Identification of a Thiomicrospira denitrificans-like epsilonproteobacterium as a catalyst for autotrophic denitrification in the central Baltic Sea

Applied and Environmental Microbiology

Volumn 72, Issue 2, 2006, Pages 1364-1372

  Brettar, Ingrid ^a   Labrenz, Matthias ^a,d   Flavier, Sébastien ^b   Bötel, Julia ^a   Kuosa, Harri ^c   Christen, Richard ^b   Höfle, Manfred G ^a  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

^c UNIVERSITY OF HELSINKI   (Finland)

^d LEIBNIZ INSTITUTE FOR BALTIC SEA RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; DENITRIFICATION; GENES; RNA; SULFUR COMPOUNDS; SURFACE WATER RESOURCES;

AUTOTROPHIC DENITRIFICATIONS; BACTERIAL COMMUNITIES; BIOGEOCHEMICAL PROCESSES;

BACTERIOLOGY;

BACTERIAL RNA; CARBON; DNA; NITRATE; NITROGEN; OXYGEN; RNA 16S; SULFIDE; SULFUR;

BACTERIUM; DENITRIFICATION; IDENTIFICATION METHOD; MICROBIAL ECOLOGY;

ARTICLE; AUTOTROPHY; BACTERIAL COUNT; BACTERIAL FLORA; BACTERIAL METABOLISM; BACTERIUM IDENTIFICATION; BALTIC SEA; BIOGEOCHEMICAL CYCLING; CARBON DIOXIDE FIXATION; CATALYST; CONTINUOUS CULTURE; CONTROLLED STUDY; DENITRIFICATION; ECOSYSTEM; EPSILONPROTEOBACTERIA; ESTUARY; GENE SEQUENCE; MARINE ENVIRONMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; PHYLOGENY; REAL TIME POLYMERASE CHAIN REACTION; SINGLE STRAND CONFORMATION POLYMORPHISM; TAXON; THIOBACILLUS DENITRIFICANS; THIOMICROSPIRA; THIOMICROSPIRA DENITRIFICANS;

BALTIC STATES; DNA, BACTERIAL; ECOSYSTEM; EPSILONPROTEOBACTERIA; GENES, BACTERIAL; MARINE BIOLOGY; MOLECULAR SEQUENCE DATA; NITROGEN; PHYLOGENY; PISCIRICKETTSIACEAE; POLYMORPHISM, SINGLE-STRANDED CONFORMATIONAL; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; SEAWATER;

BACTERIA (MICROORGANISMS); EPSILONPROTEOBACTERIA; THIOBACILLUS DENITRIFICANS; THIOMICROSPIRA; THIOMICROSPIRA DENITRIFICANS;

EID: 33144487676     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.72.2.1364-1372.2006     Document Type: Article

References (43)

