Pyrosequencing for assessing diversity of eukaryotic microbes: Analysis of data on marine planktonic ciliates and comparison with traditional methods

Environmental Microbiology

Volumn 16, Issue 9, 2014, Pages 2752-2763

  Santoferrara, Luciana F ^a   Grattepanche, Jean David ^b   Katz, Laura A ^b,c   Mcmanus, George B ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b SMITH COLLEGE   (United States)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOREOTRICHIA; CILIOPHORA; EUKARYOTA; OLIGOTRICHIA; OTUS; SPIROTRICHEA;

SEA WATER;

BIODIVERSITY; BIOLOGY; CILIATE; CLASSIFICATION; COMPARATIVE STUDY; DNA SEQUENCE; ESTUARY; GENE LIBRARY; GENETICS; MICROBIOLOGY; PHYLOGENY; PROCEDURES; UNITED STATES;

BIODIVERSITY; CILIOPHORA; COMPUTATIONAL BIOLOGY; CONNECTICUT; ESTUARIES; GENE LIBRARY; NEW YORK; PHYLOGENY; SEAWATER; SEQUENCE ANALYSIS, DNA;

EID: 84906944211     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12380     Document Type: Article

References (56)

1. Agatha, S., and Strüder-Kypke, M.C. (2012) Reconciling cladistic and genetic analyses in choreotrichid ciliates (Ciliophora, Spirotricha, Oligotrichea). J Eukaryot Microbiol 59: 325-350.
2. Agatha, S., Struder-Kypke, M.C., Beran, A., and Lynn, D.H. (2005) Pelagostrobilidium neptuni (Montagnes and Taylor, 1994) and Strombidium biarmatum nov. spec. (Ciliophora, Oligotrichea): phylogenetic position inferred from morphology, ontogenesis, and gene sequence data. Eur J Protistol 41: 65-83.
3. Alder, V.A. (1999) Tintinnoinea. In South Atlantic Zooplankton. Boltovskoy, D. (ed.). Leiden: Backhuys Publishers, pp. 321-384.
4. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
5. Amaral-Zettler, L.A., McCliment, E.A., Ducklow, H.W., and Huse, S.M. (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.
6. Bachy, C., Lopez-Garcia, P., Vereshchaka, A., and Moreira, D. (2011) Diversity and vertical distribution of microbial eukaryotes in the snow, sea ice and seawater near the North Pole at the end of the polar night. Front Microbiol 2: 106.
7. Bachy, C., Dolan, J.R., Lopez-Garcia, P., Deschamps, P., and Moreira, D. (2013) Accuracy of protist diversity assessments: morphology compared with cloning and direct pyrosequencing of 18S rRNA genes and ITS regions using the conspicuous tintinnid ciliates as a case study. ISME J 7: 244-255.
8. Bik, H.M., Porazinska, D.L., Creer, S., Caporaso, J.G., Knight, R., and Thomas, W.K. (2012a) Sequencing our way towards understanding global eukaryotic biodiversity. Trends Ecol Evol 27: 233-243.
9. Bik, H.M., Sung, W.A.Y., De Ley, P., Baldwin, J.G., Sharma, J., Rocha-Olivares, A., and Thomas, W.K. (2012b) Metagenetic community analysis of microbial eukaryotes illuminates biogeographic patterns in deep-sea and shallow water sediments. Mol Ecol 21: 1048-1059.
10. Bittner, L., Gobet, A., Audic, S., Romac, S., Egge, E.S., Santini, S., etal. (2013) Diversity patterns of uncultured haptophytes unravelled by pyrosequencing in Naples Bay. Mol Ecol 22: 87-101.
11. Calbet, A., and Saiz, E. (2005) The ciliate-copepod link in marine ecosystems. Aquat Microb Ecol 38: 157-167.
12. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., etal. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336.
13. Capriulo, G.M., Smith, G., Troy, R., Wikfors, G.H., Pellet, J., and Yarish, C. (2002) The planktonic food web structure of a temperate zone estuary, and its alteration due to eutrophication. Hydrobiologia 475/476: 263-333.
14. Caron, D.A., and Countway, P.D. (2009) Hypotheses on the role of the protistan rare biosphere in a changing world. Aquat Microb Ecol 57: 227-238.
15. Charvet, S., Vincent, W.F., Comeau, A.M., and Lovejoy, C. (2012) Pyrosequencing analysis of the protist communities in a high arctic meromictic lake: DNA preservation and change. Front Microbiol 3: 422.
