Unveiling trophic functions of uncultured protist taxa by incubation experiments in the Brackish Baltic sea

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Weber, Felix ^a   del Campo, Javier ^b   Wylezich, Claudia ^a   Massana, Ramon ^b   Jürgens, Klaus ^a  

^a LEIBNIZ INSTITUTE FOR BALTIC SEA RESEARCH   (Germany)

^b INSTITUT DE CIÈNCIES DEL MAR   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 18S; SEA WATER;

ARTICLE; BALTIC SEA; CLADISTICS; DARKNESS; ENVIRONMENTAL PARAMETERS; GENETIC VARIABILITY; HETEROTROPH; MIXOTROPH; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOTROPH; PHYLOGENY; PROTIST; PROTISTAN COMMUNITY; RNA SEQUENCE; TAXONOMY; TROPHIC FUNCTION; UNINDEXED SEQUENCE;

MARINE BIOLOGY; MOLECULAR SEQUENCE DATA; OCEANS AND SEAS; PHYLOGENY; PLANKTON; RNA, RIBOSOMAL, 18S;

CERCOZOA; CHOANOFLAGELLIDA; CHRYSOPHYCEAE; MASTIGOPHORA (FLAGELLATES); PROTISTA; STRAMENOCHROMA;

EID: 84864429735     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041970     Document Type: Article

References (85)

