Composition and activity of beta-Proteobacteria ammonia-oxidizing communities associated with intertidal rocky biofilms and sediments of the Douro River estuary, Portugal

Journal of Applied Microbiology

Volumn 103, Issue 4, 2007, Pages 1239-1250

  Magalhaes C ^a,b   Bano, N ^c   Wiebe, W J ^c   Hollibaugh, J T ^c   Bordalo, A A ^a,b  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

Ammonia oxidizing bacteria; N biogeochemistry; Nitrification; Rocky biofilms; Sediments

Indexed keywords

AMMONIA; BACTERIA; BIOFILMS; CLUSTER ANALYSIS; ELECTROPHORESIS; HIERARCHICAL SYSTEMS; NITRIFICATION; PHYLOGENETIC; SEDIMENTS;

AMMONIA OXIDIZING BACTERIA; ASSEMBLAGE COMPOSITION; DENATURING GRADIENT GEL ELECTROPHORESIS; ENVIRONMENTAL VARIABLES; INTERTIDAL SEDIMENTS; N-BIOGEOCHEMISTRY; PHYLOGENETICS; PORTUGAL; PROTEOBACTERIA; ROCKY BIOFILMS;

BIOGEOCHEMISTRY;

AMMONIA; CHLOROPHYLL A; NITRATE; ORGANIC MATTER;

ASSEMBLY RULE; BACTERIUM; BIOFILM; COMMUNITY COMPOSITION; ENVIRONMENTAL FACTOR; INTERTIDAL COMMUNITY; INTERTIDAL ENVIRONMENT; MICROBIAL ACTIVITY; NITRIFICATION; NITROGEN CYCLE; PHYLOGENETICS; SEDIMENT;

ARTICLE; BETAPROTEOBACTERIA; BIOFILM; BIOGEOCHEMISTRY; BIOPHYSICS; CLUSTER ANALYSIS; CONTROLLED STUDY; DENATURING GRADIENT GEL ELECTROPHORESIS; ENVIRONMENTAL FACTOR; ESTUARY; GENE SEQUENCE; INTERTIDAL ZONE; MICROBIAL ACTIVITY; MICROBIAL POPULATION DYNAMICS; NITRIFICATION; NITROSOMONAS; NONHUMAN; OXIDATION; PHYLOGENY; PORTUGAL; ROCK; SEDIMENT;

BETAPROTEOBACTERIA; NITROSOMONADALES; NITROSOMONAS SP.; NITROSOSPIRA; PROTEOBACTERIA;

EID: 34848833482     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2007.03390.x     Document Type: Article

