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Tillage Management and Seasonal Effects on Denitrifier Community Abundance, Gene Expression and Structure over Winter

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Abstract

Tillage effects on denitrifier communities and nitrous oxide (N2O) emissions were mainly studied during the growing season. There is limited information for the non-growing season, especially in northern countries where winter has prolonged periods with sub-zero temperatures. The abundance and structure of the denitrifier community, denitrification gene expression and N2O emissions in fields under long-term tillage regimes [no-tillage (NT) vs conventional tillage (CT)] were assessed during two consecutive winters. NT exerted a positive effect on nirK and nosZ denitrifier abundance in both winters compared to CT. Moreover, the two contrasting managements had an opposite influence on nirK and nirS RNA/DNA ratios. Tillage management resulted in different denitrifier community structures during both winters. Seasonal changes were observed in the abundance and the structure of denitrifiers. Interestingly, the RNA/DNA ratios were greater in the coldest months for nirK, nirS and nosZ. N2O emissions were not influenced by management but changed over time with two orders of magnitude increase in the coldest month of both winters. In winter of 2009–2010, emissions were mainly as N2O, whereas in 2010–2011, when soil temperatures were milder due to persistent snow cover, most emissions were as dinitrogen. Results indicated that tillage management during the growing season induced differences in denitrifier community structure that persisted during winter. However, management did not affect the active cold-adapted community structure.

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References

  1. Almaraz JJ, Mabood F, Zhou X, Madramootoo C, Rochette P, Ma B, Smith DL (2009) Carbon dioxide and nitrous oxide fluxes in corn grown under two tillage systems in Southwestern Quebec. Soil Sci Soc Am J 73:113–119

    Article  CAS  Google Scholar 

  2. Angers DA, Eriksen-Hamel NS (2008) Full inversion tillage and organic distribution in soil profiles: a meta-analysis. Soil Sci Soc Am J 72:1370–1374

    Article  CAS  Google Scholar 

  3. Arenson LU, Sego DC (2006) The effect of salinity on the freezing of coarse-grained sands. Can Geotech J 43:325–337

    Article  CAS  Google Scholar 

  4. Avrahami S, Conrad R (2005) Cold-temperate climate: a factor for selection of ammonia oxidizers in upland soil? Can J Microbiol 51:709–714

    Article  CAS  PubMed  Google Scholar 

  5. Barta J, Melichovà T, Vanĕk D, Picek T, Šantrůčková H (2010) Effect of pH and dissolved organic matter on the abundance of nirK and nirS denitrifiers in spruce forest soil. Biogeochemistry 101:123–132

    Article  CAS  Google Scholar 

  6. Baudoin E, Philippot L, Chèneby D, Chapuis-Lardy L, Fromin N, Bru D, Rabary B, Brauman A (2009) Direct seeding mulch-based cropping increases both the activity and the abundance of denitrifier communities in a tropical soil. Soil Biol Biochem 41:1703–1709

    Article  CAS  Google Scholar 

  7. Cavigelli MA, Robertson GP (2000) The functional significance of denitrifier community composition in a terrestrial ecosystem. Ecology 81:1402–1414

    Article  Google Scholar 

  8. deBruijn AMG, Butterbach-Bahl K, Blagodatsky S, Grote R (2009) Model evaluation of different mechanisms driving freeze-thaw N2O emissions. Agric Ecosyst Environ 133:196–207

    Article  CAS  Google Scholar 

  9. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Dandie CE, Wertz S, Leclair CL, Goyer C, Burton DL, Patten CL, Zebarth BJ, Trevors JT (2011) Abundance, diversity and functional gene expression of denitrifier communities in adjacent riparian and agricultural zones. FEMS Microbiol Ecol 77:69–82

    Article  CAS  PubMed  Google Scholar 

  11. Doran JW, Elliott ET, Paustian K (1998) Soil microbial activity, nitrogen cycling, and long-term changes in organic carbon pools as related to fallow tillage management. Soil Tillage Res 49:3–18

