Phagotrophic protist diversity in the groundwater of a karstified aquifer - Morphological and molecular analysis

Journal of Eukaryotic Microbiology

Volumn 60, Issue 5, 2013, Pages 467-479

  Risse Buhl, Ute ^a,b   Herrmann, Martina ^a   Lange, Patricia ^a   Akob, Denise M ^a,c   Pizani, Natalia ^a,d   Schönborn, Wilfried ^a   Totsche, Kai Uwe ^a   Küsel, Kirsten ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b BRANDENBURG UNIVERSITY OF TECHNOLOGY   (Germany)

^c U S GEOLOGICAL SURVEY   (United States)

^d UNIVERSIDAD NACIONAL DEL SUR   (Argentina)

Author keywords

Ciliates; cloning; flagellates; limestone; micro eukaryotes; naked amoebae; qPCR; sequencing

Indexed keywords

ABUNDANCE; AQUIFER; CILIATE; CLONE; FOOD WEB; GENE; GROUNDWATER; LIMESTONE; METAZOAN; MOLECULAR ANALYSIS; POLYMERASE CHAIN REACTION; PROTIST; SPECIES DIVERSITY; SWIMMING;

GERMANY; THURINGIAN BASIN;

AMOEBA (GENUS); ANIMALIA; BACTERIA (MICROORGANISMS); CILIOPHORA; EUKARYOTA; FUNGI; HARTMANNELLA; MASTIGOPHORA (FLAGELLATES); METAZOA; MONOSIGA; PROTISTA; SPUMELLA; STRAMENOPILES; VAHLKAMPFIA; VANNELLA;

GROUND WATER; LIMESTONE; PROTOZOAL DNA; PROTOZOAL RNA; RIBOSOME DNA; RNA 18S;

ARTICLE; BIODIVERSITY; CHEMISTRY; CILIATES; CLASSIFICATION; CLONING; CLUSTER ANALYSIS; DNA SEQUENCE; EUKARYOTE; FLAGELLATES; GENETICS; GERMANY; ISOLATION AND PURIFICATION; MICRO-EUKARYOTES; MICROSCOPY; MOLECULAR GENETICS; NAKED AMOEBAE; NUCLEOTIDE SEQUENCE; PARASITE LOAD; PARASITOLOGY; PHYLOGENY; QPCR; RNA GENE; SEQUENCING;

CILIATES; CLONING; FLAGELLATES; LIMESTONE; MICRO-EUKARYOTES; NAKED AMOEBAE; QPCR; SEQUENCING;

BIODIVERSITY; CLUSTER ANALYSIS; DNA, PROTOZOAN; DNA, RIBOSOMAL; EUKARYOTA; GENES, RRNA; GERMANY; GROUNDWATER; MICROSCOPY; MOLECULAR SEQUENCE DATA; PARASITE LOAD; PHYLOGENY; RNA, PROTOZOAN; RNA, RIBOSOMAL, 18S; SEQUENCE ANALYSIS, DNA;

EID: 84884166544     PISSN: 10665234     EISSN: 15507408     Source Type: Journal    
DOI: 10.1111/jeu.12054     Document Type: Article

References (73)

