An association network analysis among microeukaryotes and bacterioplankton reveals algal bloom dynamics

Journal of Phycology

Volumn 51, Issue 1, 2015, Pages 120-132

  Tan, Shangjin ^a   Zhou, Jin ^a   Zhu, Xiaoshan ^a   Yu, Shichen ^a   Zhan, Wugen ^a   Wang, Bo ^a   Cai, Zhonghua ^a  

^a TSINGHUA UNIVERSITY   (China)

Author keywords

Parvilucifera; Roseobacter; Algal blooms; Bacteria; Co occurrence patterns; T RFLP

Indexed keywords

ALGAE; ALPHAPROTEOBACTERIA; BACTERIA (MICROORGANISMS); BACTEROIDETES; DINOPHYCEAE; GAMMAPROTEOBACTERIA; PARVILUCIFERA; PERKINSEA; ROSEOBACTER; SCRIPPSIELLA TROCHOIDEA;

EID: 84922014622     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/jpy.12259     Document Type: Article

References (66)

1. Abdo, Z., Schuette, U. M. E., Bent, S. J., Williams, C. J., Forney, L. J. & Joyce, P. 2006. Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes. Environ. Microbiol. 8:929-38.
2. Allers, E., Gómez-Consarnau, L., Pinhassi, J., Gasol, J. M., Šimek, K. & Pernthaler, J. 2007. Response of Alteromonadaceae and Rhodobacteriaceae to glucose and phosphorus manipulation in marine mesocosms. Environ. Microbiol. 9:2417-29.
3. Alonso, C. & Pernthaler, J. 2006. Roseobacter and SAR11 dominate microbial glucose uptake in coastal North Sea waters. Environ. Microbiol. 8:2022-30.
4. Amaro, A. M., Fuentes, M. S., Ogalde, S. R., Venegas, J. A. & Suárez-Isla, B. A. 2005. Identification and characterization of potentially algal-lytic marine bacteria strongly associated with the toxic dinoflagellate Alexandrium catenella. J. Eukaryot. Microbiol. 52:191-200.
5. Anderson, D. M., Burkholder, J. M., Cochlan, W. P., Glibert, P. M., Gobler, C. J., Heil, C. A., Kudela, R. M., Parsons, M. L., Rensel, J. & Townsend, D. W. 2008. Harmful algal blooms and eutrophication: examining linkages from selected coastal regions of the United States. Harmful Algae 8:39-53.
6. Bertness, M. D. & Callaway, R. 1994. Positive interactions in communities. Trends Ecol. Evol. 9:191-3.
7. Borgatti, S. P., Everett, M. G. & Freeman, L. C. 2002. Ucinet for Windows: Software for Social Network Analysis. Cambridge, Harvard, MA.
8. Brinkhoff, T., Bach, G., Heidorn, T., Liang, L. F., Schlingloff, A. & Simon, M. 2004. Antibiotic production by a Roseobacter clade-affiliated species from the German Wadden Sea and its antagonistic effects on indigenous isolates. Appl. Environ. Microb. 70:2560-5.
9. Buchan, A., Gonzalez, J. M. & Moran, M. A. 2005. Overview of the marine Roseobacter lineage. Appl. Environ. Microb. 71:5665-77.
10. Chen, M. J., Chen, F. Z., Xing, P., Li, H. B. & Wu, Q. L. L. 2010. Microbial eukaryotic community in response to Microcystis spp. bloom, as assessed by an enclosure experiment in Lake Taihu, China. FEMS Microbiol. Ecol. 74:19-31.
11. Culman, S. W., Bukowski, R., Gauch, H. G., Cadillo-Quiroz, H. & Buckley, D. H. 2009. T-REX: software for the processing and analysis of T-RFLP data. BMC Bioinformatics 10:171.
12. Culman, S. W., Gauch, H. G., Blackwood, C. B. & Thies, J. E. 2008. Analysis of T-RFLP data using analysis of variance and ordination methods: a comparative study. J. Microbiol. Meth. 75:55-63.
13. DeSantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., Huber, T., Dalevi, D., Hu, P. & Andersen, G. L. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microb. 72:5069-72.