1. Jürgens K, Massana R, (2008) Protistan grazing on marine bacterioplankton. In: Kirchman DL, ed. Microbial Ecology of the Oceans Wiley-Blackwell: New Jersey. pp. 383-441.
2. Fenchel T, (1986) The ecology of heterotrophic microflagellates. Adv Microb Ecol 9: 57-97.
3. Sherr EB, Sherr BF, (2002) Significance of predation by protists in aquatic microbial food webs. Antonie van Leeuwenhoek 81: 293-308.
4. Jürgens K, Matz C, (2002) Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. Antonie van Leeuwenhoek 81: 413-434.
5. Pernthaler J, (2005) Predation on prokaryotes in the water column and its ecological implications. Nat Rev Microbiol 3: 537-546.
6. Zöllner E, Hoppe HG, Sommer U, Jürgens K, (2009) Effect of zooplankton-mediated trophic cascades on marine microbial food web components (bacteria, nanoflagellates, ciliates). Limnol Oceanogr 54: 262-275.
7. Nagata T, (2000) Production mechanisms of dissolved organic matter. In: Kirchman DL, ed. Microbial Ecology of the Oceans Wiley-Blackwell: New Jersey. pp. 121-152.
8. Ekelund F, Rønna R, Griffiths BS, (2001) Quantitative estimation of flagellate community structure and diversity in soil samples. Protist 152: 301-314.
9. Wylezich C, Mylnikov AP, Weitere M, Arndt H, (2007) Freshwater thaumatomonads as common amoeboid heterotrophic flagellates: their phylogenetic relationships and description of the new species Thaumatomonas coloniensis n. sp. J Eukaryot Microbiol 54: 347-357.
10. 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.
11. Koch TA, Ekelund F, (2005) Strains of the heterotrophic flagellate Bodo designis from different environments vary considerably with respect to salinity preference and SSU rRNA gene composition. Protist 156: 97-112.
12. Gächter E, Weisse T, (2006) Local adaptation among geographically distant clones of the cosmopolitan freshwater ciliate Meseres corlissi. I. Temperature response. Aquat Microb Ecol45: 291-300.
13. Dawson SC, Hagen KD, (2009) Mapping the protistan 'rare biosphere'. J Biol 8: 105.
14. Arndt H, Dietrich D, Auer B, Cleven EJ, Gräfenhan T, et al. (2000) Functional diversity of heterotrophic flagellates in aquatic ecosystems. In: Leadbeater BSC, Green JC, eds. The Flagellates. Taylor & Francis: London, UK. pp. 240-268.
15. Foissner W, (1999) Protist diversity: estimates of the near-imponderable. Protist 150: 363-368.
16. 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.
17. Guillou G, Moon-van der Staay SY, Claustre H, Partensky F, Vaulot D, (1999) Diversity and abundance of Bolidophyceae (Heterokonta) in two oceanic regions. Appl Environ Microbiol 65: 4528-4536.
18. Lim EL, Dennett MR, Caron DA, (1999) The ecology of Paraphysomonas imperforata based on studies employing oligonucleotide probe identification in costal water samples and enrichment cultures. Limnol Oceanogr 44: 37-51.
19. Shi XL, Marie D, Jardillier L, Scanlan DJ, Vaulot D, (2009) Groups without cultured representatives dominate eukaryotic picophytoplankton in the oligotrophic South East Pacific Ocean. PLoS ONE 4: e7657.
20. Moreira D, López-García P, (2002) The molecular ecology of microbial eukaryotes unveils a hidden world. Trends Microbiol 10: 31-38.
21. 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.
22. Díez B, Pedrós-Alió C, Marsh TL, Massana R, (2001) Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small- subunit r RNA gene cloning and sequencing. Appl Environ Microbiol 67: 2932-2941.
23. López-García P, Rodriguez-Valera F, Pedrós- Alió C, Moreira D, (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409: 603-607.
24. Moon-van der Staay SY, De Wachter R, Vaulot D, (2001) Oceanic 18S rDNA sequences from picoplankton reveal unexpected eukaryotic diversity. Nature 409: 607-610.
25. Richards TA, Vepritskiy AA, Gouliamova DE, Nierzwicki- Bauer SA, (2005) The molecular diversity of freshwater picoeukaryotes from oligotrophic lake reveals diverse, distinctive and globally dispersed lineages. Environ Microbiol 7: 1413-1425.
26. Not F, del Campo J, Balagué V, de Vargas C, Massana R, (2009) New insights into the diversity of marine picoeukaryotes. PLoS ONE 4: e7143.
27. Massana R, Guillou L, Díez B, Pedrós-Alió C, (2002) Unveiling the organisms behind novel eukaryotic ribosomal DNA sequences from the ocean. Appl Environ Microbiol 68: 4554-4558.
28. Massana R, Castresana J, Balagué V, Guillou L, Romari K, et al. (2004) Phylogenetic and ecological analysis of novel marine stramenopiles. Appl Environ Microbiol 70: 3528-3534.
