Illumina sequencing-based analysis of free-living bacterial community dynamics during an Akashiwo sanguine bloom in Xiamen sea, China

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Yang, Caiyun ^a   Li, Yi ^a   Zhou, Benjamin ^b   Zhou, Yanyan ^a   Zheng, Wei ^a   Tian, Yun ^a   Van Nostrand, Joy D ^c   Wu, Liyou ^c   He, Zhili ^c   Zhou, Jizhong ^c,d,e   Zheng, Tianling ^a  

^a BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^b Stanford University   (United States)

^c UNIVERSITY OF OKLAHOMA   (United States)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^e TSINGHUA UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S; SEA WATER;

ALPHAPROTEOBACTERIA; BACTERIUM; CHINA; DINOFLAGELLATE; GAMMAPROTEOBACTERIA; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGH THROUGHPUT SEQUENCING; ISOLATION AND PURIFICATION; MICROBIOLOGY; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS;

ALPHAPROTEOBACTERIA; BACTERIA; CHINA; DINOFLAGELLIDA; GAMMAPROTEOBACTERIA; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SEAWATER; SEQUENCE ANALYSIS, RNA;

EID: 84923358931     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep08476     Document Type: Article

References (88)

1. Anderson, D. M., Glibert, P. M. & Burkholder, J. M. Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25, 704-726 (2002).
2. Yang, C. et al. Bacterial community dynamics during a bloom caused by Akashiwo sanguinea in the Xiamen Sea Area, China. Harmful Algae 20, 132-141 (2012).
3. Cai, W.,Wang, H., Tian, Y., Chen, F. & Zheng, T. Influence of a bacteriophage on the population dynamics of toxic dinoflagellates by lysis of algicidal bacteria. Appl. Environ. Microb. 77, 7837-7840 (2011).
4. Li, Y. et al. Toxicity of algicidal extracts from Mangrovimonas yunxiaonensis strain LY01 on a HAB causing Alexandrium tamarense. J. Hazard. Mater. 278, 372-381 (2014).
5. Wang, B. et al. An algicidal protein produced by bacterium isolated from the Donghai Sea, China. Harmful Algae 13, 83-88 (2012).
6. Li, Y. et al. Towards molecular, physiological, and biochemical understanding of photosynthetic inhibition and oxidative stress in the toxic Alexandrium tamarense induced by a marine bacterium. Appl. Microbio. Biot. 98, 4637-4652 (2014).
7. Anderson, G. & Zeutschel, R. Release of dissolved organic matter by marine phytoplankton in coastal and offshore areas of the northeast Pacific Ocean. Limnol. Oceanogr. 15, 402-407 (1970).
8. Biddanda, B. & Benner, R. Carbon, nitrogen, and carbohydrate fluxes during the production of particulate and dissolved organic matter by marine phytoplankton. Limnol. Oceanogr 42, 506-518 (1997).
9. Agustí, S. & Duarte, C. Phytoplankton lysis predicts dissolved organic carbon release in marine plankton communities. Biogeosciences 10, 1259-1264 (2013).
10. Karner, M. & Herndl, G. Extracellular enzymatic activity and secondary production in free-living and marine-snow-associated bacteria. Mar. Biol. 113, 341-347 (1992).
11. Riemann, L., Steward, G. F. & Azam, F. Dynamics of Bacterial Community Composition and Activity during a Mesocosm Diatom Bloom. Appl. Environ. Microb. 66, 578-587 (2000).
12. Middelboe, M., Søndergaard, M., Letarte, Y. & Borch, N. H. Attached and freeliving bacteria: Production and polymer hydrolysis during a diatom bloom. Microbial. Ecol. 29, 231-248 (1995).
13. Baines, S. B. & Pace, M. L. The production of dissolved organic matter by phytoplankton and its importance to bacteria: patterns across marine and freshwater systems. Limnol. Oceanogr. 36, 1078-1090 (1991).
14. Cole, J. J. Interactions between bacteria and algae in aquatic ecosystems. Annu. Rev. Ecol. 13, 291-314 (1982).
15. Ferrier, M., Martin, J. & Rooney-Varga, J. Stimulation of Alexandrium fundyense growth by bacterial assemblages from the Bay of Fundy. J. Appl. microbial. 92, 706-716 (2002).
16. Li, Y. et al. Tenacibaculum xiamenense sp. nov., an algicidal species isolated from coastal seawater. Int. J. Syst. Evol. Micr. 63, 3481-3486 (2013).
