Bacterial community dynamics during polysaccharide degradation at contrasting sites in the Southern and Atlantic Oceans

Environmental Microbiology

Volumn 17, Issue 10, 2015, Pages 3822-3831

  Wietz, Matthias ^a   Wemheuer, Bernd ^b   Simon, Heike ^a   Giebel, Helge Ansgar ^a   Seibt, Maren A ^a   Daniel, Rolf ^b   Brinkhoff, Thorsten ^a   Simon, Meinhard ^a  

^a UNIVERSITY OF OLDENBURG   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALGINIC ACID; CHITIN; GLUCURONIC ACID; GULURONIC ACID; HEXURONIC ACID; POLYSACCHARIDE; RNA 16S;

ALPHAPROTEOBACTERIA; ALTEROMONADACEAE; ANTARCTICA; ATLANTIC OCEAN; BACTEROIDETES; COLD; ECOSYSTEM; GENETICS; GEOGRAPHY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL CONSORTIUM; PHYSIOLOGY; SEA;

ALGINATES; ALPHAPROTEOBACTERIA; ALTEROMONADACEAE; ANTARCTIC REGIONS; ATLANTIC OCEAN; BACTEROIDETES; CHITIN; COLD TEMPERATURE; ECOSYSTEM; GEOGRAPHY; GLUCURONIC ACID; HEXURONIC ACIDS; MICROBIAL CONSORTIA; OCEANS AND SEAS; POLYSACCHARIDES; RNA, RIBOSOMAL, 16S;

EID: 85027932580     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12842     Document Type: Article

References (74)