29. Groisillier A, Massana R, Valentin K, Vaulot D, Guillou L, (2006) Genetic diversity and habitats of two enigmatic marine alveolate lineages. Aquat Microb Ecol 42: 277-291.
30. Not F, Valentin K, Romari K, Lovejoy C, Massana R, et al. (2007) Picobiliphytes: a marine picoplanktonic algal group with unknown affinities to other eukaryotes. Science 315: 253-255.
31. Amaral-Zettler LA, McCliment EA, Ducklow HW, Huse SM, (2009) A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS ONE 4: e6372.
32. Behnke A, Barger KJ, Bunge J, Stoeck T, (2010) Spatio-temporal variations in protistan communities along an O2/H2S gradient in the anoxic Framvaren Fjord (Norway). FEMS Microbiol Ecol 72: 89-102.
33. Edgcomb V, Orsi W, Bunge J, Jeon SO, Christen R, et al. (2011) Protistan microbial observatory in the Cariaco Basin, Caribbean. I. pyrosequencing vs sanger insights into species richness. ISME J 5: 1344-1356.
34. Bråte J, Logares R, Berney C, Ree DK, Klaveness D, et al. (2010) Freshwater Perkinsea and marine-freshwater colonizations revealed by pyrosequencing and phylogeny of environmental rDNA. ISME J 4: 1144-1153.
35. Nolte V, Pandey RV, Jost S, Medinger R, Ottenwälder B, et al. (2010) Contrasting seasonal niche separation between rare and abundant taxa conceals the extent of protist diversity. Mol Ecol 19: 2908-2915.
36. Scheckenbach F, Hausmann K, Wylezich C, Weitere M, Arndt H, (2010) Large-scale patterns in biodiversity of microbial eukaryotes from the abyssal sea floor. Proc Natl Acad Sci USA 107: 115-120.
37. Pawlowski J, Christen R, Lecroq B, Bachar D, Shahbazkia HR, et al. (2011) Eukaryotic richness in the abyss: insights from pyrotag sequencing. PLoS ONE 6: e18169.
38. del Campo J, Massana R, (2011) Emerging diversity within chrysophytes, choanoflagellates and bicosoecids based on molecular surveys. Protist 162: 435-448.
39. Worden AZ, Not F, (2008) Ecology and diversity of picoeukaryotes. In: Kirchman DL, ed. Microbial Ecology of the Oceans Wiley-Blackwell: New Jersey. pp. 159-205.
40. Mangot JF, Lepère C, Bouvier C, Debroas D, Domaizon I, (2009) Community structure and dynamics of small eukaryotes targeted by new oligonucleotide probes: new insight into the lacustrine microbial food web. Appl Environ Microbiol 75: 6373-6381.
41. Massana R, Unrein F, Rodríguez-Martínez R, Forn I, Lefort T, et al. (2009) Grazing rates and functional diversity of uncultured heterotrophic flagellates. ISME J 3: 588-596.
42. Piwosz K, Pernthaler J, (2010) Seasonal population dynamics and trophic role of planktonic nanoflagellates in coastal surface waters of the Southern Baltic Sea. Environ Microbiol 12: 364-377.
43. Frias-Lopez J, Thompson A, Waldbauer J, Chisholm SW, (2009) Use of stable isotope-labelled cells to identify active grazers of picocyanobacteria in ocean surface waters. Environ Microbiol 11: 512-525.
44. Heywood JL, Sieracki ME, Bellows W, Poulton NJ, Stepanauskas R, (2011) Capturing diversity of marine heterotrophic protists: one cell at a time. ISME J 5: 674-684.
45. 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.
46. del Campo J (2011) Culturing bias in the study of marine heterotrophic flagellates. Doctoral thesis. Institut de Ciències del Mar- CSIC. Universitat de Barcelona.
47. 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.
48. Kim DY, Countway PD, Gast RJ, Caron DA, (2011) Rapid shifts in the structure and composition of a protistan assemblage during bottle incubations affect estimates of total protistan species richness. Microb Ecol 62: 383-398.
49. Burki F, Inagaki Y, Bråte J, Archibald JM, Keeling PJ, et al. (2009) Large-scale phylogenomic analyses reveal that two enigmatic protist lineages, Telonemia and Centroheliozoa, are related to photosynthetic Chromalveolates. Genome Biol Evol 1: 231-238.
50. Massana R, Terrado R, Forn I, Lovejoy C, Pedrós-Alió C, (2006) Distribution and abundance of uncultured heterotrophic flagellates in the world oceans. Environ Microbiol 8: 1515-1522.
51. Yabuki A, Ishida K, (2011) Mataza hastifera n. g., n. sp.: A possible new lineage in the Thecofilosea (Cercozoa). J Eukaryot Microbiol 58: 94-102.
52. Cuvelier ML, Ortiz A, Kim E, Moehlig H, Richardson DE, et al. (2008) Widespread distribution of a unique marine protistan lineage. Environ Microbiol 10: 1621-1634.
53. Lebaron P, Servais P, Agogué H, Courties C, Joux F, (2001) Does the high nucleic acid content of individual bacterial cells allow us to discriminate between active cells and inactive cells in aquatic systems? Appl Environ Microbiol 67: 1775-1782.
54. Heinänen AP, (1991) Bacterial numbers, biomass and productivity in the Baltic Sea: a cruise study. Mar Ecol Prog Ser 70: 283-290.
