Bacterial community dynamics and activity in relation to dissolved organic matter availability during sea-ice formation in a mesocosm experiment

MicrobiologyOpen

Volumn 3, Issue 1, 2014, Pages 139-156

  Eronen Rasimus, Eeva ^a   Kaartokallio, Hermanni ^a   Lyra, Christina ^b   Autio, Riitta ^a   Kuosa, Harri ^a   Dieckmann, Gerhard S ^c   Thomas, David N ^a,d  

^a FINNISH ENVIRONMENT INSTITUTE   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^d BANGOR UNIVERSITY   (United Kingdom)

Author keywords

16S rDNA; Bacteria; DOM; Flow cytometry; Mesocosm; Sea ice; T RFLP

Indexed keywords

16S RDNA; BACTERIA; DOM; FLOW CYTOMETRY; MESOCOSM; SEA ICE; T-RFLP;

BACTERIA; BACTERIAL LOAD; DNA, BACTERIAL; ECOSYSTEM; FREEZING; GAMMAPROTEOBACTERIA; ICE COVER; MICROBIOTA; NORTH SEA; ORGANIC CHEMICALS; PHYLOGENY; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RIBOTYPING; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; SALINITY; SEAWATER; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 84893789726     PISSN: None     EISSN: 20458827     Source Type: Journal    
DOI: 10.1002/mbo3.157     Document Type: Article

References (87)