1. Allers, E., Niesner, C., Wild, C., and Pernthaler, J. (2008) Microbes enriched in seawater after addition of coral mucus. Appl Environ Microbiol 74: 3274–3278.
2. Amon, R.M.W., and Benner, R. (1994) Rapid cycling of high-molecular-weight dissolved organic matter in the ocean. Nature 369: 549–552.
3. Arnosti, C., Steen, A.D., Ziervogel, K., Ghobrial, S., and Jeffrey, W.H. (2011) Latitudinal gradients in degradation of marine dissolved organic carbon. PLoS ONE 6: e28900.
4. Arnosti, C., Fuchs, B.M., Amann, R., and Passow, U. (2012) Contrasting extracellular enzyme activities of particle-associated bacteria from distinct provinces of the North Atlantic Ocean. Front Microbiol 3: 425.
5. Azam, F., and Malfatti, F. (2007) Microbial structuring of marine ecosystems. Nat Rev Microbiol 5: 782–791.
6. Beier, S., and Bertilsson, S. (2013) Bacterial chitin degradation – mechanisms and ecophysiological strategies. Front Microbiol 4: 149.
7. Benner, R., Pakulski, J., McCarthy, M., Hedges, J., and Hatcher, P. (1992) Bulk chemical characteristics of dissolved organic matter in the ocean. Science 255: 1561–1564.
8. Borch, N.H., and Kirchman, D.L. (1997) Concentration and composition of dissolved combined neutral sugars (polysaccharides) in seawater determined by HPLC-PAD. Mar Chem 57: 85–95.
9. Bragg, L., Stone, G., Imelfort, M., Hugenholtz, P., and Tyson, G.W. (2012) Fast, accurate error-correction of amplicon pyrosequences using Acacia. Nat Methods 9: 425–426.
10. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335–336.
11. Chi, W.-J., Chang, Y.-K., and Hong, S.-K. (2012) Agar degradation by microorganisms and agar-degrading enzymes. Appl Microbiol Biotechnol 94: 917–930.
12. Cottrell, M.T., and Kirchman, D.L. (2000) Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl Environ Microbiol 66: 1692–1697.
13. Cowie, G.L., and Hedges, J.I. (1984) Carbohydrate sources in a coastal marine environment. Geochim Cosmochim Acta 48: 2075–2087.
14. Davis, T.A., Volesky, B., and Mucci, A. (2003) A review of the biochemistry of heavy metal biosorption by brown algae. Water Res 37: 4311–4330.
15. D'Ambrosio, L., Ziervogel, K., Macgregor, B., Teske, A., and Arnosti, C. (2014) Composition and enzymatic function of particle-associated and free-living bacteria: a coastal/offshore comparison. ISME J 8: 2167–2179.
16. Doubet, R.S., and Quatrano, R.S. (1982) Isolation of marine bacteria capable of producing specific lyases for alginate degradation. Appl Environ Microbiol 44: 754–756.
17. Durkin, C.A., Mock, T., and Armbrust, E.V. (2009) Chitin in diatoms and its association with the cell wall. Eukaryot Cell 8: 1038–1050.
18. Edgar, R.C. (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460–2461.
19. Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., and Knight, R. (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194–2200.
20. Edwards, J.L., Smith, D.L., Connolly, J., McDonald, J.E., Cox, M.J., Joint, I., et al. (2010) Identification of carbohydrate metabolism genes in the metagenome of a marine biofilm community shown to be dominated by Gammaproteobacteria and Bacteroidetes. Genes 1: 371–384.
21. Eilers, H., Pernthaler, J., and Amann, R. (2000a) Succession of pelagic marine bacteria during enrichment: a close look at cultivation-induced shifts. Appl Environ Microbiol 66: 4634–4640.
22. Eilers, H., Pernthaler, J., Glöckner, F., and Amann, R. (2000b) Culturability and in situ abundance of pelagic bacteria from the North Sea. Appl Environ Microbiol 66: 3044–3051.
23. Fernández-Gómez, B., Richter, M., Schüler, M., Pinhassi, J., Acinas, S.G., González, J.M., and Pedrós-Alió, C. (2013) Ecology of marine Bacteroidetes: a comparative genomics approach. ISME J 7: 1026–1037.
24. Giebel, H.A., Brinkhoff, T., Zwisler, W., Selje, N., and Simon, M. (2009) Distribution of Roseobacter RCA and SAR11 lineages and distinct bacterial communities from the subtropics to the Southern Ocean. Environ Microbiol 11: 2164–2178.
25. Giovannoni, S.J., Tripp, H.J., Givan, S., Podar, M., Vergin, K.L., Baptista, D., et al. (2005) Genome streamlining in a cosmopolitan oceanic bacterium. Science 309: 1242–1245.
26. Gooday, G.W. (1990) The ecology of chitin degradation. Adv Microb Ecol 11: 387–430.
27. Guixa-Boixereu, N., Lysnes, K., and Pedros-Alio, C. (1999) Viral lysis and bacterivory during a phytoplankton bloom in a coastal water microcosm. Appl Environ Microbiol 65: 1949–1958.
