Spatial and temporal variation in denitrification and in the denitrifier community in a boreal lake

Aquatic Microbial Ecology

Volumn 64, Issue 1, 2011, Pages 27-40

  Rissanen, Antti Juhani ^a,b   Tiirola, Marja ^a   Ojala, Anne ^b  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Bacterial diversity; Boreal; Denitrification; Lake; NirK; Sediment

Indexed keywords

BACTERIA (MICROORGANISMS);

EID: 79959434845     PISSN: 09483055     EISSN: None     Source Type: Journal    
DOI: 10.3354/ame01506     Document Type: Article

References (85)

1. Ahlgren I, Sörensson F, Waara T, Vrede K (1994) Nitrogen budgets in relation to microbial transformations in lakes. Ambio 23:367-377. (Pubitemid 2156288)
2. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389-3402. (Pubitemid 27359211)
3. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32-46. (Pubitemid 33719668)
4. Boyle SA, Rich JJ, Bottomley PJ, Cromack K, Myrold DD (2006) Reciprocal transfer effects on denitrifying community composition and activity at forest and meadow sites in the Cascade Mountains of Oregon. Soil Biol Biochem 38: 870-878.
5. Braker G, Ayala-del-Rio HL, Devol AH, Fesefeldt A, Tiedje JM (2001) Community structure of denitrifiers, Bacteria, and Archaea along redox gradients in Pacific northwest marine sediments by terminal restriction fragment length polymorphism analysis of amplified nitrite reductase (nirS) and 16S rRNA genes. Appl Environ Microbiol 67: 1893-1901. (Pubitemid 33644964)
6. Bryant LD, Lorrai C, McGinnis DF, Brand A, Wüest A, Little JC (2010) Variable sediment oxygen uptake in response to dynamic forcing. Limnol Oceanogr 55:950-964.
7. Cao Y, Green PG, Holden PA (2008) Microbial community composition and denitrifying enzyme activities in salt marsh sediments. Appl Environ Microbiol 74:7585-7595.
8. Christensen PB, Sørensen J (1986) Temporal variation of denitrification activity in plant-covered, littoral sediment from Lake Hampen, Denmark. Appl Environ Microbiol 51: 1174-1179. (Pubitemid 16068613)
9. Cowan JLW, Pennock JR, Boynton WR (1996) Seasonal and interannual patterns of sediment-water nutrient and oxygen fluxes in Mobile Bay, Alabama (USA): regulating factors and ecological significance. Mar Ecol Prog Ser 141: 229-245.
10. Dale OR, Tobias CR, Song B (2009) Biogeographical distribution of diverse anaerobic ammonium oxidizing (anammox) bacteria in Cape Fear river estuary. Environ Microbiol 11: 1194-1207.
11. Dalsgaard T, Thamdrup B, Canfield DE (2005) Anaerobic ammonium oxidation (anammox) in the marine environment. Res Microbiol 156:457-464. (Pubitemid 40615411)
12. Dandie CE, Burton DL, Zebarth BJ, Henderson SL, Trevors JT, Goyer C (2008) Changes in bacterial denitrifier community abundance over time in an agricultural field and their relationship with denitrification activity. Appl Environ Microbiol 74:5997-6005, .
13. De Medina HL, Marín JC, Gutiérrez E, Morales J (2003) Nitrogen mobility at the sediment-water interface of Lake Maracaibo, Venezuela. Water Air Soil Pollut 145:341-357. (Pubitemid 36656369)
14. Desnues C, Michotey VD, Wieland A, Zhizang C, Fourçans A, Duran R, Bonin PC (2007) Seasonal and diel distributions of denitrifying and bacterial communities in a hypersaline microbial mat (Camargue, France). Water Res 41: - 3407-3419. (Pubitemid 47033937)
15. Enwall K, Hallin S (2009) Comparison of T-RFLP and DGGE techniques to assess denitrifier community composition in soil. Lett Appl Microbiol 48:145-148.
