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Growth and succession patterns of major phylogenetic groups of marine bacteria during a mesocosm diatom bloom

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Abstract

Our objective was to track microbial processes associated with serial degradation of organic matter derived from algal blooms. To do this, we analyzed population fluctuations and growth responses of major phylogenetic groups of free-living marine bacteria. We used bromodeoxyuridine immunocytochemistry–fluorescence in situ hybridization methodology to examine marine bacterial community development during and after a diatom bloom in a mesocosm. We revealed that the Roseobacter/Rhodobacter, SAR11, Alteromonas, and Bacteroidetes groups were clearly major phylotypes responsible for most free-living bacterial biomass and production throughout the experiment. The clearest bacterial response was a proliferation of the Alteromonas group (cells with large volumes) during development of the bloom (up to 30 % of actively growing cells). Populations of these bacteria declined sharply thereafter, likely due to grazing. Alteromonas group responses suggest that these bacteria strongly influenced the flux of organic matter at an early bloom stage. The growth potential of Bacteroidetes was relatively large as the bloom peaked; this early development probably contributed to the initial stage of bloom decomposition. In contrast, the contribution of Roseobacter/Rhodobacter to total bacterial production increased at a late stage of decomposing of the bloom. The contributions of Betaproteobacteria, SAR11, and SAR86 groups to total bacterial abundance and production were relatively minor throughout the experiment. These results imply that the ability to utilize organic matter derived from diatoms varies among bacterial phylotypes, and, frequently, less abundant but ecological specialist taxa such as Alteromonas may play major roles in the flux of organic matter during diatom blooms.

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References

  • Acinas SG, Anton J, Rodriguez-Valera F (1999) Diversity of free-living and attached bacteria in offshore western Mediterranean waters as depicted by analysis of genes encoding 16S rRNA. Appl Environ Microbiol 65:514–522

    Google Scholar 

  • Alldredge AL, Passow U, Logan BE (1993) The abundance of a class of large, transparent organic particles in the ocean. Deep Sea Res 40:1131–1140

    Article  Google Scholar 

  • Allers E, Gomaz-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

    Article  Google Scholar 

  • Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56:1919–1925

    Google Scholar 

  • Azam F (1998) Microbial control of oceanic carbon flux: the plot thickens. Science 280:694–696

    Article  Google Scholar 

  • Beardsley C, Pernthaler J, Wosniok W, Amann R (2003) Are readily cultured bacteria in coastal North Sea waters suppressed by selective grazing mortality? Appl Environ Microbiol 69:2624–2630

    Article  Google Scholar 

  • del Giorgio PA, Gasol JM, Vaqué D, Mura P, Agustí S, Duarte CM (1996) Bacterioplankton community structure: protists control net production and the proportion of active bacteria in a coastal marine community. Limnol Oceanogr 41:1169–1179

    Article  Google Scholar 

  • Eilers H, Pernthaler J, Amann R (2000a) Succession of pelagic marine bacteria during enrichment: a close look at cultivation-induced shifts. Appl Environ Microbiol 66:4634–4640

    Article  Google Scholar 

  • Eilers H, Pernthaler J, Glöckner FO, Amann R (2000b) Culturability and in situ abundance of pelagic bacteria from the North Sea. Appl Environ Microbiol 66:3044–3051

    Article  Google Scholar 

  • Fandino LB, Riemann L, Steward GF, Long RA, Azam F (2001) Variations in bacterial community structure during a dinoflagellate bloom analyzed by DGGE and 16S rDNA sequencing. Aquat Microb Ecol 23:119–130

    Article  Google Scholar 

  • Giuliano L, De Domenico M, De Domenico E, Höfle MG, Yakimov MM (1999) Identification of culturable oligotrophic bacteria within naturally occurring bacterioplankton communities of the Ligurian Sea by 16S rRNA sequencing and probing. Microb Ecol 37:77–85