1. Brettar, I. 1991. Denitrification in the water column of the central Baltic: regulatory factors and microbiological aspects. Ph.D. thesis. University of Kiel, Kiel, Germany. Ber. Inst. Meereskd. Kiel 208:1-145. [Online.] http://www.baltic.vtt.fi/pdfs/ber208.pdf.
2. 2S-oxidation as motor of denitrification at the oxic-anoxic interface. Mar. Ecol. Prog. Ser. 77:157-169.
3. Brettar, I., and G. Rheinheimer. 1992. Influence of carbon availability on denitrification in the water column of the central Baltic. Limnol. Oceanogr. 37:1146-1163.
4. Campbell, B. J., C. Jeanthon, J. E. Kostka, G. W. Luther III, and C. Cary. 2001. Growth and phylogenetic properties of novel bacteria belonging to the epsilon subdivision of the Proteobacteria enriched from Alvinella pompejana and deep-sea hydrothermal vents. Appl. Environ. Microbiol. 67:4566-4572.
5. Dettmer, A. E., H. C. Giesenhagen, V. M. Trenkel, H. Au dem Venne, and F. J. Jochem. 1993. Phototrophic and heterotrophic pico- and nanoplankton in anoxic depths of the central Baltic Sea. Mar. Ecol. Progr. Ser. 99:197-203.
6. Elmgren, R. 1989. Man's impact on the ecosystem of the Baltic: energy flows today and at the turn of the century. Ambio 18:326-332.
7. Gascuel, O. 1997. BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol. Biol. Evol. 14:685-695.
8. Gocke, K. 1989. Bakterielle Stoffaufnahme im aeroben und anaeroben Milieu der Ostsee. Ber. Inst. Meereskd. Kiel 188:40-47.
9. Grasshoff, K., M. Ehrhardt, and K. Kremling. 1983. Methods of sea water analysis, Verlag Chemie, Weinheim, Germany.
10. Höfle, M. G., and I. Brettar. 1995. Taxonomic diversity and metabolic activity of microbial communities in the water column of the central Baltic Sea. Limnol. Oceanogr. 40:868-874.
11. Höfle, M. G., S. Flavier, R. Christen, J. Bötel, M. Labrenz, and I. Brettar. 2005. Retrieval of nearly complete 16S rRNA gene sequences from environmental DNA following 16S rRNA based community fingerprinting. Environ. Microbiol. 7:670-675.
12. Huettel, M., S. Forster, S. Klöser, and H. Fossing. 1996. Vertical migration in the sediment-dwelling sulfur bacteria Thioploca spp. in overcoming diffusion limitations. Appl. Environ. Microbiol. 62:1863-1872.
13. 2 fixation via the reductive tricarboxylic acid cycle by members of the epsilon subdivision of proteobacteria. J. Bacteriol. 187:3020-3027.
14. Hurst, C. J. 2002. Neighborhoods and community involvement: no microbe is an island, p. 6-18. In C. J. Hurst, R. L. Crawford, G. R. Knudsen, M. J. McInerney, and L. D. Stelzenbach (ed.), Manual of environmental microbiology, 2nd ed. ASM Press, Washington, D.C.
15. Inagaki, F., K. Takai, H. Kobayashi, K. H. Nealson, and K. Horikoshi. 2003. Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing epsilon-Proteobacteria isolated from hydrothermal sediments in the Mid-Okinawa Trough. Int. J. Syst. Evol. Microbiol. 53:1801-1805.
16. 2 fixation and bacterial-mat growth in intermittently anoxic Saanich Inlet, British Columbia. Mar. Ecol. Progr. Ser. 33:41-50.
17. Kerkhof, L., and P. Kemp. 1999. Small ribosome RNA content in marine Proteobacteria during non-steady state growth. FEMS Microbiol. Ecol. 30: 253-260.
18. Labrenz, M., S. Flavier, R. Christen, J. Bötel, I. Brettar, and M. G. Höfle. 2004. Development and application of a real-time PCR approach for quantification of uncultured bacteria in the central Baltic Sea. Appl. Environ. Microbiol. 70:4971-4979.
19. Lane, D. J. 1991. 16S/23S rRNA sequencing, p. 115-175. In E. Stackebrandt and M. Goodfellow (ed.), Nucleic acid techniques in bacterial systematics. John Wiley and Sons, Chichester, United Kingdom.
20. Liu, W. T., and D. A. Stahl. 2002. Molecular approaches for the measurement of density, diversity and phytogeny, p. 114-134. In C. J. Hurst, R. L. Crawford, G. R. Knudsen, M. J. McInerney, and L. D. Stetzenbach (ed.), Manual of environmental microbiology, 2nd ed. ASM Press, Washington, D.C.
21. Madrid, V. M., G. T. Taylor, M. I. Scranton, and A. Y. Chistoserdov. 2001. Phylogenetic diversity of bacterial and archaeal communities in the anoxic zone of the Cariaco Basin. Appl. Environ. Microbiol. 67:1663-1674.
22. Muyzer, G., A. Teske, C. O. Wirsen, and H. W. Jannasch. 1995. Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gel electrophoressis of 16S rDNA fragments. Arch. Microbiol. 164:165-172.