1. Adl, S. M., Simpson, A. G. B., Lane, C. E., Lukes, J., Bass, D., Bowser, S. S., Brown, M. W., Burki, F., Dunthorn, M., Hampl, V., Heiss, A., Hoppenrath, M., Lara, E., le Gall, L., Lynn, D. H., McManus, H., Mitchell, E. A. D., Mozley-Stanridge, S. E., Parfrey, L. W., Pawlowski, J., Rueckert, S., Shadwick, L., Schoch, C. L., Smirnov, A., &, Spiegel, F. W., 2012. The revised classification of eukaryotes. J. Eukaryot. Microbiol., 59: 429-493.
2. Adl, S. M., Simpson, A. G. B., Farmer, M. A., Andersen, R. A., Anderson, O. R., Barta, J. R., Browser, S. S., Brugerolle, G., Fensome, R. A., Fredericq, S., James, T. Y., Karpov, S., Kugrens, P., Krug, J., Lane, C. E., Lewis, L. A., Lodge, J., Lynn, D. H., Mann, D. G., McCourt, R. M., Mendoza, L., Moestrup, O., Mozley-Standridge, S. E., Nerad, T. A., Shearer, C. A., Smirnov, A. V., Spiegel, F. W., &, Taylor, M., 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol., 52: 399-451.
3. Akob, D. M., &, Küsel, K., 2011. Where microorganisms meet rocks in the earth's critical zone. Biogeosciences, 8: 2523-2562.
4. Azam, F., Fenchel, T., Field, J. G., Gray, J. S., Meyer-Reil, L. A., &, Thingstad, F., 1983. The ecological role of water-column microbes in the sea. Mar. Ecol.-Prog Ser., 10: 257-263.
5. Berney, C., Fahrni, J., &, Pawlowski, J., 2004. How many novel eukaryotic 'kingdoms'? Pitfalls and limitations of environmental DNA surveys. BMC Biol., 2: 1-13.
6. Bert, W., Manhout, J., Van Colen, C., Borgonie, G., &, Decraemer, W., 2009. Nematode assemblages in a nature reserve with historical pollution. Belg. J. Zool., 139: 3-14.
7. Boenigk, J., &, Arndt, H., 2002. Bacterivory by heterotrophic flagellates: community structure and feeding strategies. Anton. Leeuw. Int. J. G., 81: 465-480.
8. Boenigk, J., Pfandl, K., Stadler, P., &, Chatzinotas, A., 2005. High diversity of the 'Spumella-like' flagellates: an investigation based on the SSU rRNA gene sequences of isolates from habitats located in six different geographic regions. Environ. Microbiol., 7: 685-697.
9. Boulton, A. J., Humphreys, W. F., &, Eberhard, S. M., 2003. Imperilled subsurface waters in Australia: biodiversity, threatening processes and conservation. Aquat. Ecosyst. Health, 6: 41-54.
10. Buonanno, F., 2011. The changes in the predatory behavior of the microturbellarian Stenostomum sphagnetorum on two species of toxin-secreting ciliates of the genus Spirostomum. Biologia, 66: 648-653.
11. Buonanno, F., Guella, G., Strim, C., &, Ortenzi, C., 2012. Chemical defence by mono-prenyl hydroquinone in a freshwater ciliate, Spirostomum ambiguum. Hydrobiologia, 684: 97-107.
12. Butler, H., &, Rogerson, A., 1995. Temporal and spatial abundance of naked amoebas (Gymnamoebae) in marine benthic sediments of the Clyde-Sea Area, Scotland. J. Eukaryot. Microbiol., 42: 724-730.
13. del Campo, J., Not, F., Forn, I., Sieracki, M. E., &, Massana, R., 2013. Taming the smallest predators of the oceans. ISME J., 351-358.
14. Cunningham III, J. J., Kinner, N. E., &, Lewis, M., 2009. Protistan predation affects trichloroethene biodegradation in a bedrock aquifer. Appl. Environ. Microb., 75: 7588-7593.
15. DeLong, E. F., 1992. Archaea in coastal marine environments. P. Natl. Acad. Sci. USA, 89: 5685-5689.
16. Euringer, K., &, Lueders, T., 2008. An optimised PCR/T-RFLP fingerprinting approach for the investigation of protistan communities in groundwater environments. J. Microbiol. Meth., 75: 262-268.
17. Fenchel, T., 1987. Ecology of Protozoa: The Biology of Free-Living Phagotrophic Protists, 1st ed. Springer, Berlin. p. 194.