17. Zheng, X. et al. A marine algicidal actinomycete and its active substance against the harmful algal bloom species Phaeocystis globosa. Appl. Microbiol. Biot. 97, 9207-9215 (2013).
18. González, J. M. et al. Bacterial community structure associated with a dimethylsulfoniopropionate-producing North Atlantic algal bloom. Appl. Environ. Microb. 66, 4237-4246 (2000).
19. Rooney-Varga, J. N. et al. Links between phytoplankton and bacterial community dynamics in a coastal marine environment. Microb. Ecol., 49, 163-175 (2005).
20. Larsen, A. et al. Spring phytoplankton bloom dynamics in Norwegian coastal waters: Microbial community succession and diversity. Limnol. Oceanogr. 49, 180-190 (2004).
21. Teeling, H. et al. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336, 608-611 (2012).
22. Morris, R., Longnecker, K. G. & iovannoni, S. Pirellula and OM43 are among the dominant lineages identified in an Oregon coast diatom bloom. Environ. microbial. 8, 1361-1370 (2006).
23. Rinta-Kanto, J. M., Sun, S., Sharma, S., Kiene, R. P. & Moran, M. A. Bacterial community transcription patterns during a marine phytoplankton bloom. Environ. microbial. 14, 228-239 (2012).
24. Howard, E. C. et al. Changes in dimethylsulfoniopropionate demethylase gene assemblages in response to an induced phytoplankton bloom. Appl. Environ. Microb. 77, 524-531 (2011).
25. Li, N. et al. Metagenome of microorganisms associated with the toxic Cyanobacteria Microcystis aeruginosa analyzed using the 454 sequencing platform. Chin. J. Oceanol. Limnol. 29, 505-513 (2011).
26. Tada, Y., Taniguchi, A., Sato-Takabe, Y. & Hamasaki, K. Growth and succession patterns of major phylogenetic groups of marine bacteria during a mesocosm diatom bloom. J. Oceanogr. 68, 509-519 (2012).
27. Vasileiadis, S. et al. Soil bacterial diversity screening using single 16S rRNA gene V regions coupled with multi-million read generating sequencing technologies. PloS one 7, e42671 (2012).
28. Matsubara, T. et al. Effects of temperature, salinity, and irradiance on the growth of the dinoflagellate Akashiwo sanguinea. J. Exp. Mar. Biol. Ecol. 342, 226-230 (2007).
29. Yamasaki, Y. et al.Growth inhibition and formation of morphologically abnormal cells of Akashiwo sanguinea (Hirasaka) G. Hansen et Moestrup by cell contact with Cochlodinium polykrikoides Margalef. Mar. Biol. 152, 157-163 (2007).
30. Qiu, X. et al. Growth interactions between the raphidophyte Chattonella antiqua and the dinoflagellate Akashiwo sanguinea. Harmful Algae 11, 81-87 (2011).
31. Qiu, X. et al. Allelopathy of the raphidophyte Heterosigma akashiwo against the dinoflagellate Akashiwo sanguinea is mediated via allelochemicals and cell contact. Mar. Ecol. Prog. Ser. 446, 107-118 (2012).
32. Du, X., Peterson, W., McCulloch, A. & Liu, G. An unusual bloom of the dinoflagellate Akashiwo sanguinea off the central Oregon, USA, coast in autumn 2009. Harmful Algae 10, 784-793 (2011).
33. Jessup, D. A. et al. Mass stranding of marine birds caused by a surfactantproducing red tide. PLoS One 4, e4550 (2009).
34. Ahn, S. J., Costa, J. & Emanuel, J. R. PicoGreen Quantitation of DNA: Effective Evaluation of Samples Pre-or Psost-PCR. Nucleic. Acids. Res. 24, 2623-2625 (1996).
35. Caporaso, J. G. et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME. J. 6, 1621-1624 (2012).
36. Kong, Y. Btrim: a fast, lightweight adapter and quality trimming program for nextgeneration sequencing technologies. Genomics 98, 152-153 (2011).
37. Magoč, T. & Salzberg, S. L. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957-2963 (2011).
38. Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194-2200 (2011).
39. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461 (2010).
40. Cole, J. R. et al. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic. Acids. Res. 37, 141-145 (2009).
41. Team, R. D. C. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. ISBN 3-900051-07-0 (2008) Available at: http://www. R-project. org. (Accessed: 15th January 2013)
42. Clarke, K. R. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18, 117-143 (1993).
43. Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral. Ecol. 26, 32-46 (2001).
