Culturing Bias in Marine Heterotrophic Flagellates Analyzed Through Seawater Enrichment Incubations

Microbial Ecology

Volumn 66, Issue 3, 2013, Pages 489-499

  del Campo, Javier ^a,c   Balagué, Vanessa ^a   Forn, Irene ^a   Lekunberri, Itziar ^a,b   Massana, Ramon ^a  

^a INSTITUT DE CIÈNCIES DEL MAR   (Spain)

^b UNIVERSITY OF VIENNA   (Austria)

^c INSTITUTE OF EVOLUTIONARY BIOLOGY CSIC UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); EUKARYOTA; MASTIGOPHORA (FLAGELLATES); PROTISTA;

SEA WATER;

ARTICLE; BACTERIUM; BIODIVERSITY; CHEMISTRY; CLASSIFICATION; EUKARYOTE; FILTRATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HETEROTROPHY; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PARASITOLOGY; PHYLOGENY;

BACTERIA; BIODIVERSITY; EUKARYOTA; FILTRATION; HETEROTROPHIC PROCESSES; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEAWATER;

EID: 84884411804     PISSN: 00953628     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00248-013-0251-y     Document Type: Article

References (55)

1. Sherr EB, Sherr BF (2002) Significance of predation by protists in aquatic microbial food webs. Anton Leeuw 81: 293-308.
2. Jürgens K, Massana R (2008) Protistan grazing on marine bacterioplankton. In: Kirchman DL (ed) Microbial ecology of the oceans, 2nd edn. Wiley, New York, pp 383-441.
3. Pernthaler J (2005) Predation on prokaryotes in the water column and its ecological implications. Nat Rev Microbiol 3: 537-546.
4. Guillou L, Viprey M, Chambouvet A, Welsh RM, Kirkham AR, Massana R, Scanlan DJ, Worden AZ (2008) Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environ Microbiol 10: 397-408.
5. Fenchel T (1982) Ecology of heterotrophic microflagellates: I. Some important forms and their functional morphology. Mar Ecol Prog Ser 8: 211-223.
6. 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.
7. Cowling AJ (1991) Free-living heterotrophic flagellates: methods of isolation and maintenance, including sources of strains in culture. In: Patterson DJ, Larsen J (eds) The biology of free-living heterotrophic flagellates. Oxford University Press, Oxford, pp 477-492.
8. Wang J, Levin P (2009) Metabolism, cell growth and the bacterial cell cycle. Nat Rev Microbiol 7: 822-827.
9. Fenchel T (1982) Ecology of heterotrophic microflagellates: IV. Quantitative occurrence and importance as bacterial consumers. Mar Ecol Prog Ser 9: 35-42.
10. Lim EL, Dennet MR, Caron DA (1999) The ecology of Paraphysomonas imperforata based on studies employing oligonucleotide probe identification in coastal water samples and enrichment cultures. Limnol Oceanogr 44: 37-51.
11. Arndt H, Dietrich D, Auer B, Cleven EJ, Gräfenhan T, Weitere M, Mylnikov AP (2000) Functional diversity of heterotrophic flagellates in aquatic ecosystems. In: Leadbeater BSC, Green JC (eds) The flagellates: unity, diversity and evolution. Taylor & Francis Press, London, pp 240-268.
12. Scheckenbach F, Wylezich C, Weitere M, Hausmann K, Arndt H (2005) Molecular identity of strains of heterotrophic flagellates isolated from surface waters and deep-sea sediments of the South Atlantic based on SSU rDNA. Aquat Microb Ecol 38: 239-247.
13. Massana R, del Campo J, Dinter C, Sommaruga R (2007) Crash of a population of the marine heterotrophic flagellate Cafeteria roenbergensis by viral infection. Environ Microbiol 9: 2660-2669.
14. del Campo J, Massana R (2011) Emerging diversity within chrysophytes, choanoflagellates and bicosoecids based on molecular surveys. Protist 162: 435-448.
15. Massana R, Balagué V, Guillou L, Pedrós-Alió C (2004) Picoeukaryotic diversity in an oligotrophic coastal site studied by molecular and culturing approaches. FEMS Microbiol Ecol 50: 231-243.
16. Massana R, Guillou L, Terrado R, Forn I, Pedrós-Alió C (2006) Growth of uncultured heterotrophic flagellates in unamended seawater incubations. Aquat Microb Ecol 45: 171-180.
17. Handelsman J (2004) Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 68: 669-685.
18. Snyder JC, Spuhler J, Wiedenheft B, Roberto FF, Douglas T, Young MJ (2004) Effects of culturing on the population structure of a hyperthermophilic virus. Microb Ecol 48: 561-566.
19. Countway PD, Gast RJ, Savai P, Caron DA (2005) Protistan diversity estimates based on 18S rDNA from seawater incubations in the Western North Atlantic. J Eukaryot Microbiol 52: 95-106.
20. Massana R, Gasol JM, Bjørnsen PK, Blackburn N, Hagström A, Hietanen S, Hygu BH, Kuparinen J, Pedrós-Alió C (1997) Measurement of bacterial size via image analysis of epifluorescence preparations: description of an inexpensive system and solutions to some of the most common problems. Sci Mar 61: 397-407.
21. Díez B, Pedrós-Alió C, Massana R (2001) Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing. Appl Environ Microbiol 67: 2932-2941.
22. Muyzer G, Brinkhoff T, Nübel U, Santegoeds C, Schäfer H, Wawer C (1997) Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. In: Akkermans ADL, van Elsas JD, de Bruijn FJ (eds) Molecular microbial ecology manual, vol. 3. 4. 4. Kluwer, Dordrecht, pp 1-27.