References (43)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215, 403 410.
2. Bano, N. Hollibaugh, J.T. (2000) Diversity and distribution of DNA sequences with affinity to ammonia-oxidizing bacteria of the β subdivision of the class Proteobacteria in the Arctic Ocean. Appl Environ Microbiol 66, 1960 1969.
3. Bano, N. Hollibaugh, J.T. (2002) Phylogenetic composition of bacterioplankton assemblages from the Arctic Ocean. Appl Environ Microbiol 68, 505 518.
4. Bano, N., Ruffin, S., Ransom, B. Hollibaugh, J.T. (2004) Phylogenetic composition of Arctic Ocean Archaeal assemblages and comparison with Antarctic assemblages. Appl Environ Microbiol 70, 781 789.
5. Bartosch, S., Hartwig, C., Spieck, E. Bock, E. (2002) Immunological detection of Nitrospira-like bacteria in various soils. Microb Ecol 43, 26 33.
6. Bernhard, A.E., Donn, T., Giblin, A.E. Stahl, D.A. (2005) Loss of diversity of ammonium-oxidizing bacteria correlates with increasing salinity in an estuary system. Environ Microbiol 7, 1289 1297.
7. de Bie, M.J.M., Speksnijder, A.G.C.L., Kowalchuk, G.A., Schuurman, T., Zwart, G., Stephen, J.R., Diekmann, O.E. Laanbroek, H.J. (2001) Shifts in the dominant populations of ammonia oxidizing β-subclass Proteobacteria along the eutrophic Schelde estuary. Aquat Microb Ecol 23, 225 236.
8. Bollmann, A. Laanbroek, H.J. (2001) Continuous culture enrichments of ammonia-oxidizing bacteria at low ammonium concentrations. FEMS Microbiol Ecol 37, 211 221.
9. Brümmer, I.H.M., Fehr, W. Wagner-Döbler, I. (2000) Biofilm community structure in polluted rivers: abundance of dominant phylogenetic groups over a complete annual cycle. Appl Environ Microbiol 66, 3078 3082.
10. Bruns, M.A., Stephen, J.R., Kowalchuk, G.A., Prosser, J.I. Paul, E.A. (1999) Comparative diversity of ammonia oxidizer 16S rRNA gene sequences in native, tilled and successional soils. Appl Environ Microbiol 65, 2994 3000.
11. Caffrey, J.M., Harrington, N., Solem, I. Ward, B.B. (2003) Biogeochemical processes in a small California estuary. 2. Nitrification activity, community structure and role in nitrogen budgets. Mar Ecol Prog Ser 248, 27 40.
12. Cébron, A., Berth, T. Garnier, J. (2003) Nitrification and nitrifying bacteria in the lower Seine River and estuary (France). Appl Environ Microbiol 69, 7091 7100.
13. Cébron, A., Coci, M., Garnier, J. Laanbroek, H.J. (2004) Denaturing gradient gel electrophoretic analysis of ammonia-oxidizing bacterial community structure in the lower Seine River: impact of Paris wastewater effluents. Appl Environ Microbiol 70, 6726 6737.
14. Clarke, K.R. Warwick, R.M. (1994) Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. Plymouth, UK : Plymouth Marine Laboratory.
15. Ferrari, V.C. Hollibaugh, J.T. (1999) Distribution of microbial assemblages in the central Arctic Ocean basin studies by PCR/DGGE: Analysis of a large data set. Hydrobiologia 401, 55 68.
16. Francis, C.A., Roberts, K.J., Beman, J.M., Santoro, A.E. Oakley, B.B. (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 102, 14683 14688.
17. Freitag, T.E. Prosser, J.I. (2003) Community structure of ammonia-oxidizing bacteria within anoxic marine sediments. Appl Environ Microbiol 69, 1359 1371.
18. Gieseke, A., Purkhold, U., Wagner, M., Amann, R. Schramm, A. (2001) Community structure and activity dynamics of nitrifying bacteria in a phosphate-removing biofilm. Appl Environ Microbiol 67, 1351 1362.
19. Hollibaugh, J.T., Nasreen, B. Ducklow, H.W. (2002) Widespread distribution in Polar Oceans of a 16S rRNA gene sequence with affinity to Nitrosospira-like ammonia-oxidizing bacteria. Appl Environ Microbiol 68, 1478 1484.
20. Jensen, K.M., Jensen, M.H. Kristensen, E. (1996) Nitrification and denitrification in Wadden Sea sediments (Konigshafen, Island of Sylt, Germany) as measured by nitrogen isotope pairing and isotope dilution. Aquat Microb Ecol 11, 181 191.
21. Könneke, M., Bernhard, A.E., de la Torre, J.R., Walker, C.B., Waterbury, J.B. Stahl, D.A. (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543 546.
22. Koops, H.-P. Pommerening-Röser, A. (2001) Distribution and ecophysiology of the nitrifying bacteria emphasizing cultured species. FEMS Microb Ecol 37, 1 9.
23. Koops, H.-P., Purkhold, U., Pommerening-Röser, A., Timmermann, G. Wagner, M. (2003) The lithotrophic ammonia oxidizing bacteria. In The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community, 3rd edn. ed. Dworkin, M., et al. New York : Springer Verlag. Available at: http://link.springer-ny.com/link/service/books/10125/.