44. Mielke, P. W., Berry, K. J., Brockwell, P. J. & Williams, J. S. A class of nonparametric tests based on multiresponse permutation procedures. Biometrika 68, 720-724 (1981).
45. Dixon, P. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927-930 (2003).
46. Hansen, P. J. Effect of high pH on the growth and survival of marine phytoplankton: implications for species succession. Aquat. Microb. Ecol. 28, 279-288 (2002).
47. Qasim, S., Bhattathiri, P. & Devassy, V. The influence of salinity on the rate of photosynthesis and abundance of some tropical phytoplankton. Mar. Biol. 12, 200-206 (1972).
48. DeLong, E. F., Franks, D. G.&Alldredge, A. L. Phylogenetic diversity of aggregateattached vs. free-living marine bacterial assemblages. Limnol. Oceanogr. 38, 924-934 (1993).
49. West, N. J., Obernosterer, I., Zemb,O.& Lebaron, P. Major differences of bacterial diversity and activity inside and outside of a natural iron-fertilized phytoplankton bloom in the Southern Ocean. Environ. Microbiol. 10, 738-756 (2008).
50. Wong, K., Lee, J. H. & Hodgkiss, I. A simple model for forecast of coastal algal blooms. Estuar. Coast. Shelf. S. 74, 175-196 (2007).
51. Cullen, J. J. & MacIntyre, J. G. Behavior, physiology and the niche of depthregulating phytoplankton. Nato. Asi. Series. G. Ecol. Sci. 41, 559-580 (1998).
52. Watanabe, M. et al. Generation of a Chattonella antiqua bloom by imposing a shallow nutricline in a mesocosm. Limnol. Oceanogr. 40, 1447-1480 (1995).
53. Paerl, H. [Cyanobacterial harmful algal blooms: state of the science and research needs] Nutrient and other environmental controls of harmful cyanobacterial blooms along the freshwater-marine continuum [217-237] (Springer, Berlin, 2008).
54. Yergeau, E., Newsham, K. K., Pearce, D. A. & Kowalchuk, G. A. Patterns of bacterial diversity across a range of Antarctic terrestrial habitats. Environ. Microbial. 9, 2670-2682 (2007).
55. Fogg, G. The ecological significance of extracellular products of phytoplankton photosynthesis. Bot. Mar. 26, 3-14 (1983).
56. Sarmento, H. & Gasol, J. M. Use of phytoplankton-derived dissolved organic carbon by different types of bacterioplankton. Environ. Microbial. 14, 2348-2360 (2012).
57. Molloy, S. Marine microbiology: SAR86: streamlined for success. Nat. Rev. Microbiol. 10, 82-83 (2012).
58. Dupont, C. L. et al. Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage. ISME. J. 6, 1186-1199 (2011).
59. Schattenhofer, M. et al. Latitudinal distribution of prokaryotic picoplankton populations in the Atlantic Ocean. Environ. Microbial. 11, 2078-2093 (2009).
60. Giovannoni, S. J., Britschgi, T. B., Moyer, C. L. & Field, K. G. Genetic diversity in Sargasso Sea bacterioplankton. Nature 345, 60-63 (1990).
61. Giovannoni, S. & Rappé, M. [Ecological and Applied Microbiology] Evolution, diversity, andmolecular ecology of marine prokaryotes [47-84] (Wiley, New York, 2000).
62. Spring, S. et al. Taxonomy and evolution of bacteriochlorophyll a-containing members of the OM60/NOR5 clade of marine gammaproteobacteria: description of Luminiphilus syltensis gen. nov., sp. nov., reclassification of Haliea rubra as Pseudohaliea rubra gen. nov., comb. nov., and emendation of Chromatocurvus halotolerans. BMC Microbiol. 13, 118 (2013).
63. Cho, J. C. et al. Polyphyletic photosynthetic reaction centre genes in oligotrophic marine Gammaproteobacteria. Environ. Microbial. 9, 1456-1463 (2007).
64. Beardsley, C., Pernthaler, J., Wosniok, W. & Amann, R. Are readily culturable bacteria in coastal North Sea waters suppressed by selective grazing mortality? Appl. Environ. Microb. 69, 2624-2630 (2003).
65. Pernthaler, A. & Pernthaler, J. Diurnal variation of cell proliferation in three bacterial taxa from coastal North Sea waters. Appl. Environ. Microb. 71, 4638-4644 (2005).
66. Yan, S. et al. Biogeography and phylogeny of the NOR5/OM60 clade of Gammaproteobacteria. Syst. Appl. Microbiol. 32, 124-139 (2009).
67. Hahn, M. W. Description of seven candidate species affiliated with the phylum Actinobacteria, representing planktonic freshwater bacteria. Int. J. Syst. Evol. Microbiol. 59, 112-117 (2009).