16. Enwall K, Philippot L, Hallin S (2005) Activity and composition of the denitrifying bacterial community respond differently to long-term fertilization. Appl Environ Microbiol 71:8335-8343. (Pubitemid 41803961)
17. Fortunato CS, Carlini DB, Ewers E, Bushaw-Newton KL (2009) Nitrifier and denitrifier molecular operational taxonomic unit compositions from sites of a freshwater estuary of Chesapeake Bay. Can J Microbiol 55:333-346.
18. Griffiths RI, Whiteley AS, O'Donnell AG, Bailey MJ (2000) Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl Environ Microbiol 66:5488-5491. (Pubitemid 32217162)
19. Groffman PM, Altabet MA, Böhlke JK, Butterbach-Bahl K and others (2006) Methods for measuring denitrification: diverse approaches to a difficult problem. Ecol Appl 16: 2091-2122. (Pubitemid 44917573)
20. Hallin S, Lindgren PE (1999) PCR detection of genes encoding nitrite reductase in denitrifying bacteria. Appl Environ Microbiol 65:1652-1657. (Pubitemid 29173697)
21. Hallin S, Throbäck IN, Dicksved J, Pell M (2006) Metabolic profiles and genetic diversity of denitrifying communities in activated sludge after addition of methanol or ethanol. Appl Environ Microbiol 72:5445-5452.
22. Hamersley MR, Woebken D, Boehrer B, Schultze M, Lavik G, Kuypers MMM (2009) Water column anammox and denitrification in a temperate permanently stratified lake (Lake Rassnitzer, Germany). Syst Appl Microbiol 32:571-582.
23. Harrison JA, Maranger RJ, Alexander RB, Giblin AE and others (2009) The regional and global significance of nitrogen removal in lakes and reservoirs. Biogeochemistry 93: 143-157.
24. Hasegawa T, Okino T (2004) Seasonal variation of denitrification rate in Lake Suwa sediment. Limnology 5:33-39. (Pubitemid 38617097)
25. Hietanen S (2007) Anaerobic ammonium oxidation (anammox) in sediments of the Gulf of Finland. Aquat Microb Ecol 48:197-205. (Pubitemid 351525812)
26. Hietanen S, Kuparinen J (2008) Seasonal and short-term variation in denitrification and anammox at a coastal station on the Gulf of Finland, Baltic Sea. Hydrobiologia 596: 67-77.
27. Hobbs WO, Lalonde SV, Vinebrooke RD, Konhauser KO, Weidman RP, Graham MD, Wolfe AP (2010) Algal-silica cycling and pigment diagenesis in recent alpine lake sediments: mechanisms and paleoecological implications. J Paleolimnol 44:613-628.
28. Hochberg Y (1988) A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75:800-802.
29. Jäntti H (2007) The spatial and temporal variation of nitrogen fixation in aquatic environments. MSc Thesis, University of Jyväskylä, Jyväskylä.
30. Junier P, Kim O, Witzel K, Imhoff JF, Hadas O (2008) Habitat partitioning of denitrifying bacterial communities carrying nirS or nirK genes in the stratified water column of Lake Kinneret, Israel. Aquat Microb Ecol 51:129-140. (Pubitemid 351959712)
31. Kim OS, Imhoff JF, Witzell KP, Junier P (2011) Distribution of denitrifying bacterial communities in the stratified water column and sediment-water interface in two freshwater lakes and the Baltic Sea. Aquat Ecol 45:99-112.
32. Koop-Jakobsen K, Giblin AE (2009) Anammox in tidal marsh sediments: the role of salinity, nitrogen loading, and marsh vegetation. Estuaries Coasts 32:238-245.