16. Colwell, R.K. (2012) EstimateS: statistical estimation of species richness and shared species from samples. Version 9. Persistent URLpurl.oclc.org/estimates.
17. Darriba, D., Taboada, G.L., Doallo, R., and Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9: 772.
18. Doherty, M., Costas, B., McManus, G., and Katz, L. (2007) Culture-independent assessment of planktonic ciliates in coastal northwest Atlantic waters. Aquat Microb Ecol 48: 141-154.
19. Doherty, M., Tamura, M., Costas, B.A., Ritchie, M.E., McManus, G.B., and Katz, L.A. (2010a) Ciliate diversity and distribution across an environmental and depth gradient in Long Island Sound, USA. Environ Microbiol 12: 886-898.
20. Doherty, M., Tamura, M., Vriezen, J.A.C., McManus, G.B., and Katz, L.A. (2010b) Diversity of Oligotrichia and Choreotrichia ciliates in coastal marine sediments and in overlying plankton. Appl Environ Microbiol 76: 3924-3935.
21. Dolan, J.R., Agatha, S., Coats, D.W.C., Montagnes, D.J.S., and Stoecker, D.K. (2012) Biology and Ecology of Tintinnid Ciliates: Models for Marine Plankton. Oxford: Wiley/ Blackwell.
22. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
23. Edgar, R.C. (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
24. Edgar, R.C., Haas, B., Clemente, J., Quince, C., and Knight, R. (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
25. Edgcomb, V., Orsi, W., Bunge, J., Jeon, S., Christen, R., Leslin, C., etal. (2011) Protistan microbial observatory in the Cariaco Basin, Caribbean. I. Pyrosequencing vs Sanger insights into species richness. ISME J 5: 1344-1356.
26. Fenchel, T., Esteban, G.F., and Finlay, B.J. (1997) Local versus global diversity of microorganisms: cryptic diversity of ciliated protozoa. Oikos 80: 220-225.
27. Finlay, B., Esteban, G.F., Brown, S., Fenchel, T., and Hoef-Emden, K. (2006) Multiple cosmopolitan ecotypes within a microbial eukaryote morphospecies. Protist 157: 377-390.
28. Gong, J., Dong, J., Liu, X., and Massana, R. (2013) Extremely high copy numbers and polymorphisms of the rDNA operon estimated from single cell analysis of oligotrich and peritrich ciliates. Protist 164: 369-379.
29. Grattepanche, J.-D., Santoferrara, L.F., Andrade, J., Oliverio, A., McManus, G., and Katz, L.A. (2014) Distribution and diversity of oligotrich and choreotrich ciliates assessed by morphology and by DGGE in temperate coastal waters. Aquat Microb Ecol 71: 211-221.
30. Huse, S.M., Welch, D.M., Morrison, H.G., and Sogin, M.L. (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12: 1889-1898.
31. Katoh, K., and Toh, H. (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9: 286-298.
32. Katz, L.A., McManus, G.B., Snoeyenbos-West, O., Griffin, A., Pirog, K., Costas, B., and Foissner, W. (2005) Reframing the 'Everything is everywhere' debate: evidence for high gene flow and diversity in ciliate morphospecies. Aquat Microb Ecol 41: 55-65.
33. Kunin, V., Engelbrektson, A., Ochman, H., and Hugenholtz, P. (2010) Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol 12: 118-123.
34. Li, J., Liu, W., Gao, S., Warren, A., and Song, W. (2013) Multigene-based analyses of the phylogenetic evolution of oligotrich ciliates, with consideration of the internal transcribed spacer 2 secondary structure of three systematically ambiguous genera. Eukaryot Cell 12: 430-437.
35. Liu, W., Yi, Z., Lin, X., Warren, A., and Song, W. (2012) Phylogeny of three choreotrich genera (Protozoa, Ciliophora, Spirotrichea), with morphological, morphogenetic and molecular investigations on three strobilidiid species. Zool Scr 41: 417-434.
36. Logares, R., Audic, S., Santini, S., Pernice, M.C., de Vargas, C., and Massana, R. (2012) Diversity patterns and activity of uncultured marine heterotrophic flagellates unveiled with pyrosequencing. ISME J 6: 1823-1833.