14. Díez, B., Pedrós-Alió, C., Marsh, T. L. & 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. Microb. 67:2942-51.
15. Dollhopf, S. L., Hashsham, S. A. & Tiedje, J. M. 2001. Interpreting 16S rDNA T-RFLP Data: application of self-organizing maps and principal component analysis to describe community dynamics and convergence. Microb. Ecol. 42:495-505.
16. Doucette, G. J., McGovern, E. R. & Babinchak, J. A. 1999. Algicidal bacteria active against Gymnodinium breve (Dinophyceae). I. bacterial isolation and characterization of killing activity. J. Phycol. 35:1447-54.
17. Eiler, A., Heinrich, F. & Bertilsson, S. 2012. Coherent dynamics and association networks among lake bacterioplankton taxa. ISME J. 6:330-42.
18. Faust, K. & Raes, J. 2012. Microbial interactions: from networks to models. Nat. Rev. Microbiol. 10:538-50.
19. Figueroa, R. I., Garces, E., Massana, R. & Camp, J. 2008. Description, host-specificity, and strain selectivity of the dinoflagellate parasite Parvilucifera sinerae sp. nov. (Perkinsozoa). Protist 159:563-78.
20. Fuhrman, J. A. 2009. Microbial community structure and its functional implications. Nature 459:193-9.
21. Fuhrman, J. A. & Steele, J. A. 2008. Community structure of marine bacterioplankton: patterns, networks, and relationships to function. Aquat. Microb. Ecol. 53:69-81.
22. Grossart, H. P., Czub, G. & Simon, M. 2006. Algae-bacteria interactions and their effects on aggregation and organic matter flux in the sea. Environ. Microbiol. 8:1074-84.
23. Hallegraeff, G. M. 1993. A review of harmful algal blooms and their apparent global increase. Phycologia 32:79-99.
24. Heisler, J., Glibert, P., Burkholder, J., Anderson, D., Cochlan, W., Dennison, W., Dortch, Q., Gobler, C., Heil, C. & Humphries, E. 2008. Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae 8:3-13.
25. Hwang, C. Y. & Cho, B. C. 2008. Ponticoccus litoralis gen. nov., sp nov., a marine bacterium in the family Rhodobacteraceae. Int. J. Syst. Evol. Microbiol. 58:1332-8.
26. Jones, K. L., Mikulski, C. M., Barnhorst, A. & Doucette, G. J. 2010. Comparative analysis of bacterioplankton assemblages from Karenia brevis bloom and nonbloom water on the west Florida shelf (Gulf of Mexico, USA) using 16S rRNA gene clone libraries. FEMS Microbiol. Ecol. 73:468-85.
27. Kaplan, C. W. & Kitts, C. L. 2003. Variation between observed and true terminal restriction fragment length is dependent on true TRF length and purine content. J. Microbiol. Meth. 54:121-5.
28. Kirchman, D. L. 2002. The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol. Ecol. 39:91-100.
29. Kodama, M., Doucette, G. J. & Green, D. H. 2006. Relationships between bacteria and harmful algae. In Granéli, E. & Turner, J. [Eds.] Ecology of Harmful Algae. Springer, Berlin, Heidelberg, pp. 243-55.
30. Lane, D. J. 1991. 16S/23S rRNA sequencing. In Stackebrandt, E. & Goodfellow, M. [Eds.] Nucleic Acid Techniques in Bacterial Systematics. John Wiley & Sons, Inc., New York, pp. 115-75.
31. Li, L., Wei, S. G., Huang, Z. L., Ye, W. H. & Cao, H. L. 2008. Spatial patterns and interspecific associations of three canopy species at different life stages in a subtropical forest, China. J. Integr. Plant Biol. 50:1140-50.