23. Díez B, Pedrós-Alió C, Marsh TL, Massana R (2001) Application of denaturing gradient gel electrophoresis (DGGE) to study the diversity of marine picoeukaryotic assemblages and comparison of DGGE with other molecular techniques. Appl Environ Microbiol 67: 2942-2951.
24. Elwood HJ, Olsen GJ, Sogin ML (1985) The small subunit ribosomal RNA gene sequences from the hypotrichous ciliates Ogwicha nova and Stylonychia pustulata. J Mol Biol Evol 2: 399-410.
25. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
26. 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 JR, Dunthorn M, Edvardsen B, Holzmann M, Kooistra WHCF, Lara E, Le Bescot N, Logares R, Mahe F, Massana R, Montresor M, Morard R, Not F, Pawlowski J, Probert I, Sauvadet AL, 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 Acids Res 41: 597-604.
27. Katoh K, Misawa K, Kuma L, Miyata Y (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30: 3059-3066.
28. Galtier N, Gouy M, Gautier C (1996) SeaView and Phylo_Win, two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12: 543-548.
29. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540-552.
30. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
31. Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinfoma 17: 754-755.
32. Hamady M, Lozupone C, Knight R (2010) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4: 17-27.
33. Massana R, Castresana J, Balagué V, Guillou L, Romari K, Groisillier A, Valentin K, Pedrós-Alió C (2004) Phylogenetic and ecological analysis of novel marine stramenopiles. Appl Environ Microbiol 70: 3528-3534.
34. Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27: 379-656.
35. Eilers H, Pernthaler J, Amann R (2000) Succession of pelagic marine bacteria during enrichment: a close look on cultivation-induced shifts. Appl Environ Microbiol 66: 4634-4640.
36. Rappé MS, Connon SA, Vergin KL, Giovannoni SJ (2002) Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418: 630-633.
37. Pedrós-Alió C (2006) Marine microbial diversity: can it be determined? Trends Microbiol 14: 257-263.
38. Allers E, Gómez-Consarnau L, Pinhassi J, Gasol JM, Simek K, Pernthaler J (2007) Response of Alteromonadaceae and Rhodobacteriaceae to glucose and phosphorus manipulation in marine mesocosms. Environ Microbiol 9: 2417-2429.
39. Jürgens K, Güde H (1994) The potential importance of grazing-resistant bacteria in planktonic systems. Mar Ecol Prog Ser 112: 169-188.
40. Davis PG, Sieburth JM (1984) Estuarine and oceanic microflagellate predation of actively growing bacteria: estimation by frequency of dividing-divided bacteria. Mar Ecol Prog Ser 19: 237-246.
41. Hahn MW, Moore ERB, Höfle MG (2000) Role of microcolony formation in the protistan grazing defense of the aquatic bacterium Pseudomonas sp. MWH1. Microb Ecol 39: 175-185.
42. Simek K, Pernthaler J, Weinbauer MG, Hornak K, Dolan JR, Nedoma J, Masin M, Amann R (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. Weber F, del Campo J, Wylezich C, Massana R, Jürgens K (2012) Unveiling trophic functions of uncultured protist taxa by incubation experiments in the brackish Baltic Sea. PLoS One 7: e41970.
44. Fenchel T (1982) Ecology of heterotrophic microflagellates: II. Bioenergetics and growth. Mar Ecol Prog Ser 8: 225-231.
45. Caron DA, Goldman JC, Andersen OK, Dennett MR (1985) Nutrient cycling in a microflagellate food chain: II. Population dynamics and carbon cycling. Mar Ecol Prog Ser 24: 243-254.
46. Eccleston-Parry JD, Leadbeater BSC (1994) A comparison of the growth kinetics of six marine heterotrophic nanoflagellates fed with one bacterial species. Mar Ecol Prog Ser 105: 167-177.
47. López-García P, Rodríguez-Valera F, Pedrós-Alió C, Moreira D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409: 603-607.
48. Moon-van der Staay SY, de Wachter R, Vaulot D (2001) Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409: 607-610.
49. Patterson DJ, Nygaard K, Steinberg G, Turley CM (1993) Heterotrophic flagellates and other protists associated with oceanic detritus throughout the water column in the mid North Atlantic. J Mar Biol Assoc UK 73: 67-95.
50. Vørs N, Buck K, Chavez F, Eikrem W, Hansen L, Ostergaard J, Thomsen H (1995) Nanoplankton of the equatorial Pacific with emphasis on the heterotrophic protists. Deep Sea Res II 42: 585-595.
51. Tong SM (1997) Heterotrophic flagellates from the water column in Shark Bay, Western Australia. Mar Biol 128: 517-536.
52. Tong SM, Vørs N, Patterson DJ (1997) Heterotrophic flagellates, centrohelid heliozoa and filose amoebae from marine and freshwater sites in the Antarctic. Polar Biol 18: 91-106.
53. Tikhonenkov DV, Mazei YA (2006) Distribution of heterotrophic flagellates at the littoral of estuary of Chernaya River (Kandalaksha Bay, White Sea). Russ J Mar Biol 32: 276-283.
54. Tikhonenkov DV, Mazei YA, Mylnikov AP (2006) Species diversity of heterotrophic flagellates in White Sea littoral sites. Eur J Protistol 42: 191-200.
55. del Campo J, Not F, Forn I, Sieracki ME, Massana R (2013) Taming the smallest predators of the oceans. ISME J 7: 351-358.