    Article  Google Scholar 

  • Gonzalez JM, Sherr EB, Sherr BF (1990) Size-selective grazing on bacteria by natural assemblages of estuarine flagellates and ciliates. Appl Environ Microbiol 56:583–589

    Google Scholar 

  • Grossart HP, Levold F, Allgaier M, Simon M, Brinkhoff T (2005) Marine diatom species harbor distinct bacterial communities. Environ Microbiol 7:860–873

    Article  Google Scholar 

  • Hamasaki K (2006) Comparison of bromodeoxyuridine immunoassay with tritiated thymidine radioassay for measuring bacterial productivity in oceanic waters. J Oceanogr 62:793–799

    Article  Google Scholar 

  • Holm-Hansen O, Lorenzen CJ, Holmes RW, Strickland JDH (1965) Fluorometric determination of chlorophyll. J Cons Perm Int Explor Mer 30:3–15

    Google Scholar 

  • Mague TH, Friberg E, Hughes DJ, Morris I (1980) Extracellular release of carbon by marine phytoplankton; a physiological approach. Limnol Oceanogr 25:262–279

    Article  Google Scholar 

  • Malmstrom RR, Kiene RP, Kirchman DL (2004) Identification and enumeration of bacteria assimilating dimethylsulfoniopropionate (DMSP) in the North Atlantic and Gulf of Mexico. Limnol Oceanogr 49:597–606

    Article  Google Scholar 

  • Manz W, Amann R, Ludwig W, Wagner M, Schleifer KH (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: problems and solutions. Syst Appl Microbiol 15:593–600

    Article  Google Scholar 

  • Manz W, Amann R, Ludwig W, Vancanneyt M, Schleifer KH (1996) Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum CytophagaFlavobacterBacteroides in the natural environment. Microbiology 142:1097–1106

    Article  Google Scholar 

  • Marr D, Hildreth EC (1980) Theory of edge detection. Proc R Soc Lond B 207:187–217

    Article  Google Scholar 

  • McCarren J, Becker JW, Repeta DJ, Shi Y, Young CR, Malmstrom RR, Chisholm SW, Delong EF (2010) Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea. Proc Natl Acad Sci USA 107:16420–16427

    Article  Google Scholar 

  • Middelboe M, Jørgensen NOG, Kroer N (1996) Effects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton. Appl Environ Microbiol 62:1991–1997

    Google Scholar 

  • Monger BC, Landry MR (1991) Prey-size dependency of grazing by free-living marine flagellates. Mar Ecol Prog Ser 74:239–248

    Article  Google Scholar 

  • Neef A (1997) Anwendung der in situ-Einzelzell-Identifizierung von Bakterien zur Populationsanalyse in komplexen mikrobiellen Biozönosen. Dissertation, Technische Universität München

  • Ogawa H, Fukuda R, Koike I (1999) Vertical distributions of dissolved organic carbon and nitrogen in the Southern Ocean. Deep Sea Res I 46:1809–1826

    Article  Google Scholar 

  • Pinhassi J, Sala MM, Havskum H, Peters F, Guadayol Ò, Malits A, Marrase CL (2004) Changes in bacterioplankton composition under different phytoplankton regimens. Appl Environ Microbiol 70:6753–6766

    Article  Google Scholar 

  • Pukall R, Päuker O, Buntefuß D, Ulrichs G, Lebaron P, Bernard L, Guindulain T, Vives-Rego J, Stackebrandt E (1999) High sequence diversity of Alteromonas macleodii-related cloned and cellular 16S rDNAs from a Mediterranean seawater mesocosm experiment. FEMS Microbiol Ecol 28:335–344

    Article  Google Scholar 

  • Rappé MS, Connon SA, Vergin KL, Giovannoni S (2002) Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418:630–633

    Article  Google Scholar 

  • Riemann L, Steward GF, Azam F (2000) Dynamics of bacterial community composition and activity during a mesocosm diatom bloom. Appl Environ Microbiol 66:578–587