33. Liu WT, Marsh TL, Cheng H, Forney LJ (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63:4516-4522. (Pubitemid 27485783)
34. Liu XD, Tiquia SM, Holguin G, Wu LY and others (2003) Molecular diversity of denitrifying genes in continental margin sediments within the oxygen-deficient zone off the Pacific coast of Mexico. Appl Environ Microbiol 69: 3549-3560. (Pubitemid 36693366)
35. Maerki M, Müller B, Dinkel C, Wehrli B (2009) Mineralization pathways in lake sediments with different oxygen and organic carbon supply. Limnol Oceanogr 54:428-438.
36. Magalhães C, Bano N, Wiebe WJ, Bordalo AA, Hollibaugh JT (2008) Dynamics of nitrous oxide reductase genes (nosZ) in intertidal rocky biofilms and sediments of the Douro river estuary (Portugal), and their relation to N-biogeochemistry. Microb Ecol 55:259-269. (Pubitemid 351171467)
37. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290-297. (Pubitemid 32106404)
38. McCarthy MJ, Gardner WS, Lavrentyev PJ, Moats KM, Jochem FJ, Klarer DM (2007) Effects of hydrological flow regime on sediment-water interface and water column nitrogen dynamics in a Great Lakes coastal wetland (Old Woman Creek, Lake Erie). J Gt Lakes Res 33:219-231. (Pubitemid 46624398)
39. Mengis M, Gachter R, Wehrli B, Bernasconi S (1997) Nitrogen elimination in two deep eutrophic lakes. Limnol Oceanogr 42:1530-1543. (Pubitemid 28181004)
40. Müller B, Maerki M, Schmid M, Vologina EG, Wehrli B, Wüest A, Sturm M (2005) Internal carbon and nutrient cycling in Lake Baikal: sedimentation, upwelling, and early diagenesis. Global Planet Change 46:101-124. (Pubitemid 40599950)
41. Murphy J, Riley JP (1962) A modified single solution method for determination of phosphate in natural waters. Anal Chim Acta 27:31-36.
42. Muyzer G, Dewaal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reactionamplified genes coding for 16S ribosomal-RNA. Appl Environ Microbiol 59:695-700. (Pubitemid 23072343)
43. Nielsen LP (1992) Denitrification in sediment determined from nitrogen isotope pairing. FEMS Microbiol Lett 86: 357-362.
44. Nizzoli D, Carraro E, Nigro V, Viaroli P (2010) Effect of organic enrichment and thermal regime on denitrification and dissimilatory nitrate reduction to ammonium (DNRA) in hypolimnetic sediments of two lowland lakes.Water Res 44:2715-2724.
45. Nogales B, Timmis KN, Nedwell DB, Osborn AM(2002) Detection and diversity of expressed denitrification genes in estuarine sediments after reverse transcription-PCR amplification from mRNA. Appl Environ Microbiol 68: 5017-5025. (Pubitemid 35154813)
46. Nõges P, Järvet A, Tuvikene L, Nõges T (1998) The budgets of nitrogen and phosphorus in shallow eutrophic Lake Võrtsjärv (Estonia). Hydrobiologia 363:219-227.
47. O'Connor BL, Hondzo M, Dopraca D, LaPara TM, Finlay JC, Brezonik PL (2006) Quantity-activity relationship of denitrifying bacteria and environmental scaling in streams of a forested watershed. J Geophys Res 111:G04014.
48. Ojala A, Bellido JL, Tulonen T, Kankaala P, Huotari J (2011) Carbon gas fluxes from a brown water and a clear-water lake in the boreal zone during a summer with extreme rain events. Limnol Oceanogr 56:61-76.