    Article  Google Scholar 

  12. Dörsch P, Bakken LR (2004) Low-temperature response of denitrification: comparison of soil. Eurasian Soil Sci 39(suppl 1):S102–S106

    Google Scholar 

  13. Drury CF, Reynolds WD, Tan CS, Welacky TW, Calder W, McLaughlin NB (2006) Emissions of nitrous oxide and carbon dioxide. Soil Sci Soc Am J 70:570–581

    Article  CAS  Google Scholar 

  14. Elder JW, Lal R (2008) Tillage effects on gaseous emissions from an intensively farmed organic soil in North Central Ohio. Soil Tillage Res 98:45–55

    Article  Google Scholar 

  15. Elmi A, Mehdi B, Chandra M, Dam R, Smith D (2009) Long-term effect of conventional and no-tillage production systems on nitrous oxide fluxes from corn (Zea mays L.) field in Southwestern Quebec. Am J Environ Sci 5:238–246

    Article  CAS  Google Scholar 

  16. Enwall K, Throbäck I, Stenberg M, Söderström M, Hallin S (2010) Soil resources influence spatial patterns of denitrifying community at scales compatible with land management. Appl Environ Microbiol 76:2243–2250

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Gao M, Zhou Z, Wei C, Xie D, Zhang L (2004) Effect of tillage system on soil animal, microorganism and enzyme activity in paddy field. Chin J Appl Ecol 15:1171–1181

    Google Scholar 

  18. Govaerts B, Mezzalama M, Unno Y, Sayre KD, Luna-Guido M, Vanherck K, Dendooven L, Deckers J (2007) Influence of tillage, residue management and crop rotation on soil microbial biomass and catabolic diversity. Appl Soil Ecol 37:18–30

    Article  Google Scholar 

  19. 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- ad rRNA-based microbial community composition. Appl Environ Microbiol 66:5488–5491

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  20. Grogan A, Michelsen A, Ambus P, Jonasson S (2004) Effect of differing freeze-thaw regimes on nutrient cycling and respiration in sub-arctic heath tundra. Soil Biol Biochem 36:641–664

    Article  CAS  Google Scholar 

  21. Hallin S, Jones CM, Schloter M, Philippot L (2009) Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J 3:597–605

    Article  CAS  PubMed  Google Scholar 

  22. Hamza MA, Anderson WK (2005) Soil compaction in cropping systems: a review of the nature, causes and possible solutions. Soil Tillage Res 82:121–145

    Article  Google Scholar 

  23. Henderson SL, Dandie CE, Patten CL, Zebarth BJ, Burton DL, Trevors JT, Goyer C (2010) Changes in denitrifier abundance, denitrification gene mRNA levels, nitrous oxide emissions, and denitrification in anoxic soil microcosms amended with glucose and plant residues. Appl Environ Microbiol 76:2155–2166

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. Kay B, Fukuda M, Izuta H, Sheppard MI (1981) The importance of water migration in the measurement of the thermal conductivity of unsaturated frozen soils. Cold Reg Sci Technol 5:95–106

    Article  Google Scholar 

  25. Koga N, Tsuruta H, Sawamoto T, Nishimura S, Yagi K (2004) N2O emission and CH4 uptake in arable fields managed under conventional and reduced tillage cropping system in northern Japan. Glob Biogeochem Cycles 18:1–11

    Article  Google Scholar 

  26. Ismaili I, Blevins RL, Frye WW (1994) Long-term no-tillage effects on soil properties and continuous corn yields. Soil Sci Soc Am J 58:193–198

    Article  Google Scholar 

  27. Laughlin RJ, Rütting T, Müller C, Watson CJ, Stevens RJ (2009) Effect of acetate on soil respiration, N2O emissions and gross N transformations related to fungi and bacteria in a grassland soil. Appl Soil Ecol 42:25e30

    Article  Google Scholar 

  28. Lemke RL, Izaurralde RC, Nyborg M, Solberg ED (1999) Tillage and N source influence soil-emitted nitrous oxide in Alberta Parkland region. Can J Soil Sci 79:15–24