    Article  Google Scholar 

  • Schäfer H, Servais P, Muyzer G (2000) Successional changes in the genetic diversity of a marine assemblage during confinement. Arch Microbiol 173:138–145

    Article  Google Scholar 

  • Sieracki ME, Viles CL, Webb KL (1989) Algorithm to estimate cell biovolume using image analyzed microscopy. Cytometry 10:551–557

    Article  Google Scholar 

  • Simon M, Azam F (1989) Protein content and protein synthesis rates of planktonic marine bacteria. Mar Ecol Prog Ser 51:201–213

    Article  Google Scholar 

  • Smith DC, Steward GF, Long RA, Azam F (1995) Bacterial mediation of carbon fluxes during a diatom bloom in a mesocosm. Deep Sea Res II 42:75–97

    Article  Google Scholar 

  • Steward GF, Azam F (1999) Bromodeoxyuridine as an alternative to H-3-thymidine for measuring bacterial productivity in aquatic samples. Aquat Microb Ecol 19:57–66

    Article  Google Scholar 

  • Suzuki R, Ishimaru T (1990) An improved method for the determination of phytoplankton chlorophyll using N, N-dimethylformamide. J Oceanogr 46:190–194

    Google Scholar 

  • Tada Y, Taniguchi A, Hamasaki K (2009) Phylotype-specific productivity of marine bacterial populations in eutorphic seawater, as revealed by bromodeoxyuridine immunocytochemistry combined with fluorescence in situ hybridization. Microbes Environ 24:315–321

    Article  Google Scholar 

  • Tada Y, Taniguchi A, Hamasaki K (2010) Phylotype-specific growth rates of marine bacteria measured by bromodeoxyuridine immunocytochemistry and fluorescence in situ hybridization. Aquat Microb Ecol 59:229–238

    Article  Google Scholar 

  • Tada Y, Taniguchi A, Nagao I, Miki T, Uematsu M, Tsuda A, Hamasaki K (2011) Differing growth response of major phylogenetic groups of marine bacteria to natural phytoplankton blooms in the western North Pacific. Appl Environ Microbiol 77:4055–4065

    Article  Google Scholar 

  • Vila M, Simó R, Kiene RP, Pinhassi J, González JM, Moran MA, Pedrós-Alió C (2004) Use of microautoradiography combined with fluorescence in situ hybridization to determine dimethylsulfoniopropionate incorporation by marine bacterioplankton taxa. Appl Environ Microbiol 70:4648–4657

    Article  Google Scholar 

  • Wallner G, Amann R, Beisker W (1993) Optimizing fluorescent in situ-hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14:136–143

    Article  Google Scholar 

  • Zubkov MV, Fuchs BM, Archer SD, Kiene RP, Amann R, Burkill PA (2001) Linking the composition of bacterioplankton to rapid turnover of dissolved dimethylsulfoniopropionate in an algal bloom in the North Sea. Environ Microbiol 3:304–311

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Associate Prof. H. Ogawa of the University of Tokyo, Japan for permitting us to perform DOC analysis in his laboratory and to Prof. S. Taguchi of Soka University, Japan, for POC analysis. We are grateful to Prof. N. Ramaiah of the National Institute of Oceanography, India, and Prof. K. Kogure, Prof. T. Nagata, and Prof. K. Furuya of the University of Tokyo, for valuable comments on the manuscript. This research was supported by the Japan Society for the Promotion of Science (JSPS) Research Fellowships for Young Scientists (No. 192357) to Y.T. and grants-in-aid (No. 17201004, 18310011, 18201003, and 19030006) from JSPS to K.H.

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Correspondence to Koji Hamasaki.

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Tada, Y., Taniguchi, A., Sato-Takabe, Y. et al. Growth and succession patterns of major phylogenetic groups of marine bacteria during a mesocosm diatom bloom. J Oceanogr 68, 509–519 (2012). https://doi.org/10.1007/s10872-012-0114-z

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  • DOI: https://doi.org/10.1007/s10872-012-0114-z

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