Nitrate reduction functional genes and nitrate reduction potentials persist in deeper estuarine sediments why?

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Papaspyrou, Sokratis ^a,b   Smith, Cindy J ^a,c   Dong, Liang F ^a   Whitby, Corinne ^a   Dumbrell, Alex J ^a   Nedwell, David B ^a  

^a UNIVERSITY OF ESSEX   (United Kingdom)

^b Laboratorio de Microbiología y Genética Departamento de Biomedicina Biotecnología y Salud Pública Campus Río San Pedro S n   (Spain)

^c NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

NITRATE; NITRATE REDUCTASE; NITRITE; RNA 16S; NITRITE REDUCTASE;

ARTICLE; BEGGIATOA; BIOTURBATION; CONTROLLED STUDY; DENITRIFICATION; ESTUARY; GENE; NAPA GENE; NARG GENE; NIRS GENE; NITRATE REDUCER; NITRATE REDUCTION; NITRATE REDUCTION TO AMMONIUM; NONHUMAN; NRFA GENE; PYROSEQUENCING; REDUCTION; SEDIMENT; THIOPLOCA; UNITED KINGDOM; GENETICS; MICROBIOLOGY; PHYSIOLOGY;

DENITRIFICATION; ESTUARIES; GEOLOGIC SEDIMENTS; NITRITE REDUCTASES; RNA, RIBOSOMAL, 16S;

EID: 84899657917     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094111     Document Type: Article

References (77)