    Article  CAS  Google Scholar 

  29. Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implication of dormancy. Nat Rev Microbiol 9:119–130

    Article  CAS  PubMed  Google Scholar 

  30. Linn DM, Doran JW (1984) Aerobic and anaerobic microbial populations in no-till and plowed soil. Soil Sci Soc Am J 48:794–799

    Article  Google Scholar 

  31. Logsdon SD, Karlen DL (2004) Bulk density as a soil quality indicator during conversion to no-tillage. Soil Tillage Res 78:143–149

    Article  Google Scholar 

  32. Maljanen M, Hytönen J, Martikanen PJ (2010) Cold-season nitrous oxide dynamics in a drained boreal peatland differ depending on land-use practice. Can J For Res 40:565–572

    Article  CAS  Google Scholar 

  33. Matzner E, Borken W (2008) Do freeze-thaw events enhance C and N losses from soils of different ecosystems? A review. Eur J Soil Sci 59:274–284

    Article  Google Scholar 

  34. Melero S, Perez-de-Mora A, Murillo JM, Buegger F, Kleinedam K, Kublik S, Vanderlinden K, Moreno F, Schloter M (2011) Denitrification in a vertisol under long-term tillage and no-tillage management in dryland agricultural systems: key genes and potential rates. Appl Soil Ecol 47:221–225

    Article  Google Scholar 

  35. Mkhabela MS, Madani A, Gordon R, Burton D, Cudmore D, Elmi A, Hart W (2008) Gaseous and leaching nitrogen losses from no-tillage and conventional tillage systems following surface application of cattle manure. Soil Tillage Res 98:187–199

    Article  Google Scholar 

  36. Németh DD, Wagner-Riddle C, Dunfield KE (2014) Abundance and gene expression in nitrifier and denitrifier communities associated with a field scale spring thaw N2O flux event. Soil Biol Biochem 73:1–9

    Article  Google Scholar 

  37. Oorts K, Merckx R, Grèhan E, Labreuche J, Nicolardot B (2007) Determinants of annual fluxes of CO2 and N2O in long-term no tillage and conventional tillage systems in northern France. Soil Tillage Res 95:133–148

    Article  Google Scholar 

  38. Parkin TB, Kaspar TC (2006) Nitrous oxide emissions from corn-soybean systems in the Midwest. J Environ Qual 35:1496–1506

    Article  CAS  PubMed  Google Scholar 

  39. Passionato CC, Ahrens T, Feigl BJ, Stendler PS, do-Carmo JA, Melillo JM (2003) Emissions of CO2, N2O and NO in conventional and no-till management practices in Rondonia. Brasil Biol Fertil Soils 38:200–208

    Article  Google Scholar 

  40. Pastorelli R, Vignozzi N, Landi S, Piccolo R, Orsini R, Seddaiu G, Ruggero PP, Pagliai M (2013) Consequences on macroporosity and bacterial diversity of adopting a no-tillage system in a clayish soil of Central Italy. Soil Biol Biochem 66:78–93

    Article  CAS  Google Scholar 

  41. Peixoto RS, Coutinho HLC, Madari B, Machado PLOA, Rumjanek NG, VanElsas JD, Seldin L, Rosado AS (2006) Soil aggregation and bacterial community structure as affected by tillage and cover cropping in the Brazilian Cerrados. Soil Tillage Res 90:16–28

    Article  Google Scholar 

  42. Pelster DE, Larouche F, Rochette P, Chantigny MH, Allaire S, Angers DA (2011) Nitrogen fertilization but not soil tillage affects nitrous oxide emissions from a clay loam soil under a maize-soybean rotation. Soil Tillage Res 115–116:16–26

    Article  Google Scholar 

  43. Pesaro M, Widmer F, Nicollier G, Zeyer J (2003) Effects of freeze-thaw stress during soil storage on microbial communities and methidathion degradation. Soil Biol Biochem 35:1049–1061