49. Perryman SE, Rees GN, Walsh CJ (2008) Analysis of denitrifying communities in streams from an urban and non-urban catchment. Aquat Ecol 42:95-101. (Pubitemid 351640760)
50. Piña-Ochoa E, Álvarez-Cobelas M (2006) Denitrification in aquatic environments: a cross-system analysis. Biogeochemistry 81:111-130. (Pubitemid 44484889)
51. Prosser JI (2010) Replicate or lie. Environ Microbiol 12: 1806-1810.
52. Quinn G, Keough M (2002) Experimental design and data analysis for biologists. Cambridge University Press.
53. Revsbech NP, Jacobsen JP, Nielsen LP (2005) Nitrogen transformations in microenvironments of river beds and riparian zones. Ecol Eng 24:447-455. (Pubitemid 40793635)
54. Rich JJ, Myrold DD (2004) Community composition and activities of denitrifying bacteria from adjacent agricultural soil, riparian soil, and creek sediment in Oregon, USA. Soil Biol Biochem 36:1431-1441. (Pubitemid 38965027)
55. Rich JJ, Heichen RS, Bottomley PJ, Cromack K, Myrold DD (2003) Community composition and functioning of denitrifying bacteria from adjacent meadow and forest soils. Appl Environ Microbiol 69:5974-5982. (Pubitemid 37280320)
56. Risgaard-Petersen N, Rysgaard S, Nielsen LP, Revspech NP (1994) Diurnal variation of denitrification and nitrification in sediments colonized by benthic microphytes. Limnol Oceanogr 39:573-579. (Pubitemid 2086022)
57. Risgaard-Petersen N, Skarup S, Nielsen LP (1999) Denitrification in a soft bottom lake: evaluation of laboratory incubations. Aquat Microb Ecol 17:279-287. (Pubitemid 29341946)
58. Rissanen AJ, Kurhela E, Aho T, Oittinen T, Tiirola M (2010) Storage of environmental samples for guaranteeing nucleic acid yields for molecular microbiological studies. Appl Microbiol Biotechnol 88:977-984.
59. 2-fixing, and total-community bacteria by terminal restriction fragment length polymorphism analysis using multiple restriction enzymes. Appl Environ Microbiol 71: 2026-2035. (Pubitemid 40546127)
60. Rysgaard S, Risgaard-Petersen N, Sloth NP, Jensen K, Nielsen LP (1994) Oxygen regulation of nitrification and denitrification in sediments. Limnol Oceanogr 39:1643-1652.
61. Rysgaard S, Christensen PB, Nielsen LP (1995) Seasonal variation in nitrification and denitrification in estuarine sediment colonized by benthic microalgae and bioturbating infauna. Mar Ecol Prog Ser 126:111-121. (Pubitemid 26440191)
62. Saunders DL, Kalff J (2001a) Nitrogen retention in wetlands, lakes and rivers. Hydrobiologia 443:205-212. (Pubitemid 32442340)
63. Saunders DL, Kalff J (2001b) Denitrification rates in the sediments of Lake Memphremagog, Canada-USA. Water Res 35:1897-1904. (Pubitemid 32280264)
64. Scala DJ, Kerkhof LJ (2000) Horizontal heterogeneity of denitrifying bacterial communities in marine sediments by terminal restriction fragment length polymorphism analysis. Appl Environ Microbiol 66:1980-1986. (Pubitemid 30253721)
65. Schernewski G (2003) Nutrient budgets, dynamics and storm effects in a eutrophic, stratified baltic lake. Acta Hydro - chim Hydrobiol 31:152-161. (Pubitemid 37431554)
66. Schubert CJ, Durisch-Kaiser E, Wehrli B, Thamdrup B, Lam P, Kuypers MMM (2006) Anaerobic ammonium oxidation in a tropical freshwater system (Lake Tanganyika). Environ Microbiol 8:1857-1863. (Pubitemid 44326477)
67. Seitzinger SP (1988) Denitrification in freshwater and coastal marine ecosystems: ecological and geochemical significance. Limnol Oceanogr 33:702-724.