1. Herbert A (1999) Nitrogen cycling in coastal marine ecosystems. FEMS Microbiol Rev 23: 563-590.
2. Nedwell DB, Jickells TD, Trimmer M, Sanders R (1999) Nutrients in estuaries. Adv Ecol Res 29: 43-92.
3. Seitzinger SP (1988) Denitrification in fresh-water and coastal marine ecosystems-Ecological and geochemical significance. Limnol Oceanogr 33: 702-724.
4. Dalsgaard T, Canfield DE, Petersen J, Thamdrup B, Acuna-Gonzalez J (2003) N-2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature 422: 606-608.
5. Trimmer M, Nicholls JC, Morley N, Davies CA, Aldridge J (2005) Biphasic behavior of Anammox regulated by nitrite and nitrate in an estuarine sediment. Appl Environ Microbiol 71: 1923-1930.
6. Bell LC, Richardson DJ, Ferguson SJ (1990) Periplasmic and membrane-bound respiratory nitrate reductases in Thiosphaera pantotropha-the periplasmic enzyme catalyzes the 1st step in aerobic denitrification. FEBS Lett 265: 85-87.
7. Potter LC, Millington P, Griffiths L, Thomas GH, Cole JA (1999) Competition between Escherichia coli strains expressing either a periplasmic or a membranebound nitrate reductase: does Nap confer a selective advantage during nitratelimited growth? Biochem J 344: 77-84.
8. Sears HJ, Ferguson SJ, Richardson DJ, Spiro S (1993) The identification of a periplasmic nitrate reductase in Paracoccus denitrificans. FEMS Microbiol Lett 113: 107-111.
9. Megonigal JP, Hines ME, Visscher PT (2003) Anaerobic metabolism: Linkages to trace gases and aerobic processes. Biogeochemistry. Elsevier Pergamon. pp. 317-424.
10. Burgin AJ, Hamilton SK (2007) Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Front Ecol Environ 5: 89-96.
11. Robinson AD, Nedwell DB, Harrison RM, Ogilvie BG (1998) Hypernutrified estuaries as sources of N2O emission to the atmosphere: the estuary of the River Colne, Essex, UK. Mar Ecol Prog Ser 164: 59-71.
12. Dong LF, Nedwell DB, Underwood GJC, Thornton DCO, Rusmana I (2002) Nitrous oxide formation in the Colne estuary, England: the central role of nitrite. Appl Environ Microbiol 68: 1240-1249.
13. Dong LF, Thornton DCO, Nedwell DB, Underwood GJC (2000) Denitrification in sediments of the River Colne estuary, England. Mar Ecol Prog Ser 203: 109-112.
14. 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.
15. 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.
16. Grasshoff K (1976) Methods of seawater analysis. New York: Verlag Chemie.
17. Jensen MM, Thamdrup B, Dalsgaard T (2007) Effects of specific inhibitors on anammox and denitrification in marine sediments. Appl Environ Microbiol 73: 3151-3158.
18. Sorensen J (1978) Denitrification rates in a marine sediment as measured by the acetylene inhibition technique. Appl Environ Microbiol 36: 139-143.
19. Groffman PM, Altabet MA, Bolke J, Butterbach-Bahl K, David MB, et al. (2006) Methods for measuring denitrification: diverse approaches to a difficult problem. Ecol Appl 16: 2091-2122.
20. Kucera I (2006) Interference of chlorate and chlorite with nitrate reduction in resting cells of Paracoccus denitrificans. Microbiology 152: 3529-3534.
21. Canfield DE, Kristensen E, Thamdrup B (2005) The Nitrogen Cycle. Academic Press.
22. Bower CE, Holm-Hansen T (1980) A salicylate-hypochlorite method for determining ammonia in seawater. Can J Fish Aquat Sci 37: 794-798.
23. Weiss RF, Price BA (1980) Nitrous-oxide solubility in water and seawater. Mar Chem 8: 347-359.
24. Thompson RC, Tobin ML, Hawkins SJ, Norton TA (1999) Problems in extraction and spectrophotometric determination of chlorophyll from epilithic microbial biofilms: towards a standard method. J Mar Biol Ass U K 79: 551-558.
25. Hedges JI, Stern JH (1984) Carbon and nitrogen determinations of carbonatecontaining solids. Limnol Oceanogr 29: 657-663.
26. Buchanan JB (1984) Sediment Analysis. In: N. A. . Holme and A. D. . McIntyre, editors. Methods for the study of marine benthos. Oxford: Blackwell Scientific Publications. pp. 41-65.
27. Miller DN (2001) Evaluation of gel filtration resins for the removal of PCRinhibitory substances from soils and sediments. J Microbiol Methods 44: 49-58.
28. Suzuki MT, Taylor LT, DeLong EF (2000) Quantitative analysis of smallsubunit rRNA genes in mixed microbial populations via 5 9-nuclease assays. Appl Environ Microbiol 66: 4605-4614.