1. Abdo, Z., U. M. E. Schuette, S. J. Bent, C. J. Williams, L. J. Forney, and P. Joyce 2006. Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes. Environ. Microbiol. 8:929-938.
2. Allers, E., L. Gomez-Consarnau, J. Pinhassi, J. M. Gasol, K. Simek, and J. Pernthaler 2007. Response of Alteromonadaceae and Rhodobacteriaceae to glucose and phosphorus manipulation in marine mesocosms. Environ. Microbiol. 9:2417-2429.
3. Alonso-Saez, L., and J. M. Gasol 2007. Seasonal variations in the contributions of different bacterial groups to the uptake of low-molecular-weight compounds in Northwestern Mediterranean coastal waters. Appl. Environ. Microbiol. 73:3528-3535.
4. Alonso-Saez, L., O. Sanchez, and J. M. Gasol 2012. Bacterial uptake of low molecular weight organics in the subtropical Atlantic: are major phylogenetic groups functionally different? Limnol. Oceanogr. 57:798-808.
5. Alvarez-Aviles, L., W. R. Simpson, T. A. Douglas, M. Sturm, D. Perovich, and F. Domine 2008. Frost flower chemical composition during growth and its implications for aerosol production and bromine activation. J. Geophys. Res. Atmos. 113:D21304.
6. Amon, R. M. W., H. P. Fitznar, and R. Benner 2001. Linkages among the bioreactivity, chemical composition, and diagenetic state of marine dissolved organic matter. Limnol. Oceanogr. 46:287-297.
7. Anderson, M. J., and J. Robinson 2003. Generalized discriminant analysis based on distances. Aust. N. Z. J. Stat. 45:301-318.
8. Anderson, M. J., R. N. Gorley, and K. R. Clarke 2008. PERMANOVA+ for PRIMER: guide to software and statistical methods. Primer-E Ltd, Plymouth, U.K.
9. Arrigo, K. R., T. Mock, and M. P. Lizotte 2010. Primary producers in sea ice. Pp. 283-325 in D. N. Thomas and G. S. Dieckmann, eds. Sea ice. 2nd ed. Wiley-Blackwell Publishing, Oxford, U.K.
10. Aslam, S. N., G. J. C. Underwood, H.Kaartokallio, L. Norman, R. Autio, M. Fischer, et al. 2012. Dissolved extracellular polymeric substances (dEPS) dynamics and bacterial growth during sea ice formation in an ice tank study. Polar Biol. 35:661-676.
11. Becquevort, S., I. Dumont, J. L. Tison, D. Lannuzel, M. L. Sauvee, L. Chou, et al. 2009. Biogeochemistry and microbial community composition in sea ice and underlying seawater off East Antarctica during early spring. Polar Biol. 32:879-895.
12. Bowman, J. P., S. A. McCammon, M. V. Brown, D. S. Nichols, and T. A. McMeekin 1997. Diversity and association of psychrophilic bacteria in Antarctic sea ice. Appl. Environ. Microbiol. 63:3068-3078.
13. Bowman, J. S., and J. W. Deming 2010. Elevated bacterial abundance and exopolymers in saline frost flowers and implications for atmospheric chemistry and microbial dispersal. Geophys. Res Lett. 37:L13501.
14. Bowman, J. S., S. Rasmussen, N. Blom, J. W. Deming, S. Rysgaard, and T. Sicheritz-Ponten 2012. Microbial community structure of Arctic multiyear sea ice and surface seawater by 454 sequencing of the 16S RNA gene. ISME J. 6:11-20.
15. Bowman, J. S., C. Larose, T. M. Vogel, and J. W. Deming 2013. Selective occurrence of Rhizobiales in frost flowers on the surface of young sea ice near Barrow, Alaska and distribution in the polar marine rare biosphere. Environ. Microbiol. Rep. 5:575-582.
16. Brinkmeyer, R., K. Knittel, J. Jurgens, H. Weyland, R. Amann, and E. Helmke 2003. Diversity and structure of bacterial communities in Arctic versus Antarctic pack ice. Appl. Environ. Microbiol. 69:6610-6619.
17. Brown, M. V., and J. P. Bowman 2001. A molecular phylogenetic survey of sea-ice microbial communities (SIMCO). FEMS Microbiol. Ecol. 35:267-275.
18. Caron, D. A., and R. J. Gast 2010. Heterotrophic protists associated with sea ice. Pp. 327-356 in G. S. Dieckmann and D. N. Thomas, eds. Sea ice. 2nd ed. Wiley-Blackwell Publishing, Oxford, U.K.
19. Clarke, K. R., and R. N. Gorley 2006. Primer v6: user manual/tutorial. Primer-E Ltd, Plymouth, U.K.
20. Cole, J. R., Q. Wang, E. Cardenas, J. Fish, B. Chai, R. J. Farris, et al. 2009. The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37:D141-D145.