23. Nakagawa, S., K. Takai F. Inagaki, K. Horikoshi, and Y. Sako. 2005. Nitratiruptor tergarcus gen. nov., sp. nov. and Nitratifractor salsuginis gen. nov., sp. nov., nitrate-reducing chemolithoautotrophs of the epsilon-Proteobacteria isolated from a deep-sea hydrothermal system in the Mid-Okinawa Trough. Int. J. Syst. Evolution. Microbiol. 55:925-933.
24. Nehring, D. 1987. Temporal variations of phosphate and inorganic nitrogen compounds in the central Baltic Sea. Limnol. Oceaonogr. 32:494-499.
25. Newman, D. K., and J. F. Banfield. 2002. 2002. Geomicrobiology: how molecular-scale interactions underpin biogeochemical systems. Science 296: 1071-1077.
26. Pöhler, I., D. F. Wenderoth, K. Wendt-Potthoff, and M. G. Höfle. 2002. Bacterioplankton community structure and dynamics in enclosures during bio-remediation experiments in an acid mining lake. Water Air Soil Pollut. Focus 2:111-121.
27. Rahm, L. 1987. Oxygen consumption in the Baltic proper. Limnol. Oceanogr. 32:973-978.
28. Rappé, M. S., and S. J. Giovannoni. 2003. The uncultured microbial majority. Annu. Rev. Microbiol. 57:369-394.
29. Reysenbach, A.-L., K. Longnecker, and J. Kirshstein. 2000. Novel bacterial and archaeal lineages from an in situ growth chamber deployed at a Mid-Atlantic Ridge hydrothermal vent. Appl. Environ. Microbiol. 66:3798-3806.
30. Rheinheimer, G., K. Gocke, and H. G. Hoppe. 1989. Vertical distribution of microbiological and hydrographic-chemical parameters in different areas of the Baltic Sea. Mar. Ecol. Prog. Ser. 52:55-70.
31. Savchuk, O., and F. Wulff. 2001. A model of the biogeochemical cycles of nitrogen and phosphorus in the Baltic, p. 373-415. In F. V. Wulff, L. A. Rahm, and P. Larson. (ed.), A system analysis of the Baltic Sea. Springer, Berlin, Germany.
32. Schwieger, F., and C. Tebbe. 1998. A new approach to utilize PCR-single-strand conformation polymorphism for 16S rRNA gene-based microbial community analysis. Appl. Environ. Microbiol. 64:4870-4876.
33. 14C) for measuring organic production in the sea. J. Cons. Int. Explor. Mer 18:117-140.
34. Takai, K., F. Inagaki, S. Nakagawa, H. Hirayama, T. Nunoura, Y. Sako, K. H. Nealson, and K. Horikoshi. 2003. Isolation and phylogenetic diversity of members of previously uncultivated epsilon-Proteobacteria in deep-sea hydrothermal fields. FEMS Microbiol. Lett. 218:167-174.
35. Taylor, G. T., M. Iabichella, T. Y. Ho, and M. I. Scranton. 2001. Chemoautotrophy in the redox transition zone of the Cariaco Basin: a significant midwater source of organic carbon production. Limnol. Oceanogr. 46:148-163.
36. Thunell, R. C., D. M. Sigraan, F. Muller-Karger, Y. Astor, and R. Varela. 2004. Nitrogen isotope dynamics of the Cariaco Basin, Venezuela. Global Biogeochem. Cycles 18:GB3001. [Online.] doi:10.1029/2003GB002185.
37. Timmer-ten-Hoor, A. 1981. Cell yield and bioenergetics of Thiomicrospira denitrificans compared with Thiobacillus denitrificans. Antonie Leeuwenhoek 47:231-243.
38. Tyson, G. W., J. Chapman, P. Hugenholtz, E. E. Allen, R. J. Ram, P. M. Richardson, V. V. Solovyev, E. M. Rubin, D. S. Rokhsar, and J. F. Banfield. 2004. Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature (London) 428:37-43.
39. Venter, J. C., K. Remington, J. F. Heidelberg, A. L. Halpern, D. Rusch, J. A. Eisen, D. Wu, I. Paulsen, K. E. Nelson, W. Nelson, D. E. Fouts, S. Levy, A. H. Knap, M. W. Lomas, K. Nealson, O. White, J. Peterson, J. Hoffman, R. Parsons, H. Baden-Tillson, C. Pfannkoch, Y.-H. Rogers, and H. O. Smith. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66-74.
40. Weinbauer, M. G., I. Fritz, D. F. Wenderoth, and M. G. Höfle. 2002. Simultaneous extraction of total RNA and DNA from bacterioplankton suitable for quantitative structure and function analyses. Appl. Environ. Microbiol. 68:1082-1087.
41. Weinbauer, M. G., I. Brettar, and M. G. Höfle. 2003. Viral infection and lysogeny of bacterioplankton in surface, deep and anoxic marine waters. Limnol. Oceanogr. 48:1457-1465.
42. Wulff, F. V., L. A. Rahm, and P. Larson. 2001. A system analysis of the Baltic Sea. Springer, Berlin, Germany.
43. Wulff, F. V., A. Stigebrandt, and L. A. Rahm. 1990. Nutrient dynamics of the Baltic Sea. Ambio 19:126-133.