29. Smith CH, Nedwell DB, Dong LF, Osborn AM (2006) Evaluation of quantitative polymerase chain reaction-based approaches for determining gene copy and gene transcript numbers in environmental samples. Environ Microbiol 8: 804-815.
30. Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, et al. (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiology 8: 125.
31. Ishak HD, Plowes R, Sen R, Kellner E, Meyer E, et al. (2011) Bacterial diversity in Solenopsis invicta and Solenopsis geminata ant colonies characterized by 16S amplicon 454 pyrosequencing. Microb Ecol 61: 821-831.
32. Giongo A, Crabb DB, Davis-Richardson AG, Chauliac D, Mobberley JM, et al. (2010) PANGEA: pipeline for analysis of next generation amplicons. ISME J 4.
33. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
34. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
35. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Na?̈ve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267.
36. Dickie IA (2010) Insidious effects of sequencing errors on perceived diversity in molecular surveys. New Phytol 188: 916-918.
37. Anderson MJ (2001) A new method for non-parametric multivariate analyses of variance in ecology. Austral Ecol 26: 32-46.
38. Clarke KR, Green RH (1988) Statistical design and analysis for a 'biological effects' study. Mar Ecol Prog Ser 46: 213-226.
39. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82: 290-297.
40. Clarke KR, Gorley RN (2001) PRIMER v6: User Manual/Tutorial. Plymouth: PRIMER-E. 190 p.
41. Laverman AM, Van Cappellen P, Rotterdam-Los D, Pallud C, Abell J (2006) Potential rates and pathways of microbial nitrate reduction in coastal sediments. FEMS Microbiol Ecol 58: 179-192.
42. Dong LF, Nedwell DB, Stott A (2006) Sources of nitrogen used for denitrification and nitrous oxide formation in sediments of the hypernutrified Colne, the nutrified Humber, and the oligotrophic Conwy estuaries, United Kingdom. Limnol Oceanogr 51: 545-557.
43. Dong LF, Smith CJ, Papaspyrou S, Stott A, Osborn AM, et al. (2009) Changes in benthic denitrification, nitrate ammonification, and anammox process rates and nitrate and nitrite reductase gene abundances along an estuarine nutrient gradient (the Colne Estuary, United Kingdom). Appl Environ Microbiol 75: 3171-3179.
44. Herbert RA, Nedwell DB (1990) Role of environmental factors in regulating nitrate respiration in intertidal sediments. In: N. P. . Revsbech and J. . Sorensen, editors. Denitrification in soils and sediments. New York, NY: Plenum Press. pp. 77-90.
45. Strohm TO, Griffin B, Zumft WG, Schink B (2007) Growth yields in bacterial denitrification and nitrate ammonification. Appl Environ Microbiol 73: 1420-1424.
46. Mosier AC, Francis CA (2010) Denitrifier abundance and activity across the San Francisco Bay estuary. Environ Microbiol Rep 2: 667-676.
47. Krekeler D, Cypionka H (1995) The preferred electron-acceptor of Desulfovibrio desulfuricans CSN. FEMS Microbiol Ecol 17: 271-277.
48. Marietou A, Griffiths L, Cole J (2009) Preferential reduction of the thermodynamically less favorable electron acceptor, sulfate, by a nitratereducing strain of the sulphate-reducing bacterium Desulfovibrio desulfuricans 27774. J Bacteriol 191: 882-889.
49. Dalsgaard T, Bak F (1992) Effect of acetylene on nitrous-oxide reduction and sulfide oxidation in batch and gradient cultures of Thiobacillus denitrificans. Appl Environ Microbiol 58: 1601-1608.
50. Yu KW, Seo DC, DeLaune RD (2010) Incomplete acetylene inhibition of nitrous oxide reduction in potential denitrification assay as revealed by using 15N-nitrate tracer. Communications in Soil Science and Plant Analysis 41: 2201-2210.
51. Rich JJ, Dale OR, Song B, Ward BB (2008) Anaerobic ammonium oxidation (anammox) in Chesapeake Bay sediments. Microb Ecol 55.
52. Richardson DJ (2001) Introduction: nitrate reduction and the nitrogen cycle. Cell Mol Life Sci 58: 163-164.
53. Jones CM, Hallin S (2010) Ecological and evolutionary factors underlying global and local assembly of denitrifier communities. ISME J 4: 633-641.
54. Braker G, Ayala-Del-R?́o 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.
55. 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.