55. Heinänen A, Kuparinen J, (1991) Horizontal variation of bacterioplankton in the Baltic Sea. Appl Environ Microbiol 57: 3150-3155.
56. Andersson AF, Riemann L, Bertilsson S, (2010) Pyrosequencing reveals contrasting seasonal dynamics of taxa within Baltic Sea bacterioplankton communities. ISME J 4: 171-181.
57. Zobell CE, Anderson Q, (1936) Observations on the multiplication of bacteria in different volumes of stored sea water and the influence of oxygen tension and solid surfaces Biol Bull. 71: 324-342.
58. Jürgens K, Gasol JM, Vaqué D, (2000) Bacteria-flagellate coupling in microcosm experiments in the Central Atlantic Ocean. J Exp Mar Biol Ecol 245: 127-147.
59. Agis M, Granda A, Dolan JR, (2007) A cautionary note: examples of possible microbial community dynamics in dilution grazing experiments. J. Exp Mar Biol Ecol 341: 176-183.
60. Hammes F, Vital M, Egli T, (2010) Critical evaluation of the volumetric "bottle effect" on microbial batch growth. Appl Environ Microbiol 76: 1278-1281.
61. von Wintzingerode F, Göbel UB, Stackebrandt E, (1997) Determination of microbial diversity in environmental samples: pitfalls of PCR- based rRNA analysis. FEMS Microbiol Rev 21: 213-229.
62. Stoeck T, Zuendorf A, Breiner HW, Behnke A, (2007) A molecular approach to identify active microbes in environmental eukaryote clone libraries. Microb Ecol 53: 328-339.
63. Wikner J, Hagström A, (1988) Evidence for a tightly coupled nanoplanktonic predator-prey link regulating the bacterivores in the marine environment. Mar Ecol Prog Ser 50: 137-146.
64. Kirchman DL, (1990) Limitation of bacterial growth by dissolved organic matter in the subarctic Pacific. Mar Ecol Prog Ser 62: 47-54.
65. Calbet A, Landry MR, Nunnery S, (2001) Bacteria-flagellate interactions in the microbial food web of the oligotrophic subtropical North Pacific. Aquat Microb Ecol 23: 283-292.
66. 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.
67. Calvo-Díaz A, Díaz-Pérez L, Suárez LA, Morán XAG, Teira E, et al. (2011) Decrease in the autotrophic-to-heterotrophic biomass ratio of picoplankton in oligotrophic marine waters due to bottle enclosure. Appl Environ Microbiol 77: 5739-5746.
68. Leadbeater BSC, Thomsen HA (2000) Order Choanoflagellida. In: Lee JJ, Leedale GF, Bradbury P, eds. The illustrated guide to the protozoa. Society of Protozoologists: Lawrence, Kansas. 2nd Ed, 14-38.
69. Cavalier-Smith T, Chao EEY, (2006) Phylogeny and megasystematics of phagotrophic heterokonts (kingdom Chromista). J Mol Evol 62: 388-420.
70. Wylezich C, Jürgens K, (2011) Protist diversity in suboxic and sulfidic waters of the Black Sea. Environ Microbiol 13: 2939-2956.
71. Yoon HS, Price DC, Stepanauskas R, Rajah VD, Sieracki ME, et al. (2011) Single-cell genomics reveals organismal interactions in uncultivated marine protists. Science 332: 714-717.
72. Gasol JM, Del Giorgio PA, (2000) Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Sci Mar 64: 197-224.
73. Weinbauer MG, Fritz I, Wenderoth DF, Höfle MG, (2002) Simultaneous extraction from bacterioplankton of total RNA and DNA suitable for quantitative structure and function analyses. Appl Environ Microbiol 68: 1082-1087.
74. Medlin LH, Elwood J, Stickel S, Sogin ML, (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71: 491-500.
75. Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, et al. (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56: 1919-1925.
76. Elwood HJ, Olsen GJ, Sogin ML, (1985) The small-subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. Mol Biol Evol 2: 399-410.
77. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
78. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, et al. (2009) Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
79. 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.
80. Castresana J, (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540-552.
81. Hall TA, (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Res Symp Ser 41: 95-98.
82. Stamatakis A, (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
83. Kumar S, Skjaeveland A, Orr RJ, Enger P, Ruden T, et al. (2009) AIR: A batch-oriented web program package for construction of supermatrices ready for phylogenomic analyses. BMC Bioinf 10: 357.
84. Huelsenbeck JP, Ronquist F, (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinfomatics 17: 754-755.
85. Massana R, Pernice M, Bunge J, del Campo J, (2010) Sequence diversity and novelty of natural assemblages of picoeukaryotes from the Indian Ocean. ISME J 5: 184-195.