    Article  CAS  Google Scholar 

  44. Philippot L, CČuhel J, Saby NPA, Chèneby C, Bru D, Arrouays D, Martin-Laurent F, SŠimek M (2009) Mapping field-scale spatial patterns of size and activity of the denitrifier community”. Environ Microbiol 11:1518–1526

    Article  PubMed  Google Scholar 

  45. Philips RL (2007) Denitrification at sub-zero temperatures in arable soils: a review. Agron Sustain Dev 28:87–93

    Article  Google Scholar 

  46. Rich JJ, Heichen RS, Bottomley PJ, Cromackjr K, Myrold DD (2003) Community composition and functioning of denitrifying bacteria from adjacent meadow and forest soils. Appl Environ Microbiol 69:5974–5982

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. Rochette P (2008) No-till only increases N2O emissions in poorly-aerated soils. Soil Tillage Res 101:97–100

    Article  Google Scholar 

  48. Rochette P, Angers DA, Chantigny MH, Bertrand N (2008) N2O emissions respond differently to no-till in a loam and a heavy clay soil. Soil Sci Soc Am J 72:1363–1369

    Article  CAS  Google Scholar 

  49. Rösch C, Mergel A, Bothe H (2002) Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil. Appl Environ Microbiol 68:3818–3829

    Article  PubMed Central  PubMed  Google Scholar 

  50. Sehy U, Ruser R, Munch JC (2003) Nitrous oxide fluxes from maize fields: relationship to yield, site-specific fertilization, and soil conditions. Agric Ecosyst Environ 99:97–111

    Article  CAS  Google Scholar 

  51. Sharma S, Szele Z, Schilling R, Munch JC, Schloter M (2006) Influence of Freeze-Thaw stress on the structure and function of microbial communities and denitrifying populations in soils. Appl Environ Microbiol 72:2148–2154

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  52. Six J, Elliott ET, Paustian K (1999) Aggregate and soil organic matter dynamics under conventional and no-tillage systems. Soil Sci Soc Am J 10:21–36

    Google Scholar 

  53. Smith J, Wagner-Riddle C, Dunfield K (2010) Season and management related changes in the diversity of nitrifying and denitrifying bacteria over winter and spring. Appl Soil Ecol 44:138–146

    Article  Google Scholar 

  54. Tatti E, Goyer C, Chantigny M, Wertz S, Zebarth BJ, Burton DL, Filion M (2014) Influences of over winter conditions on denitrification and nitrous oxide-producing microorganism abundance and structure in an agricultural soil amended with different nitrogen sources. Agric Ecosyst Environ 183:47–59

    Article  CAS  Google Scholar 

  55. Vance ED, Brookers PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  56. Verhulst N, Govaerts B, Verachtert E, Castellanos-Navarrete A, Mezzalama M, Wall P, Deckers J, Sayre KD (2010) Conservation agriculture, improving soil quality for sustainable production systems? In: Lal R, Stewart BA (eds) Advances in soil science: food security and soil quality. CRC Press, Boca Raton, pp 137–208

    Google Scholar 

  57. Virkajävi P, Maljanen SK, Haapala J, Martikainen PJ (2010) N2O emissions from boreal grass and grass-clover pasture soils. Agric Ecosyst Environ 137:59–67

    Article  Google Scholar 

  58. Yanai Y, Toyota K, Okazaki M (2007) Response of denitrifying communities to successive freeze-thaw cycles. Biol Fertil Soils 44:113–119

    Article  Google Scholar 

  59. Wagner-Riddle C, Chu QC, van Bochove E, Jayasundara S (2008) Linking nitrous oxide flux during spring thaw to nitrate denitrification in the soil profile. Soil Sci Soc Am J 72:908–916

    Article  CAS  Google Scholar 

  60. Wagner-Riddle C, Rapai J, Warland J, Furon A (2010) Nitrous oxide fluxes related to soil freeze and thaw periods identified using heat pulse probes. Can J Soil Sci 90:409–418

    Article  Google Scholar 

  61. Wang Q, Bay Y, Gao H, He J, Chen H, Chesney RC, Kuhn NJ, Li H (2008) Soil chemical properties and microbial biomass after 16 years of no-tillage farming on the Loess Plateau, China. Geoderma 144:502–508