18. Fenchel, T., Finlay, B. J., &, Giannì, A., 1989. Microaerophily in ciliates: responses of an Euplotes sp. to oxygen tension. Arch. Protistenkd., 137: 317-330.
19. Finlay, B. J., &, Esteban, G. F., 2009. Oxygen sensing drives predictable migrations in a microbial community. Environ. Microbiol., 11: 81-85.
20. Foissner, W., Berger, H., &, Kohmann, F., 1994. Taxonomische und Ökologische Revision der Ciliaten des Saprobiensystems-Band III: Hymenostomata, Prostomatida, Nassulida. Bayerisches Landesamt für Wasserwirtschaft, München. p. 548.
21. Grasshoff, K., Ehrhardt, M., &, Kremling, K., 1999. Methods of Seawater Analysis, 3rd ed. Chemie, Weinheim. p. 600.
22. Griebler, C., &, Lüders, T., 2009. Microbial biodiversity in groundwater ecosystems. Freshw. Biol., 54: 649-677.
23. Güde, H., 1979. Grazing by protozoa as selection factor for activated-sludge bacteria. Microb. Ecol., 5: 225-237.
24. Guillou, L., Bachar, D., Audic, S., Bass, D., Berney, C., Bittner, L., Boutte, C., Burgaud, G., de Vargas, C., Decelle, J., Del Campo, J., Dolan, J. R., Dunthorn, M., Edvardsen, B., Holzmann, M., Kooistra, W. H., Lara, E., Le Bescot, N., Logares, R., Mahé, F., Massana, R., Montresor, M., Morard, R., Not, F., Pawlowski, J., Probert, I., Sauvadet, A. L., Siano, R., Stoeck, T., Vaulot, D., Zimmermann, P., &, Christen, R., 2013. The protist ribosomal reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acid Res., 41: D597-D604.
25. Hancock, P. J., Boulton, A. J., &, Humphreys, W. F., 2005. Aquifers and hyporheic zones: towards an ecological understanding of groundwater. Hydrogeol. J., 13: 98-111.
26. Harvey, R. W., Mayberry, N., Kinner, N. E., Metge, D. W., &, Novarino, F., 2002. Effect of growth conditions and staining procedure upon the subsurface transport and attachment behaviors of a groundwater protist. Appl. Environ. Microb., 68: 1872-1881.
27. Herrmann, M., Hädrich, A., &, Küsel, K., 2012. Predominance of thaumarchaeal ammonia oxidizer abundance and transcriptional activity in an acidic fen. Environ. Microbiol., 14: 3013-3025.
28. Hölting, B., &, Coldewey, W. G., 2009. Hydrogeologie, 7th ed. Spektrum Akademischer Verlag, München. p. 384.
29. Johnson, M., Zaretskaya, I., Raytselis, Y., Merezhuk, Y., McGinnis, S., &, Madden, T. L., 2008. NCBI BLAST: a better web interface. Nucleic Acids Res., 36: W5-W9.
30. Jürgens, K., Pernthaler, J., Schalla, S., &, Amann, R., 1999. Morphological and compositional changes in a planktonic bacterial community in response to enhanced protozoan grazing. Appl. Environ. Microb., 65: 1241-1250.
31. Kemper, K. E., 2004. Groundwater-from development to management-Preface. Hydrogeol. J., 12: 3-5.
32. Kinner, N. E., Harvey, R. W., &, Kazmierkiewicz-Tabaka, M., 1997. Effect of flagellates on free-living bacterial abundance in an organically contaminated aquifer. FEMS Microbiol. Rev., 20: 249-259.
33. Kinner, N. E., Harvey, R. W., Shay, D. M., Metge, D. W., &, Warren, A., 2002. Field evidence for a protistan role in an organically-contaminated aquifer. Environ. Sci. Technol., 36: 4312-4318.
34. Kinner, N. E., Harvey, R. W., Blakeskee, K., Novarino, G., &, Meeker, L. D., 1998. Size-selective predation on groundwater bacteria by nanoflagellates in an organic-contaminated aquifer. Appl. Environ. Microb., 64: 618-625.
35. Kota, S., Borden, R. C., &, Barlaz, M. A., 1999. Influence of protozoan grazing on contaminant biodegradation. FEMS Microbiol. Ecol., 29: 179-189.