21. Collins, R. E., and J. W. Deming 2011. Abundant dissolved genetic material in Arctic sea ice. Part II: viral dynamics during autumn freeze-up. Polar Biol. 34:1831-1841.
22. Collins, R. E., G. Rocap, and J. W. Deming 2010. Persistence of bacterial and archaeal communities in sea ice through an Arctic winter. Environ. Microbiol. 12:1828-1841.
23. Cottrell, M. T., and D. L. Kirchman 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.
24. Deming, J. W. 2010. Sea ice bacteria and viruses. Pp. 247-282 in D. N. Thomas and G. S. Dieckmann, eds. Sea ice. 2nd ed. Wiley-Blackwell Publishing, Oxford, U.K.
25. Eilers, H., J. Pernthaler, and R. Amann 2000. Succession of pelagic marine bacteria during enrichment: a close look at cultivation-induced shifts. Appl. Environ. Microbiol. 66:4634-4640.
26. Elifantz, H., R. R. Malmström, M. T. Cottrell, and D. L. Kirchman 2005. Assimilation of polysaccharides and glucose by major bacterial groups in the Delaware estuary. Appl. Environ. Microbiol. 71:7799-7805.
27. Elifantz, H., A. Dittel, M. Cottrell, and D. Kirchman 2007. Dissolved organic matter assimilation by heterotrophic bacterial groups in the western Arctic ocean. Aquat. Microb. Ecol. 50:39-49.
28. Ewert, M., and J. Deming 2011. Selective retention in saline ice of extracellular polysaccharides produced by the cold-adapted marine bacterium Colwellia psychrerythraea strain 34H. Ann. Glaciol. 51:111-117.
29. Felsenstein, J. 2005. PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle, WA.
30. Fuchs, B. M., M. V. Zubkov, K. Sahm, P. H. Burkill, and R. Amann 2000. Changes in community composition during dilution cultures of marine bacterioplankton as assessed by flow cytometric and molecular biological techniques. Environ. Microbiol. 2:191-201.
31. Fuhrman, J. A., and F. Azam 1980. Bacterioplankton secondary production estimates for coastal waters of British Columbia, Antarctica, and California. Appl. Environ. Microbiol. 39:1085-1095.
32. Fuhrman, J. A., and F. Azam 1982. Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: evaluation and field results. Mar. Biol. 66:109-120.
33. Gasol, J. M., and P. A. Del Giorgio 2000. Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Sci. Mar. 64:197-224.
34. Gasol, J. M., U. L. Zweifel, F. Peters, J. A. Fuhrman, and A. Hagström 1999. Significance of size and nucleic acid content heterogeneity as measured by flow cytometry in natural planktonic bacteria. Appl. Environ. Microbiol. 65:4475-4483.
35. Giannelli, V., D. N. Thomas, C. Haas, G. Kattner, H. Kennedy, and G. S. Dieckmann 2001. Behaviour of dissolved organic matter and inorganic nutrients during experimental sea-ice formation. Ann. Glaciol. 33:317-321.
36. Gomez-Consarnau, L., M. V. Lindh, J. M. Gasol, and J. Pinhassi 2012. Structuring of bacterioplankton communities by specific dissolved organic carbon compounds. Environ. Microbiol. 14:2361-2378.
37. Gradinger, R., and J. Ikävalko 1998. Organism incorporation into newly forming Arctic sea ice in the Greenland sea. J. Plankton Res. 20:871-886.
38. Granskog, M. A., H. Kaartokallio, and H. Kuosa 2010. Sea ice in non-polar regions. Pp. 531-577 in D. N. Thomas and G. S. Dieckmann, eds. Sea ice. 2nd ed. Wiley-Blackwell Publishing, Oxford, U.K.
39. Grossmann, S. 1994. Bacterial activity in sea ice and open water of the Weddel sea, Antarctica: a microautoradiographic study. Microb. Ecol. 28:1-18.
40. Grossmann, S., and G. S. Dieckmann 1994. Bacterial standing stock, activity, and carbon production during formation and growth of sea ice in Weddel sea, Antarctica. Appl. Environ. Microbiol. 60:2746-2753.
41. Grossmann, S., and M. Gleitz 1993. Microbial responses to experimental sea ice formation: implications for the establishment of Antarctic sea-ice communities. J. Exp. Mar. Biol. Ecol. 173:273-289.
42. Helmke, E., and H. Weyland 1995. Bacteria in sea ice and underlying water of the eastern Weddel sea in midwinter. Mar. Ecol. Prog. Ser. 117:269-287.
43. Junge, K., F. Imhoff, T. Staley, and J. W. Deming 2002. Phylogenetic diversity of numerically important Arctic sea-ice bacteria cultured at subzero temperature. Microb. Ecol. 43:315-328.