28. Haynes, K., Hofmann, T.A., Smith, C.J., Ball, A.S., Underwood, G.J.C., and Osborn, A.M. (2007) Diatom-derived carbohydrates as factors affecting bacterial community composition in estuarine sediments. Appl Environ Microbiol 73: 6112–6124.
29. Jeuniaux, C., and Voss-Foucart, M.F. (1991) Chitin biomass and production in the marine environment. Biochem Syst Ecol 19: 347–356.
30. Kabisch, A., Otto, A., König, S., Becher, D., Albrecht, D., Schüler, M., et al. (2014) Functional characterization of polysaccharide utilization loci in the marine Bacteroidetes ‘Gramella forsetii’ KT0803. ISME J 8: 1492–1502.
31. Kirchman, D.L. (2008) Microbial Ecology of the Oceans. New York, NJ, USA: John Wiley & Sons.
32. Landa, M., Cottrell, M.T., Kirchman, D.L., Kaiser, K., Medeiros, P.M., Tremblay, L., et al. (2013) Phylogenetic and structural response of heterotrophic bacteria to dissolved organic matter of different chemical composition in a continuous culture study. Environ Microbiol 16: 1668–1681.
33. Lange, B., Wingender, J., and Winkler, U.K. (1989) Isolation and characterization of an alginate lyase from Klebsiella aerogenes. Arch Microbiol 152: 302–308.
34. Lebaron, P., Servais, P., Agogué, H., Courties, C., and 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.
35. Liu, Z., Lozupone, C., Hamady, M., Bushman, F.D., and Knight, R. (2007) Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Res 35: e120.
36. Longhurst, A.R. (1998) Ecological Geography of the Sea. San Diego, CA, USA: Academic Press.
37. McCarren, J., Becker, J.W., Repeta, D.J., Shi, Y., Young, C.R., Malmstrom, R.R., et al. (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.
38. Malmstrom, R.R., Cottrell, M.T., Elifantz, H., and Kirchman, D.L. (2005) Biomass production and assimilation of dissolved organic matter by SAR11 bacteria in the Northwest Atlantic Ocean. Appl Environ Microbiol 71: 2979–2986.
39. Manz, W., Amann, R., Ludwig, W., Wagner, M., and Schleifer, K.H. (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria – problems and solutions. Syst Appl Microbiol 15: 593–600.
40. Manz, W., Amann, R., Ludwig, W., Vancanneyt, M., and Schleifer, K.-H. (1996) Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum Cytophaga–Flavobacter–Bacteroides in the natural environment. Microbiology 142: 1097–1106.
41. Martin, M. (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet Journal 17: 10–12.
42. Mopper, K., Schultz, C.A., Chevolot, L., Germain, C., Revuelta, R., and Dawson, R. (1992) Determination of sugars in unconcentrated seawater and other natural waters by liquid chromatography and pulsed amperometric detection. Environ Sci Technol 26: 133–138.
43. Morris, R.M., Rappe, M.S., Connon, S.A., Vergin, K.L., Siebold, W.A., Carlson, C.A., and Giovannoni, S.J. (2002) SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420: 806–810.
44. Murray, A., Arnosti, C., De La Rocha, C., Grossart, H.-P., and Passow, U. (2007) Microbial dynamics in autotrophic and heterotrophic seawater mesocosms. II. Bacterioplankton community structure and hydrolytic enzyme activities. Aquat Microb Ecol 49: 123–141.
45. Neef, A. (1997) Anwendung der in situ Einzelzell-Identifizierung von Bakterien zur Populationsanalyse in komplexen mikrobiellen Biozönosen. PhD thesis. Munich, Germany: Technische Universität München.
46. Nelson, C.E., and Carlson, C.A. (2012) Tracking differential incorporation of dissolved organic carbon types among diverse lineages of Sargasso Sea bacterioplankton. Environ Microbiol 14: 1500–1516.
47. Neumann, A.M., Balmonte, J.P., Berger, M., Giebel, H.-A., Arnosti, C., Voget, S., et al. (2015) Different utilization of alginate and other algal polysaccharides by marine Alteromonas macleodii ecotypes. Environ Microbiol accepted.
48. Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O'Hara, R.B., et al. (2013) Vegan: community ecology package.
49. Pedler, B.E., Aluwihare, L.I., and Azam, F. (2014) Single bacterial strain capable of significant contribution to carbon cycling in the surface ocean. Proc Natl Acad Sci USA 111: 7202–7207.
50. Pernthaler, A., Pernthaler, J., and Amann, R. (2004) Sensitive multi-color fluorescence in situ hybridization for the identification of environmental microorganisms. In Molecular Microbial Ecology Manual. Kowalchuk, G.A., de Bruijn, F.J., Head, I.M., Akkermans, A.D., and van Elsas, J. (eds). Dordrecht, Netherlands: Kluwer Academic Publishers, pp. 2613–2627.
