala . 2001a. Attached and unattached microbial communities in a simulated basalt aquifer under fracture- and porous-flow conditions. Appl. Environ. Microbiol. 67:2799-2809.
30. Lehman, R. M., F. F. Roberto, D. Earley, D. F. Bruhn, S. E. Brink, S. P. O'connell, et al. 2001b. Attached and unattached bacterial communities in a 120-meter corehole in an acidic, crystalline rock aquifer. Appl. Environ. Microbiol. 67:2095-2106.
31. Lucena, F., F. Ribas, A. E. Duran, S. Skraber, C. Gantzer, C. Campos, et al. 2006. Occurrence of bacterial indicators and bacteriophages infecting enteric bacteria in groundwater in different geographical areas. J. Appl. Microbiol. 101:96-102.
32. Marie, D., C. P. D. Brussaard, R. Thyrhaug, G. Bratbak, and D. Vaulot . 1999. Enumeration of marine viruses in culture and natural samples by flow cytometry. Appl. Environ. Microbiol. 65:45-52.
33. Morita, R.Y. 1997. Bacteria in oligotrophic environments. Chapman and Hall, London, U.K.
34. Noble, R. T. 2001. Enumeration of viruses. Method Microbiol. 30:43-50.
35. Novarino, G., A. Warren, H. Butler, G. Lambourne, A. Boxshall, J. Bateman, et al. 1997. Protistan communities in aquifers: a review. FEMS Microbiol. Rev. 20:261-275.
36. Pronk, M., N. Goldscheider, and J. Zopfi . 2006. Dynamics and interaction of organic carbon, turbidity and bacteria in a karst aquifer system. Hydrogeol. J. 14:473-484.
37. Pronk, M., N. Goldscheider, and J. Zopfi . 2009a. Microbial communities in karst groundwater and their potential use for biomonitoring. Hydrogeol. J. 17:37-48.
38. Pronk, M., N. Goldscheider, J. Zopfi, and F. Zwahlen . 2009b. Percolation and particle transport in the unsaturated zone of a karst aquifer. Ground Water 47:361-369.
39. Reischer, G., D. Kasper, R. Steinborn, R. Mach, and A. Farnleitner . 2006. Quantitative PCR method for sensitive detection of ruminant fecal pollution in freshwater and evaluation of this method in alpine karstic regions. Appl. Environ. Microbiol. 72:5610-5614.
40. Reischer, G., D. C. Kasper, R. Steinborn, A. H. Farnleitner, and R. L. Mach . 2007. A quantitative real-time PCR assay for the highly sensitive and specific detection of human feacal influence in spring water from a large alpine catchment area. Lett. Appl. Microbiol. 44:351-356.
41. Rouch, R. 1977. Karst as an ecosystem. Comptes Rendus Hebdomadaires Des Seances De L Academie Des Sciences Serie D 284:1101-1103.
42. Roudnew, B., T. J. Lavery, J. R. Seymour, R. J. Smith, and J. G. Mitchell . 2013. Spatially varying complexity of bacteria and virus-like particle communities within an aquifer system. Aquat. Microb. Ecol. 68:259-266.
43. Säwström, C., M. A. Anesio, W. Granéli, and J. Laybourn-Parry . 2006. Seasonal viral loop dynamics in two large ultraoligotrophic antarctic freshwater lakes. Microb. Ecol. 53:1-11.
44. Sherr, B. F., E. B. Sherr, and J. Mcdaniel . 1992. Effect of protistan grazing on the frequency of dividing cells in bacterioplankton assemblages. Appl. Environ. Microbiol. 58:2381-2385.
45. Sibbald, M. J., and L. J. Albright . 1988. Aggregated and free bacteria as food sources for heterotrophic microflagellates. Appl. Environ. Microbiol. 54:613-616.
46. Simek, K., J. Armengol, M. Comerma, J. C. Garcia, P. Kojecka, J. Nedoma, et al. 2001. Changes in the epilimnetic bacterial community composition, production, and protist-induced mortality along the longitudinal axis of a highly eutrophic reservoir. Microb. Ecol. 42:359-371.
47. Simon, K. S., J. Ginert, P. Petitot, and R. Laurent . 2001. Spatial and temporal patterns of bacterial densitiy and metabolic activity in karst. Arch. Hydrobiol. 151:67-82.
48. Stadler, H., and E. Strobl. 1997. Karstwasserdynamik Zeller Staritzen (in German). Endbericht Joanneum für MA31 Stadt Wien, 171.
49. Stadler, H., Strobl, E . 1998. Karstwasserdynamik und Karstwasserschutz Hochschwab STA 28K/96 (in German). Endbericht 2. Arbeitsjahr im Auftrag MA31 Stadt Wien.
50. Starink, M., I. N. Krylova, M. J. Bargilissen, R. P. M. Bak, and T. E. Cappenberg . 1994. Rates of benthic protozoan grazing on free and attached sediment bacteria measured with fluorescently stained sediment. Appl. Environ. Microbiol. 60:2259-2264.
51. Suttle, C. A. 2005. Viruses in the sea. Nature 437:356-361.
52. Suttle, C. A. 2007. Marine viruses-major players in the global ecosystem. Nat. Rev. 5:801-812.
53. Vazquez-Dominguez, E., J. M. Gasol, S. Agusti, C. M. Duarte, and D. Vaque . 2005. Growth and grazing losses of prokaryotes in the central Atlantic Ocean. J. Plankton Res. 27:1055-1066.
54. Vazquez-Dominguez, E., C. M. Duarte, S. Agusti, K. Jurgens, D. Vaque, and J. M. Gasol . 2008. Microbial plankton abundance and heterotrophic activity across the Central Atlantic Ocean. Prog. Oceanogr. 79:83-94.
55. Weinbauer, M. G., and F. Rassoulzadegan . 2004. Are viruses driving microbial diversification and diversity? Environ. Microbiol. 6:1-11.
56. Weinbauer, M. G., I. Brettar, and M. G. Hofle . 2003. Lysogeny and virus-induced mortality of bacterioplankton in surface, deep, and anoxic marine waters. Limnol. Oceanogr. 48:1457-1465.
57. Wieltschnig, C., A. K. T. Kirschner, A. Steitz, and B. Velimirov . 2001. Weak coupling between heterotrophic nanoflagellates and bacteria ina eutrophic freshwater environment. Microb. Ecol. 42:159-167.
58. Wieltschnig, C., U. R. Fischer, A. K. T. Kirschner, and B. Velimirov . 2003. Benthic bacterial production and protozoan predation in a silty freshwater environment. Microb. Ecol. 46:62-72.
59. Wilhartitz, I. C., A. K. T. Kirschner, H. Stadler, G. J. Herndl, R. L. Mach, and A. H. Farnleitner . 2009. Heterotrophic prokaryotic production in ultra-oligotrophic alpine karst aquifers and ecological implications. FEMS Microbiol. Ecol. 68:287-299.
60. Wilhelm, S. W., and C. A. Suttle . 1999. Viruses and nutrient cycles in the sea. Bioscience 49:781-788.
61. Williamson, S. J., L. A. Houchin, L. Mcdaniel, and J. H. Paul . 2002. Seasonal variation in lysogeny as depicted by prophage induction in Tampa Bay, Florida. Appl. Environ. Microbiol. 68:4307-4314.
62. Wommack, K. E., and R. R. Colwell . 2000. Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64:69-114.