44. Kaartokallio, H. 2004. Food web components, and physical and chemical properties of Baltic Sea ice. Mar. Ecol. Prog. Ser. 273: 49-63
45. Kaartokallio, H., J. Tuomainen, H. Kuosa, J. Kuparinen, P. J. Martikainen, and K. Servomaa 2008. Succession of sea-ice bacterial communities in the Baltic sea fast ice. Polar Biol. 31:783-793.
46. Kaartokallio, H., D. H. Søgaard, L. Norman, S. Rysgaard, J. L. Tison, B. Delille, et al. 2013. Short-term variability in bacterial abundance, cell properties, leucine and thymidine incorporation in subarctic sea ice. Aquat. Microb. Ecol. 71:57-73.
47. Kirchman, D. 2012. Degradation of organic material. Pp. 79-98 in D. Kirchman, ed. Processes in microbial ecology. Oxford University Press Inc., New York, NY.
48. Kirchman, D., E. Knees, and R. Hodson 1985. Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems. Appl. Environ. Microbiol. 49:599-607.
49. Krembs, C., H. Eicken, and J. W. Deming 2011. Exopolymer alteration of physical properties of sea ice and implications for ice habitability and biogeochemistry in a warmer Arctic. Proc. Natl Acad. Sci. USA 108:3653-3658.
50. Kuosa, H., and H. Kaartokallio 2006. Experimental evidence on nutrient and substrate limitation of Baltic sea sea-ice algae and bacteria. Hydrobiologia 554:1-10.
51. Lane, D. J., B. Pace, G. J. Olsen, D. A. Stahl, M. L. Sogin, and N. R. Pace 1985. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc. Natl Acad. Sci. USA 82:6955-6959.
52. Letunic, I., and P. Bork 2007. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23:127-128.
53. Liu, W. T., T. L. Marsh, H. Cheng, and L. J. Forney 1997. Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl. Environ. Microbiol. 63:4516-4522.
54. Malmström, R. R., M. T. Cottrell, H. Elifantz, and D. L. Kirchman 2005. Biomass production and assimilation of dissolved organic matter by SAR11 bacteria in the northwest atlantic ocean. Appl. Environ. Microbiol. 71:2979-2986.
55. Morris, R. M., M. S. Rappe, S. A. Connon, K. L. Vergin, W. A. Siebold, C. A. Carlson, et al. 2002. SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420:806-810.
56. Mou, X. Z., S. L. Sun, R. A. Edwards, R. E. Hodson, and M. A. Moran 2008. Bacterial carbon processing by generalist species in the coastal ocean. Nature 451:U708-U704.
57. Müller, S., A. Vähätalo, C. Stedmon, M. Granskog, G. S. Dieckmann, and D. N. Thomas 2013. Optical properties of dissolved organic matter during an ice tank study. Mar. Chem. 155:148-157.
58. Pedros-Alio, C. 2006. Marine microbial diversity: can it be determined? Trends Microbiol. 14:257-263.
59. Pedros-Alio, C. 2012. The rare bacterial biosphere. Annu. Rev. Mar. Sci. 4:449-466.
60. Perovich, D. K., and J. A. Richter-Menge 1994. Surface characteristics of lead ice. J. Geophys. Res. Oceans 99:16341-16350.
61. Petrich, C., and H. Eicken 2010. Growth, structure and properties of sea ice. Pp. 23-77 in D. N. Thomas and G. S. Dieckmann, eds. Sea ice. 2nd ed. Wiley-Blackwell Publishing, Oxford, U.K.
62. Pinhassi, J., and T. Berman 2003. Differential growth response of colony-forming alpha- and gamma-proteobacteria in dilution culture and nutrient addition experiments from lake Kinneret (Israel), the eastern Mediterranean sea, and the Gulf of Eilat. Appl. Environ. Microbiol. 69:199-211.
63. Pomeroy, L. R., and W. J. Wiebe 2001. Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria. Aquat. Microb. Ecol. 23:187-204.
64. R Development Core Team 2011. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0.
65. Riedel, A., C. Michel, and M. Gosselin 2007a. Grazing of large-sized bacteria by sea-ice heterotrophic protists on the Mackenzie shelf during the winter-spring transition. Aquat. Microb. Ecol. 74:3-4.
66. Riedel, A., C. Michel, M. Gosselin, and B. Leblanc 2007b. Enrichment of nutrients, exopolymeric substances and microorganisms in newly formed sea ice on the Mackenzie shelf. Mar. Ecol. Prog. Ser. 342:55-67.
67. Roberts, R. J., T. Vincze, J. Posfai, and D. Macelis 2010. REBASE-a database for DNA restriction and modification: enzymes, genes and genomes. Nucleic Acids Res. 38:D234-D236.