    Article  CAS  Google Scholar 

  62. Wei W, Isobe K, Shiratori Y, Nishizawa T, Ohte N, Otsuka S, Senoo K (2014) N2O emission from cropland field soil through fungal denitrification after surface applications of organic fertilizer. Soil Biol Biochem 69:157–167

    Article  CAS  Google Scholar 

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Acknowledgments

We would like to acknowledge the great technical work of Drucie Janes and the critical reading of the manuscript of Dr. Lindsay Brin. We also like to thank Dr. Cindy Smith and Dr. Fabiana Paula for useful comments to the manuscript. Funding for this study was provided by the Sustainable Agriculture Environmental Systems (SAGES) initiative of Agriculture and Agri-Food Canada.

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Authors and Affiliations

  1. Potato Research Centre, Agriculture and Agri-Food Canada, Fredericton, NB, E3B 4Z7, Canada

    Enrico Tatti, Claudia Goyer, Sophie Wertz & Bernie J. Zebarth

  2. Department of Environmental Sciences, Agricultural Campus, Dalhousie University, PO Box 550, Truro, B2N 5E3, Canada

    David L. Burton

  3. Soils and Crops Research and Development Centre, Agriculture and Agri-Food Canada, 2560 Hochelaga Blvd, Québec, QC, G1V 2J3, Canada

    Martin Chantigny

  4. Département de Biologie, Université de Moncton, Moncton, NB, E1A 3E9, Canada

    Martin Filion

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  1. Enrico Tatti
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Correspondence to Claudia Goyer.

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Fig. S1

Daily atmospheric maximum temperature (Atm. max. temp.) and soil temperatures (Soil temp.), snow depth (A and B) and volumetric water content (VWC) (C and D)in winters of 2009-2010 (A, C) and 2010-2011 (B, D). Soil temperature and snow depth are averaged across tillage management (n = 3). Soil temperature and soil volumetric water content (VWC) were measured at 5 cm and 15 cm soil depths, respectively. Soil VWC is a measure of liquid water content thus the rapid drop in water content in January and/or February likely reflects soil freezing. The sampling dates were indicated using closed circles and soil temperatures (in °C) on the specific sampling dates are indicated. NT: no tillage regime, CT: conventional tillage regime. (GIF 118 kb)

High resolution image (EPS 1653 kb)

Fig. S2

Concentrations of NO3 -(A, B) and NH4 +(C and D) in winter 2009-2010 (A, C) and 2010-2011 (B, D).Values are means (n = 5) and error bars represent one standard error. Significant differences based on Tukey’s test (p < 0.05) among sampling times are represented by lowercase letters under the X axis. No significant interaction between time and treatment was found. NT: no tillage regime, CT: conventional tillage regime. (GIF 58 kb)

High resolution image (EPS 1071 kb)

Fig. S3

Potential denitrification measured using denitrification enzyme assay (DEA) in winter 2009-2010 and 2010-2011. Values are means (n = 5) and error bar are standard errors. Significant differences based on Tukey’s test (p < 0.05)between sampling times are represented by letters under the x axis. (GIF 37 kb)

High resolution image (EPS 784 kb)

Fig. S4

Canonical correspondence analysis (CCA) of nirK (A), nirS (B) and nosZ (C) and active (RNA transcripts) nirK (D) denitrifier community structures (plotted as symbols) obtained by T-RFLP in relation to soil environmental variables and gas emissions rates (plotted as vectors) in winter 2010-2011. Treatments are indicated by open (NT, no-tillage regime) and closed symbols (CT, conventional tillage regime). (GIF 79 kb)

High resolution image (EPS 1032 kb)

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Tatti, E., Goyer, C., Burton, D.L. et al. Tillage Management and Seasonal Effects on Denitrifier Community Abundance, Gene Expression and Structure over Winter. Microb Ecol 70, 795–808 (2015). https://doi.org/10.1007/s00248-015-0591-x

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