24. Kristensen, E., Jensen, M.H., Banta, G.T., Hansen, K., Holmer, M. King, G.H. (1999) Transformation and transport of inorganic nitrogen in sediments of a Southeast Asian mangrove forest. Aquat Microb Ecol 15, 165 175.
25. Lane, D.J. (1991) 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics. ed. Stackebrandt, E. Goodfellow, M. pp. 115 175. New York : John Wiley & Sons.
26. Limpiyakorn, T., Shinohara, Y., Kurisu, F. Yagi, O. (2005) Communities of ammonia-oxidizing bacteria in activated sludge of various sewage treatment plants in Tokyo. FEMS Microb Ecol 54, 205 217.
27. Magalhães, C., Bordalo, A.A. Wiebe, W.J. (2002) Temporal and spatial patterns of intertidal sediment-water nutrient and oxygen fluxes in the Douro River estuary, Portugal. Mar Ecol Prog Ser 233, 55 71.
28. Magalhães, C., Bordalo, A.A. Wiebe, W.J. (2003) Intertidal biofilms on rocky substratum can play a major role in estuarine carbon and nutrient dynamics. Mar Ecol Prog Ser 258, 275 281.
29. Magalhães, C.M., Joye, S.B., Moreira, R.M., Wiebe, W.J. Bordalo, A.A. (2005a) Effect of salinity and inorganic nitrogen concentrations on nitrification and denitrification rates in intertidal sediments and rocky biofilms of the Douro River estuary, Portugal. Water Res 39, 1783 1794.
30. Magalhães, C.M, Wiebe, W.J., Joye, S.B. Bordalo, A.A. (2005b) Inorganic nitrogen dynamics in intertidal rocky biofilms and sediments of the Douro river estuary (Portugal). Estuaries 28, 592 606.
31. McCaig, A.E., Phillips, C.J., Stephen, J.R., Kowalchuk, G.A., Harvey, S.M., Herbert, R.A., Embley, T.M Prosser, J.I. (1999) Nitrogen cycling and community structure of Proteobacterial β-subgroup ammonia-oxidizing bacteria within polluted marine fish farm sediments. Appl Environ Microbiol 65, 213 220.
32. Murray, A.E., Hollibaugh, J.T. Orrego, C. (1996) Phylogenetic compositions of bacterioplankton from two California estuaries compared by the denaturating gradient gel electrophoresis of 16S rDNA fragments. Appl Environ Microbiol 62, 2676 2680.
33. Myers, R.M., Fischer, S.G., Lerman, L.S. Maniatis, T. (1985) Nearly all single base substitutions in DNA fragments joined to a GC-clamp can be detected by denaturating gradient gel electrophoresis. Nucleic Acids Res 13, 3131 3145.
34. O'Mullan, G.D. Ward, B.B. (2005) Relationship of temporal and spatial variabilities of ammonia-oxidizing bacteria to nitrification rates in Monterey Bay, California. Appl Environ Microbiol 71, 697 705.
35. Paul, J.H. Myers, B. (1982) Fluorometric determination of DNA in aquatic microorganisms by use of Hoechst 33258. Appl Environ Microbiol 43, 1393 1399.
36. Phillips, C.J., Smith, Z., Embley, T.M. Prosser, J.I. (1999) Phylogenetic differences between particle-associated and planktonic ammonia-oxidizing bacteria of the β subdivision of the class Proteobacteria in the northwestern Mediterranean Sea. Appl Environ Microbiol 65, 779 786.
37. Purkhold, U., Wagner, M., Timmermann, G., Pommerening-Röser, A. Koops, H.P. (2003) 16S rRNA and amoA-based phylogeny of 12 novel betaproteobacterial ammonia-oxidizing isolates: extension of the dataset and proposal of the new lineage within the Nitrosomonas. Int J Syst Evol Microbiol 53, 1485 1494.
38. Stephen, J.R., McCaig, A.E., Smith, Z., Prosser, J.I. Embley, T.M. (1996) Molecular diversity of soil and marine 16S rRNA gene sequences related to b-subgroup ammonia-oxidizing bacteria. Appl Environ Microbiol 62, 4147 4154.
39. Stephen, J.R., Kowalchuk, G.A., Bruns, M.A.V., McCaig, A.E., Phillips, C.J., Embley, T.M. Prosser, J.I. (1998) Analysis of β-subgroup Proteobacterial ammonia oxidizer populations in soil by denaturating gradient gel electrophoresis analysis and hierarchical phylogenetic probing. Appl Environ Microbiol 64, 2958 2965.
40. Vieira, M.E.C. Bordalo, A.A. (2000) The Douro estuary (Portugal): a mesotidal salt wedge. Oceanol Acta 23, 585 594.
41. Voytek, M.A. Ward, B.B. (1995) Detection of ammonium-oxidizing bacteria of the beta-subclass of the class Proteobacteria in aquatic samples with the PCR. Appl Environ Microbiol 61, 1444 1450.
42. Ward, B.B., Voytek, M.A. Witzel, K.P. (1997) Phylogenetic diversity of natural populations of ammonia oxidizers investigated by specific PCR amplification. Microb Ecol 33, 87 96.
43. Webster, G., Embley, T.M., Freitag, T.E., Smith, Z. Prosser, J.I. (2005) Links between ammonia oxidizer species composition, functional diversity and nitrification kinetics in grassland soils. Environ Microbiol 5, 676 684.