68. Sait, L., M. Galic, R. A. Strugnell, and P. H. Janssen 2003. Secretory antibodies do not affect the composition of the bacterial microbiota in the terminal ileum of 10-week-old mice. Appl. Environ. Microbiol. 69:2100-2109.
69. Schloss, P. D., B. R. Larget, and J. Handelsman 2004. Integration of microbial ecology and statistics: a test to compare gene libraries. Appl. Environ. Microbiol. 70:5485-5492.
70. Schloss, P. D., S. L. Westcott, T. Ryabin, J. R. Hall, M. Hartmann, E. B. Hollister, et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541.
71. Sinkko, H., K. Lukkari, A. S. Jama, L. M. Sihvonen, K. Sivonen, M. Leivuori, et al. 2011. Phosphorus chemistry and bacterial community composition interact in brackish sediments receiving agricultural discharges. PLoS ONE 6:e21555.
72. Sogin, M. L., H. G. Morrison, J. A. Huber, D. Mark Welch, S. M. Huse, P. R. Neal, et al. 2006. Microbial diversity in the deep sea and the underexplored "rare biosphere". Proc. Natl Acad. Sci. USA 103:12115-12120.
73. Staden, R., K. F. Beal, and J. K. Bonfield 1998. Computer methods in molecular biology. Pp. 115-130 in S. Misener and S. A. Krawetz, eds. Bioinformatics methods and protocols. Humana Press Inc., Totowa, NJ.
74. Staden, R., D. P. Judge, and J. K. Bonfield 2003. Managing sequencing projects in the GAP4 environment. Pp. 327-344 in S. A. Krawetz and D. D. Womble, eds. Introduction to bioinformatics: a theoretical and practical approach. Humana Press Inc, Totowa, NJ.
75. Staley, J. T., and J. J. Gosink 1999. Poles apart: biodiversity and biogeography of sea ice bacteria. Annu. Rev. Microbiol. 53:189-215.
76. Stedmon, C. A., D. N. Thomas, M. Granskog, H. Kaartokallio, S. Papadimitriou, and H. Kuosa 2007. Characteristics of dissolved organic matter in baltic coastal sea ice: Allochthonous or autochthonous origins? Environ. Sci. Technol. 41:7273-7279.
77. Teeling, H., B. M. Fuchs, D. Becher, C. Klockow, A. Gardebrecht, C. M. Bennke, et al. 2012. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336:608-611.
78. Teira, E., J. M. Gasol, M. Aranguren-Gassis, A. Fernandez, J. Gonzalez, I. Lekunberri, et al. 2008. Linkages between bacterioplankton community composition, heterotrophic carbon cycling and environmental conditions in a highly dynamic coastal ecosystem. Environ. Microbiol. 10:906-917.
79. Teira, E., S. Martinez-Garcia, A. Calvo-Diaz, and X. A. G. Moran 2010. Effects of inorganic and organic nutrient inputs on bacterioplankton community composition along a latitudinal transect in the atlantic ocean. Aquat. Microb. Ecol. 60:299-313.
80. Teira, E., S. Martinez-Garcia, C. Carreira, and X. A. G. Moran 2011. Changes in bacterioplankton and phytoplankton community composition in response to nutrient additions in coastal waters off the NW Iberian peninsula. Mar. Ecol. Prog. Ser. 426:87-104.
81. Thomas, D. N., and G. S. Dieckmann 2002. Antarctic Sea ice - a habitat for extremophiles. Science 295:641-644.
82. Thomas, D. N., G. Kattner, R. Engbrodt, V. Giannelli, H. Kennedy, C. Haas, et al. 2001. Dissolved organic matter in Antarctic sea ice. Ann. Glaciol. 33:297-303.
83. Thomas, D.N., S. Papadimitriou, and C. Michel 2010. Biogeochemistry in sea ice. Pp. 425-467 in D. N. Thomas and G. S. Dieckmann, eds. Sea ice. 2nd ed. Wiley-Blackwell Publishing, Oxford, U.K.
84. Underwood, G. J. C., S. Fietz, S. Papadimitriou, D. N. Thomas, and G. S. Dieckmann 2010. Distribution and composition of dissolved extracellular polymeric substances (EPS) in Antarctic sea ice. Mar. Ecol. Prog. Ser. 404:1-19.
85. Underwood, G. J. C., S. N. Aslam, C. Michel, A. Niemi, L. Norman, K. M. Meiners, et al. 2013. Broad-scale predictability of carbohydrates and exopolymers in Antarctic and Arctic sea ice. Proc. Natl Acad. Sci. USA 110: 15734-15739.
86. Wang, Q., G. M. Garrity, J. M. Tiedje, and J. R. Cole 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73:5261-5267.
87. Weissenberger, J., and S. Grossmann 1998. Experimental formation of sea ice: importance of water circulation and wave action for incorporation of phytoplankton and bacteria. Polar Biol. 20:178-188.