51. Piontek, J., Handel, N., De Bodt, C., Harlay, J., Chou, L., and Engel, A. (2011) The utilization of polysaccharides by heterotrophic bacterioplankton in the Bay of Biscay (North Atlantic Ocean). J Plankton Res 33: 1719–1735.
52. Pukall, R., Päuker, O., Buntefuß, D., Ulrichs, G., Lebaron, P., Bernard, L., et al. (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.
53. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., et al. (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41: D590–D596.
54. R Core Team (2012) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
55. Sarmento, H., and Gasol, J.M. (2012) Use of phytoplankton-derived dissolved organic carbon by different types of bacterioplankton. Environ Microbiol 14: 2348–2360.
56. Schäfer, H., Bernard, L., Courties, C., Lebaron, P., Servais, P., Pukall, R., et al. (2001) Microbial community dynamics in Mediterranean nutrient-enriched seawater mesocosms: changes in the genetic diversity of bacterial populations. FEMS Microbiol Ecol 34: 243–253.
57. Schwalbach, M.S., Tripp, H.J., Steindler, L., Smith, D.P., and Giovannoni, S.J. (2010) The presence of the glycolysis operon in SAR11 genomes is positively correlated with ocean productivity. Environ Microbiol 12: 490–500.
58. Sharma, A.K., Becker, J.W., Ottesen, E.A., Bryant, J.A., Duhamel, S., Karl, D.M., et al. (2013) Distinct dissolved organic matter sources induce rapid transcriptional responses in coexisting populations of Prochlorococcus, Pelagibacter and the OM60 clade. Environ Microbiol 16: 2815–2830.
59. Simon, M., Billerbeck, S., Kessler, D., Selje, N., and Schlingloff, A. (2012) Bacterioplankton communities in the Southern Ocean: composition and growth response to various substrate regimes. Aquat Microb Ecol 68: 13–28.
60. Souza, C.P., Almeida, B.C., Colwell, R.R., and Rivera, I.N. (2011) The importance of chitin in the marine environment. Mar Biotechnol 13: 823–830.
61. Steen, A.D., Hamdan, L.J., and Arnosti, C. (2008) Dynamics of dissolved carbohydrates in the Chesapeake Bay: insights from enzyme activities, concentrations, and microbial metabolism. Limnol Oceanogr 53: 936–947.
62. Tada, Y., Taniguchi, A., Nagao, I., Miki, T., Uematsu, M., Tsuda, A., and 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 Microbiol 77: 4055–4065.
63. Tang, K., Jiao, N., Liu, K., Zhang, Y., and Li, S. (2012) Distribution and functions of TonB-dependent transporters in marine bacteria and environments: implications for dissolved organic matter utilization. PLoS ONE 7: e41204.
64. Tanoue, E., and Handa, N. (1987) Monosaccharide composition of marine particles and sediments from the Bering Sea and northern North Pacific. Oceanol Acta 10: 91–99.
65. Teeling, H., Fuchs, B.M., Becher, D., Klockow, C., Gardebrecht, A., Bennke, C.M., et al. (2012) Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336: 608–611.
66. Thomas, F., Barbeyron, T., Tonon, T., Génicot, S., Czjzek, M., and Michel, G. (2012) Characterization of the first alginolytic operons in a marine bacterium: from their emergence in marine Flavobacteriia to their independent transfers to marine Proteobacteria and human gut Bacteroides. Environ Microbiol 14: 2379–2394.
67. von Wintzingerode, F., Göbel, U.B., and Stackebrandt, E. (1997) Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev 21: 213–229.
68. Wallner, G., Amann, R., and Beisker, W. (1993) Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14: 133–141.
69. Wang, Y., and Qian, P.-Y. (2009) Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. PLoS ONE 4: e7401.
70. Wemheuer, B., Güllert, S., Billerbeck, S., Giebel, H.-A., Voget, S., Simon, M., and Daniel, R. (2013) Impact of a phytoplankton bloom on the diversity of the active bacterial community in the southern North Sea as revealed by metatranscriptomic approaches. FEMS Microbiol Ecol 87: 378–389.
71. Weyland, H., Ruger, H.-J., and Schwarz, H. (1970) Zur Isolierung und Identifizierung mariner Bakterien. Ein Beitrag zur Standardisierung und Entwicklung adäquater Methoden. Veröff Inst Meeresforsch Bremerhaven 12: 269–296.
72. Yong, J.-J., Park, S.-J., Kim, H.-J., and Rhee, S.-K. (2007) Glaciecola agarilytica sp. nov., an agar-digesting marine bacterium from the East Sea, Korea. Int J Syst Evol Microbiol 57: 951–953.
73. Zhou, J., Bruns, M., and Tiedje, J. (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62: 316–322.
74. Zimmerman, A.E., Martiny, A.C., and Allison, S.D. (2013) Microdiversity of extracellular enzyme genes among sequenced prokaryotic genomes. ISME J 7: 1187–1199.