32. Li, H. B., Xing, P. & Wu, Q. L. L. 2012. Characterization of the bacterial community composition in a hypoxic zone induced by Microcystis blooms in Lake Taihu, China. FEMS Microbiol. Ecol. 79:773-84.
33. Lovdal, T., Tanaka, T. & Thingstad, T. F. 2007. Algal-bacterial competition for phosphorus from dissolved DNA, ATP, and orthophosphate in a mesocosm experiment. Limnol. Oceanogr. 52:1407-19.
34. Mannerova, S., Pantucek, R., Doskar, J., Svec, P., Snauwaert, C., Vancanneyt, M., Swings, J. & Sedlacek, I. 2003. Macrococcus brunensis sp nov., Macrococcus hajekii sp. nov. and Macrococcus lamae sp. nov., from the skin of llamas. Int. J. Syst. Evol. Microbiol. 53:1647-54.
35. Mayali, X. & Doucette, G. J. 2002. Microbial community interactions and population dynamics of an algicidal bacterium active against Karenia brevis (Dinophyceae). Harmful Algae 1:277-93.
36. McCune, B., Grace, J. B. & Urban, D. L. 2002. Analysis of Ecological Communities. MjM Software Design, Gleneden Beach, Oregon.
37. Moeseneder, M. M., Arrieta, J. M., Muyzer, G., Winter, C. & Herndl, G. J. 1999. Optimization of terminal-restriction fragment length polymorphism analysis for complex marine bacterioplankton communities and comparison with denaturing gradient gel electrophoresis. Appl. Environ. Microb. 65:3518-25.
38. Monchy, S., Grattepanche, J. D., Breton, E., Meloni, D., Sanciu, G., Chabé, M., Delhaes, L., Viscogliosi, E., Sime-Ngando, T. & Christaki, U. 2012. Microplanktonic community structure in a coastal system relative to a Phaeocystis bloom inferred from morphological and tag pyrosequencing methods. PLoS ONE 7:e39924.
39. Montoya, J. M., Pimm, S. L. & Sole, R. V. 2006. Ecological networks and their fragility. Nature 442:259-64.
40. Moran, M. A., Buchan, A., Gonzalez, J. M., Heidelberg, J. F., Whitman, W. B., Kiene, R. P., Henriksen, J. R. et al. 2004. Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature 432:910-3.
41. Noren, F., Moestrup, O. & Rehnstam-Holm, A. S. 1999. Parvilucifera infectans Noren et Moestrup gen. et sp nov (Perkinsozoa phylum nov.): a parasitic flagellate capable of killing toxic microalgae. Eur. J. Protistol. 35:233-54.
42. Osborn, A. M., Moore, E. R. B. & Timmis, K. N. 2000. An evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. Environ. Microbiol. 2:39-50.
43. Paerl, H. W. & Huisman, J. 2008. Climate - Blooms like it hot. Science 320:57-8.
44. Park, M. G., Yih, W. & Coats, D. W. 2004. Parasites and phytoplankton, with special emphasis on dinoflagellate infections. J. Eukaryot. Microbiol. 51:145-55.
45. Pruesse, E., Quast, C., Knittel, K., Fuchs, B. M., Ludwig, W., Peplies, J. & Glöckner, F. O. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35:7188-96.
46. Riemann, L., Steward, G. F. & Azam, F. 2000. Dynamics of bacterial community composition and activity during a mesocosm diatom bloom. Appl. Environ. Microb. 66:578-87.
47. Rooney-Varga, J. N., Giewat, M. W., Savin, M. C., Sood, S., LeGresley, M. & Martin, J. 2005. Links between phytoplankton and bacterial community dynamics in a coastal marine environment. Microb. Ecol. 49:163-75.
48. Ruan, Q., Dutta, D., Schwalbach, M. S., Steele, J. A., Fuhrman, J. A. & Sun, F. 2006. Local similarity analysis reveals unique associations among marine bacterioplankton species and environmental factors. Bioinformatics 22:2532-8.