36. Kugrens, P., &, Lee, R. E., 1991. Organization of cryptomonads. In:, Patterson, D. J., &, Larsen, J., (eds), The Biology of Free-Living Heterotrophic Flagellates. Systematics Association Special Volume no. 45. Clarndon Press, Oxford.
37. Lane, D. J., 1991. 16S/23S rRNA sequencing. In:, Stackebrandt, E., &, Goodfellow, M., (eds), Nucleic Acid Techniques in Bacterial Systematics. John Wiley and Sons, New York. p. 115-175.
38. Longnecker, K., Da Costa, A., Bhatia, M., &, Kujawinski, E. B., 2009. Effect of carbon addition and predation on acetate-assimilating bacterial cells in groundwater. FEMS Microbiol. Ecol., 70: 456-470.
39. Loquay, N., Wylezich, C., &, Arndt, H., 2009. Composition of groundwater nanoprotist communities in different aquifers based on aliquot cultivation and genotype assessment of cercomonads. Fund. Appl. Limnol., 174: 261-269.
40. Lu, S., Chourey, K., Reiche, M., Nietzsche, S., Shah, M. B., Neu, T. R., Hettich, R. L., &, Küsel, K., 2013. Insights into the structure and metabolic function of microbes that shape pelagic iron-rich aggregates (iron snow). Appl. Environ. Microbiol. doi: 10.1128/AEM.00467-13.
41. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar Buchner, A., Lai, T., Steppi, S., Jobb, G., Förster, W., Brettske, I., Gerber, S., Ginhart, A. W., Gross, O., Grumann, S., Hermann, S., Jost, R., König, A., Liss, T., Lüssmann, R., May, M., Nonhoff, B., Reichel, B., Strehlow, R., Stamatakis, A., Stuckmann, N., Vilbig, A., Lenke, M., Ludwig, T., Bode, A., &, Schleifer, K. H., 2004. ARB: a software environment for sequence data. Nucleic Acids Res., 32: 1363-1371.
42. Madsen, E. L., Sinclair, J. L., &, Ghiorse, W. C., 1991. In situ biodegradation: microbiological patterns in a contaminated aquifer. Science, 252: 830-833.
43. Mattison, R. G., &, Harayama, S., 2001. The predatory soil flagellate Heteromita globosa stimulates toluene biodegradation by a Pseudomonas sp. FEMS Microbiol. Lett., 194: 39-45.
44. Novarino, G., Warren, A., Kinner, N. E., &, Harvey, R. W., 1994. Protists from a sewage-contaminated aquifer on Cape-Cod, Massachusetts. Geomicrobiol J., 12: 23-36.
45. Novarino, G., Warren, A., Butler, H., Lambourne, G., Boxshall, A., Bateman, J., Kinner, N. E., Harvey, R. W., Mosse, R. A., &, Teltsch, B., 1997. Protistan communities in aquifers: a review. FEMS Microbiol. Rev., 20: 261-275.
46. Oki, T., &, Kanae, S., 2006. Global hydrological cycles and world water resources. Science, 313: 1068-1072.
47. Page, F. C., 1988. A New Key to Freshwater and Soil Gymnamoebae with Instructions for Culture. Freshwater Biological Association, Ambleside. p. 122.
48. Page, F. C., 1976. An Illustrated Key to Freshwater and Soil Amoebae. Freshwater Biological Association, Cambridge. p. 155.
49. Page, F. C., &, Siemensma, F. J., 1991. Nackte Rhizopoden und Heliozoea. In:, Matthes, D., (ed.), Protozoenfauna. 1st ed, Vol. 2. Gustav Fischer Verlag, Stuttgart. p. 1-297.
50. Parry, J. D., 2004. Protozoan grazing of freshwater biofilms. Adv. Appl. Microbiol., 54: 167-196.
51. Patterson, D. J., 2003. Free-living Freshwater Protozoa: A Colour Guide, 1st ed. ASM Press, Washington, DC. p. 223.
52. Porter, K. G., &, Feig, Y. S., 1980. The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr., 25: 943-948.
53. Pronk, M., Goldscheider, N., &, Zopfi, J., 2006. Dynamics and interaction of organic carbon, turbidity and bacteria in a karst aquifer system. Hydrogeol. J., 14: 473-484.
54. Pruesse, E., Quast, C., Knittel, K., Fuchs, B. M., Ludwig, W. G., Peplies, J., &, Glockner, F. O., 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res., 35: 7188-7196.