68. Seitzinger SP, Kroeze C, Bouwman AF, Caraco N, Dentener F, Styles RV (2002) Global patterns of dissolved inorganic and particulate nitrogen inputs to coastal systems: recent conditions and future projections. Estuaries 25:640-655. (Pubitemid 35211654)
69. Silvennoinen H, Hietanen S, Liikanen A, Stange CF, Russow R, Kuparinen J, Martikainen PJ (2007) Denitrification in the river estuaries of the northern Baltic Sea. Ambio 36: 134-140. (Pubitemid 46942182)
70. Silvennoinen H, Liikanen A, Torssonen J, Stange CF, Martikainen PJ (2008) Denitrification and nitrous oxide effluxes in boreal, eutrophic river sediments under increasing nitrate load: a laboratory microcosm study. Biogeochemistry 91:105-116.
71. Simola H, Arvola L (2005) Lakes of Northern Europe. In: O'Sullivan PE, Reynolds CS (eds) The lakes handbook, Vol 2: lake restoration and rehabilitation. Blackwell Science, Oxford.
72. Smith CJ, Nedwell DB, Dong LF, Osborn AM (2007) Diversity and abundance of nitrate reductase genes (narG and napA), nitrite reductase genes (nirS and nrfA), and their transcripts in estuarine sediments. Appl Environ Microbiol 73:3612-3622. (Pubitemid 46871451)
73. Sollie S, Verhoeven JTA (2008) Nutrient cycling and retention along a littoral gradient in a Dutch shallow lake in relation to water level regime. Water Air Soil Pollut 193:107-121.
74. 15N isotope pairing technique. Appl Environ Microbiol 67: 3771-3778. (Pubitemid 33641659)
75. 2O, nitrification and denitrification in a eutrophic lake sediment bioturbated by Chironomus plumosus. Aquat Microb Ecol 14:289-299. (Pubitemid 128487639)
76. Svensson JM, Enrich-Prast A, Leonardson L (2001) Nitrification and denitrification in a eutrophic lake sediment bioturbated by oligochaetes. Aquat Microb Ecol 23:177-186. (Pubitemid 34253480)
77. Throbäck IN, Enwall K, Jarvis A, Hallin S (2004) Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiol Ecol 49:401-417. (Pubitemid 39119598)
78. Tiquia SM, Masson SA, Devol A (2006) Vertical distribution of nitrite reductase genes (nirS) in continental margin sediments of the Gulf of Mexico. FEMS Microbiol Ecol 58: 464-475. (Pubitemid 44748155)
79. Tuominen L, Heinänen A, Kuparinen J, Nielsen LP (1998) Spatial and temporal variability of denitrification in the sediments of the northern Baltic Proper.Mar Ecol Prog Ser 172:13-24. (Pubitemid 28504218)
80. Wallenstein MD, Myrold DD, Firestone M, Voytek M (2006) Environmental controls on denitrifying communities and denitrification rates: Insights from molecular methods. Ecol Appl 16:2143-2152. (Pubitemid 44917575)
81. Wertz S, Dandie CE, Goyer C, Trevors JT, Patten CL (2009) Diversity of nirK denitrifying genes and transcripts in an agricultural soil. Appl Environ Microbiol 75:7365-7377.
82. Wolsing M, Priemé A (2004) Observation of high seasonal variation in community structure of denitrifying bacteria in arable soil receiving artificial fertilizer and cattle manure by determining T-RFLP of nir gene fragments. FEMS Microbiol Ecol 48:261-271. (Pubitemid 38553969)
83. Wood ED, Armstrong FA, Richards FA (1967) Determination of nitrate in sea water by cadmium-copper reduction to nitrite. J Mar Biol Assoc UK 47:23-31.
84. Wu L, Kellogg L, Devol AH, Tiedje JM, Zhou J (2008) Microarray-based characterization of microbial community functional structure and heterogeneity in marine sediments from the gulf of Mexico. Appl Environ Microbiol 74:4516-4529. (Pubitemid 352031034)
85. Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61:533-616. (Pubitemid 28006959)