56. Bulow SE, Francis CA, Jackson GA, Ward BB (2008) Sediment denitrifier community composition and nirS gene expression investigated with functional gene microarrays. Environ Microbiol 10: 3057-3069.
57. Petersen DG, Blazewicz SJ, Firestone M, Herman DJ, Turetsky M, et al. (2012) Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska. Environ Microbiol 14: 993-1008.
58. Sorensen J (1978) Capacity for denitrification and reduction of nitrate to ammonia in a coastal matine sediment. Appl Environ Microbiol 35: 301-305.
59. Joye SB, Smith SV, Hollibaugh JT, Paerl HW (1996) Estimating denitrification rates in estuarine sediments: A comparison of stoichiometric and acetylene based methods. Biogeochemistry 33: 197-215.
60. Koskiniemi S, Sun S, Berg OG, Andersson DI (2012) Selection-driven gene loss in bacteria. PLoS Genet 8: e1002787.
61. Mira A, Ochman H, Moran NA (2001) Deletional bias and the evolution of bacterial genomes. Trends Genet 17: 589-596.
62. Hanlon ARM, Bellinger B, Haynes K, Xiao G, Hofmann TA, et al. (2006) Dynamics of extracellular polymeric substance (EPS) production and loss in an estuarine, diatom-dominated, microalgal biofilm over a tidal emersionimmersion period. Limnol Oceanogr 51: 79-93.
63. Nielsen OI, Gribsholt B, Kristensen E, Revsbech NP (2004) Microscale distribution of oxygen and nitrate in sediment inhabited by Nereis diversicolor: spatial patterns and estimated reaction rates. Aquat Microb Ecol 34: 23-32.
64. Nizzoli D, Bartoli M, Cooper M, Welsh DT, Underwood GJC, et al. (2007) Implications for oxygen, nutrient fluxes and denitrification rates during the early stage of sediment colonisation by the polychaete Nereis spp. in four estuaries. Estuar Coast Shelf Sci 75: 125-134.
65. Takeuchi J (2006) Habitat segregation of a functional gene encoding nitrate ammonification in estuarine sediments. Geomicrobiol J 23: 75-87.
66. Nedwell DB, Embley TM, Purdy KJ (2004) Sulphate reduction, methanogenesis and phylogenetics of the sulphate reducing bacterial communities along an estuarine gradient. Aquat Microb Ecol 37: 209-217.
67. Clarke TA, Hemmings AM, Burlat B, Butt JN, Cole JA, et al. (2006) Comparison of the structural and kinetic properties of the cytochrome c nitrite reductases from Escherichia coli, Wolinella succinogenes, Sulfurospirillum deleyianum and Desulfovibrio desulfuricans. Biochem Soc Trans 34: 143-145.
68. Simon J, Kern M, Hermann B, Einsle O, Butt JN (2011) Physiological function and catalytic versatility of bacterial multihaem cytochromes c involved in nitrogen and sulfur cycling. Biochem Soc Trans 39: 1864-1870.
69. Nedwell DB, Walker TR (1995) Sediment-water fluxes of nutrients in an Antarctic coastal environment: influence of bioturbation. Polar Biol 15: 57-64.
70. Garcia-Robledo E, Corzo A, Papaspyrou S, Jimenez-Arias JL, Villahermosa D (2010) Freeze-lysable inorganic nutrients in intertidal sediments: dependence on microphytobenthos abundance. Mar Ecol Prog Ser 403: 155-163.
71. Dalsgaard T (2003) Benthic primary production and nutrient cycling in sediments with benthic microalgae and transient accumulation of macroalgae. Limnol Oceanogr 48: 2138-2150.
72. Kamp A, de Beer D, Nitsch JL, Lavik G, Stief P (2011) Diatoms respire nitrate to survive dark and anoxic conditions. Proc Natl Acad Sci U S A 108 5649-5654.
73. Risgaard-Petersen N, Langezaal AM, Ingvardsen S, Schmid MC, Jetten MSM, et al. (2006) Evidence for complete denitrification in a benthic foraminifer. Nature 443: 93-96.
74. Pina-Ochoa E, Hogslund S, Geslin E, Cedhagen T, Revsbech NP, et al. (2010) Widespread occurrence of nitrate storage and denitrification among Foraminifera and Gromiida. Proc Natl Acad Sci U S A 107: 1148-1153.
75. Zopfi J, Kjær T, Nielsen LP, Jorgensen BB (2001) Ecology of Thioploca spp.: Nitrate and sulfur storage in relation to chemical microgradients and influence of Thioploca spp. on the sedimentary nitrogen cycle. Appl Environ Microbiol 67: 5530-5537.
76. Matson PA, McDowell WH, Townsend AR, Vitousek PM (1999) The globalization of N deposition: ecosystem consequences in tropical environments. Biogeochemistry 46: 67-83.
77. Lomstein E, Jensen MH, Sorensen J (1990) Intracellular NH4 + and NO3 2 pools associated with deposited phytoplankton in a marine sediment (Aarhus Bright, Denmark). Mar Ecol Prog Ser 61: 97-105.