68. Kang, I. et al.Genome sequence of "Candidatus Aquiluna" sp. strain IMCC13023, a marine member of the actinobacteria isolated from an Arctic Fjord. J. Bacteriol. 194, 3550-3551 (2012).
69. Rappé,M. S., Vergin, K. & Giovannoni, S. J. Phylogenetic comparisons of a coastal bacterioplankton community with its counterparts in open ocean and freshwater systems. FEMS. Microbiol. Ecol. 33, 219-232 (2000).
70. Giovannoni, S. J. et al. The small genome of an abundant coastal ocean methylotroph. Environ. Microbial. 10, 1771-1782 (2008).
71. Heikes, B. G. et al. Atmospheric methanol budget and ocean implication. Global. Biogeochem. Cy. 16, 1133, doi:10.1029/2002GB001895 (2002).
72. Rinta-Kanto, J. M. et al. Analysis of sulfur-related transcription by Roseobacter communities using a taxon-specific functional gene microarray. Environ. Microbial. 13, 453-467 (2011).
73. Biers, E. J., Sun, S. & Howard, E. C. Prokaryotic genomes and diversity in surface ocean waters: interrogating the global ocean sampling metagenome. Appl. Environ. Microb. 75, 2221-2229 (2009).
74. Prasad, S. et al. Diversity of Chemotactic Heterotrophic Bacteria Associated with Arctic Cyanobacteria. Curr. Microbial. 66, 64-71 (2013).
75. Nedashkovskaya, O. I., Vancanneyt, M., Kim, S. B. & Zhukova, N. V. Winogradskyella echinorum sp. nov., a marine bacterium of the family Flavobacteriaceae isolated from the sea urchin Strongylocentrotus intermedius. Int. J. Syst. Evol. Microbiol. 59, 1465-1468 (2009).
76. Pinhassi, J., Nedashkovskaya, O. I., Hagström, Å. & Vancanneyt, M. Winogradskyella rapida sp. nov., isolated from protein-enriched seawater. Int. J. Syst. Evol. Microbiol. 59, 2180-2184 (2009).
77. Cheng, C. et al. Pyrosequencing Reveals the Bacterial Community during Microcystis water Bloom in Guanting Reservoir, Beijing. Pro. Eng. 18, 341-346 (2011).
78. Schattenhofer, M. et al. Latitudinal distribution of prokaryotic picoplankton populations in the Atlantic Ocean. Environ. Microbiol. 11, 2078-93 (2009).
79. Bryan, M. J. et al. Evidence for the intense exchange of MazG in marine cyanophages by horizontal gene transfer. PLoS One 3, e2048 (2008).
80. Chen, W. M., Lin, C. Y. & Sheu, S. Y. Investigating antimicrobial activity in Rheinheimera sp. due to hydrogen peroxide generated by l-lysine oxidase activity. Enzyme. Microb. Tech. 46, 487-493 (2010).
81. Fernandes, N. et al. Genomes and virulence factors of novel bacterial pathogens causing bleaching disease in the marine red alga Delisea pulchra. PloS one 6, e27387 (2011).
82. Jeong, S. Y., Ishida, K., Ito, Y., Okada, S. & Murakami, M. Bacillamide, a novel algicide from the marine bacterium, Bacillus sp. SY-1, against the harmful dinoflagellate, Cochlodinium polykrikoides. Tetrahedron letters 44, 8005-8007 (2003).
83. Kawafune, K., Hongoh, Y., Hamaji, T. & Nozaki, H. Molecular identification of rickettsial endosymbionts in the non-phagotrophic volvocalean green algae. PLoS One 7, e31749 (2012).
84. Palacios, L., Arahal, D. R., Reguera, B. & Marin, I. Hoeflea alexandrii sp. nov., isolated from the toxic dinoflagellate Alexandrium minutum AL1V. Int. J. Syst. Evol. Microbiol. 56, 1991-1995 (2006).
85. Zarnowski, R., Felske, A., Ellis, R. J., Geuns, J. M. & Pietr, S. J. A Methylobacterium-like organism from algal crusts covering silicone rubber electric insulators in Africa. J. Appl. Microbiol. 93, 1012-1019 (2002).
86. Goecke, F., Thiel, V., Wiese, J., Labes, A. & Imhoff, J. F. Algae as an important environment for bacteria-phylogenetic relationships among new bacterial species isolated from algae. Phycologia 52, 14-24 (2013).
87. Wagner-Dobler, I. et al. The complete genome sequence of the algal symbiont Dinoroseobacter shibae: a hitchhiker's guide to life in the sea. ISME. J. 4, 61-77 (2010).
88. Williams, T. J. et al. The role of planktonic Flavobacteria in processing algal organic matter in coastal East Antarctica revealed using metagenomics and metaproteomics. Environ. Microbiol. 15, 1302-1317 (2013).