49. Sapp, M., Schwaderer, A. S., Wiltshire, K. H., Hoppe, H. G., Gerdts, G. & Wichels, A. 2007. Species-specific bacterial communities in the phycosphere of microalgae? Microb. Ecol. 53:683-99.
50. 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. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microb. 75:7537-41.
51. Schluter, D. 1984. A variance test for detecting species associations, with some example applications. Ecology 65:998-1005.
52. Seibold, A., Wichels, A. & Schutt, C. 2001. Diversity of endocytic bacteria in the dinoflagellate Noctiluca scintillans. Aquat. Microb. Ecol. 25:229-35.
53. Sellner, K. G., Doucette, G. J. & Kirkpatrick, G. J. 2003. Harmful algal blooms: causes, impacts and detection. J. Ind. Microbiol. Biot. 30:383-406.
54. Seyedsayamdost, M. R., Case, R. J., Kolter, R. & Clardy, J. 2011. The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat. Chem. 3:331-5.
55. Shi, L. M., Cai, Y. F., Li, P. F., Yang, H. W., Liu, Z. L., Kong, L. D., Yu, Y. & Kong, F. X. 2009. Molecular identification of the colony-associated cultivable bacteria of the cyanobacterium Microcystis aeruginosa and their effects on algal growth. J. Freshw. Ecol. 24:211-8.
56. Shyu, C., Soule, T., Bent, S. J., Foster, J. A. & Forney, L. J. 2007. MiCA: a web-based tool for the analysis of microbial communities based on terminal-restriction fragment length polymorphisms of 16S and 18S rRNA genes. Microb. Ecol. 53:562-70.
57. Steele, J. A., Countway, P. D., Xia, L., Vigil, P. D., Beman, J. M., Kim, D. Y., Chow, C. E. T., Sachdeva, R., Jones, A. C. & Schwalbach, M. S. 2011. Marine bacterial, archaeal and protistan association networks reveal ecological linkages. ISME J. 5:1414-25.
58. Strom, S. L. 2008. Microbial ecology of ocean biogeochemistry: a community perspective. Science 320:1043.
59. Tada, Y., Taniguchi, A., Nagao, I., Miki, T., Uematsu, M., Tsuda, A. & Hamasaki, K. 2011. Differing growth responses of major phylogenetic groups of marine bacteria to natural phytoplankton blooms in the western North Pacific Ocean. Appl. Environ. Microb. 77:4055-65.
60. Tameishi, M., Yamasaki, Y., Nagasoe, S., Shimasaki, Y., Oshima, Y. & Honjo, T. 2009. Allelopathic effects of the dinophyte Prorocentrum minimum on the growth of the bacillariophyte Skeletonema costatum. Harmful Algae 8:421-9.
61. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Bio. Evol. 28:2731-9.
62. Teeling, H., Fuchs, B. M., Becher, D., Klockow, C., Gardebrecht, A., Bennke, C. M., Kassabgy, M., Huang, S., Mann, A. J. & Waldmann, J. 2012. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336:608-11.
63. Tillmann, U., Alpermann, T., John, U. & Cembella, A. 2008. Allelochemical interactions and short-term effects of the dinoflagellate Alexandrium on selected photoautotrophic and heterotrophic protists. Harmful Algae 7:52-64.
64. Tillmann, U. & Hansen, P. J. 2009. Allelopathic effects of Alexandrium tamarense on other algae: evidence from mixed growth experiments. Aquat. Microb. Ecol. 57:101-12.
65. Utermöhl, H. 1931. Neue Wege in der quantitativen Erfassung des Planktons. Verh. Int. Verein. Theor. Angew. Limnol. 5:567-96.
66. Zhao, G., Du, J., Jia, Y., Lv, Y., Han, G. & Tian, X. 2012. The importance of bacteria in promoting algal growth in eutrophic lakes with limited available phosphorus. Ecol. Eng. 42:107-11.