37. Lynn, D.H. (2008) The Ciliated Protozoa. Characterization, Classification, and Guide to the Literature. Dordrecht: Springer Verlag.
38. Marande, W., López-García, P., and Moreira, D. (2009) Eukaryotic diversity and phylogeny using small- and large-subunit ribosomal RNA genes from environmental samples. Environ Microbiol 11: 3179-3188.
39. Medinger, R., Nolte, V., Pandey, R.V., Jost, S., OttenwÄLder, B., Schlötterer, C., and Boenigk, J. (2010) Diversity in a hidden world: potential and limitation of next-generation sequencing for surveys of molecular diversity of eukaryotic microorganisms. Mol Ecol 19: 32-40.
40. Miller, M.A., Pfeiffer, W., and Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov 2010, New Orleans, LA, pp. 1-8.
41. Monchy, S., Grattepanche, J.-D., Breton, E., Meloni, D., Sanciu, G., Chabé, M., etal. (2012) Microplanktonic community structure in a coastal system relative to a Phaeocystis bloom inferred from morphological and tag pyrosequencing methods. PLoS ONE 7: e39924.
42. Porter, T.M., and Golding, G.B. (2011) Are similarity- or phylogeny-based methods more appropriate for classifying internal transcribed spacer (ITS) metagenomic amplicons? New Phytologist 192: 775-782.
43. Quince, C., Lanzen, A., Davenport, R., and Turnbaugh, P. (2011) Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12: 38.
44. Reeder, J., and Knight, R. (2010) Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Methods 7: 668-669.
45. Santoferrara, L.F., and Alder, V.A. (2012) Abundance and diversity of tintinnids (planktonic ciliates) under contrasting levels of productivity in the Argentine Shelf and Drake Passage. J Sea Res 71: 25-30.
46. Santoferrara, L.F., McManus, G.B., and Alder, V.A. (2012) Phylogeny of the order Tintinnida (Ciliophora, Spirotrichea) inferred from small- and large-subunit rRNA genes. J Eukaryot Microbiol 59: 423-426.
47. Santoferrara, L.F., McManus, G.B., and Alder, V.A. (2013) Utility of genetic markers and morphology for species discrimination within the order Tintinnida (Ciliophora, Spirotrichea). Protist 164: 24-36.
48. Sievers, F., Wilm, A., Dineen, D., Gibson, T.J., Karplus, K., Li, W., etal. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7: 539.
49. Snoeyenbos-West, O., Salcedo, T., McManus, G., and Katz, L. (2002) Insights into the diversity of choreotrich and oligotrich ciliates (class: Spirotrichea) based on genealogical analyses of multiple loci. Int J Syst Evol Microbiol 52: 1901-1913.
50. Sogin, M.L., Morrison, H.G., Huber, J.A., Welch, D.M., Huse, S.M., Neal, P.R., etal. (2006) Microbial diversity in the deep sea and the underexplored 'rare biosphere. Proc Natl Acad Sci USA 103: 12115-12120.
51. Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
52. Stoeck, T., Behnke, A., Christen, R., Amaral-Zettler, L., Rodriguez-Mora, M.J., Chistoserdov, A., etal. (2009) Massively parallel tag sequencing reveals the complexity of anaerobic marine protistan communities. BMC Biol 7: 72.
53. Stoeck, T., Bass, D., Nebel, M., Christen, R., Jones, M.D.M., Breiner, H.W., and Richards, T.A. (2010) Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol Ecol 19: 21-31.
54. Stoeck, T., Breiner, H.-W., Filker, S., Ostermaier, V., Kammerlander, B., and Sonntag, B. (2014) A morpho-genetic survey on ciliate plankton from a mountain lake pinpoints the necessity of lineage-specific barcode markers in microbial ecology. Environ Microbiol 16: 430-444.
55. Tamura, M., Katz, L.A., and McManus, G.B. (2011) Distribution and diversity of oligotrich and choreotrich ciliates across an environmental gradient in a large temperate estuary. Aquat Microb Ecol 64: 51-67.
56. Zinger, L., Gobet, A., and Pommier, T. (2012) Two decades of describing the unseen majority of aquatic microbial diversity. Mol Ecol 21: 1878-1896.