55. Scheckenbach, F., Wylezich, C., Mylnikov, A. P., Weitere, M., &, Arndt, H., 2006. Molecular comparisons of freshwater and marine isolates of the same morphospecies of heterotrophic flagellates. Appl. Environ. Microb., 72: 6638-6643.
56. Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., Robinson, C. J., Sahl, J. W., Stres, B., Thallinger, G. G., Van Horn, D. J., &, Weber, C. F., 2009. Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microb., 75: 7537-7541.
57. Schuster, F. L., &, Pollak, A., 1978. Ultrastructure of Cercomonas sp., a free-living ameboid flagellate. Arch. Protistenkd., 120: 206-212.
58. Sherr, E. B., &, Sherr, B. F., 2002. Significance of predation by protists in aquatic microbial food webs. Anton. Leeuw. Int. J. G., 81: 293-308.
59. Simon, K. S., Gibert, J., Petitot, P., &, Laurent, R., 2001. Spatial and temporal patterns of bacterial density and metabolic activity in a karst aquifer. Arch. Hydrobiol., 151: 67-82.
60. Sinclair, J. L., &, Ghiorse, W. C., 1989. Distribution of aerobic bacteria, protozoa, algae, and fungi in deep subsurface sediments. Geomicrobiol J., 7: 15-31.
61. Sinclair, J. L., &, Alexander, M., 1989. Effect of protozoan predation on relative abundance of fast-growing and slow-growing bacteria. Can. J. Microbiol., 35: 578-582.
62. Sinclair, J. L., Kampbell, D. H., Cook, M. L., &, Wilson, J. T., 1993. Protozoa in subsurface sediments from sites contaminated with aviation gasoline or jet fuel. Appl. Environ. Microb., 59: 467-472.
63. Singleton, D. R., Furlong, M. A., Rathbun, S. L., &, Whitman, W. B., 2001. Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl. Environ. Microb., 67: 4374-4376.
64. Smirnov, A. V., Chao, E., Nassonova, E. S., &, Cavalier-Smith, T., 2011. A revised classification of naked lobose amoebae (Amoebozoa: Lobosa). Protist, 162: 545-570.
65. Streble, H., &, Krauter, D., 2010. Das Leben im Wassertropfen, 12th ed. Franckh-Kosmos Verlag, Stuttgart. p. 429.
66. Sugiyama, J., Hosaka, K., &, Suh, S.-O., 2006. Early diverging Ascomycota: phylogenetic divergence and related evolutionary enigmas. Mycologia, 98: 996-1005.
67. Takai, K., &, Horikoshi, K., 2000. Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl. Environ. Microb., 66: 5066-5072.
68. Velghe, N., &, Claeys, A., 1985. Rapid spectrophotometric determination of nitrate in mineral waters with resorcinol. Analyst, 110: 313-314.
69. Wetzel, R. G., 2001. Limnology: Lake and River Ecosystems, 3rd ed. Academic Press, San Diego, London. p. 1006.
70. Wilhartitz, I. C., Kirschner, A. K. T., Stadler, H., Herndl, G. J., Dietzel, M., Latal, C., Mach, R. L., &, Farnleitner, A. H., 2009. Heterotrophic prokaryotic production in ultraoligotrophic alpine karst aquifers and ecological implications. FEMS Microbiol. Ecol., 68: 287-299.
71. Yagi, J. M., Neuhauser, E. F., Ripp, J. A., Mauro, D. M., &, Madsen, E. L., 2010. Subsurface ecosystem resilience: long-term attenuation of subsurface contaminants supports a dynamic microbial community. ISME J., 4: 131-143.
72. Zarda, B., Mattison, G., Hess, A., Hahn, D., Höhener, P., &, Zeyer, J., 1998. Analysis of bacterial and protozoan communities in an aquifer contaminated with monoaromatic hydrocarbons. FEMS Microbiol. Ecol., 27: 141-152.
73. Zhu, F., Massana, R., Not, F., Marie, D., &, Vaulot, D., 2005. Mapping of picoeucaryotes in marine ecosystems with quantitative PCR of the 18S rRNA gene. FEMS Microbiol. Ecol., 52: 79-92.