Abstract
The present research was performed to clarify the changes of denitrifying genes (nirK, nirS, and nosZ) abundances under different physico-chemical parameters through evaluating the relationships between the genes abundances and parameters during agricultural waste composting. The genes abundances were determined by real-time quantitative PCR (qPCR). The correlations between physico-chemical parameters and denitrifying genes abundances were analysed by regression analysis. qPCR results showed that the nosZ gene abundance was higher than that of nirK and nirS genes. The nirK gene abundance was higher than nirS gene indicating that nitrite reducers with Cu-containing enzyme encoded by nirK gene were more of importance than those with cytochrome cd1 nitrite reductase encoded by nirS gene in the nitrite reduction step. Regression analysis suggested that (1) nirK gene abundance was correlated with pile temperature following quadratic model; (2) nirS gene abundance was linearly correlated with pile temperature and concentration of NH4 +, while correlated with concentration of NO3 − and pH following inverse and quadratic model respectively; (3) nosZ gene abundance was quadratically correlated with pH and linearly correlated with water soluble carbon (WSC).
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Angnes G, Nicoloso RS, da Silva MLB, de Oliveira PAV, Higarashi MM, Mezzari MP, Miller PRM (2013) Correlating denitrifying catabolic genes with N2O and N2 emissions from swine slurry composting. Bioresour Technol 140:368–375
Avrahami S, Conrad R, Braker G (2002) Effect of soil ammonium concentration on N2O release and on the community structure of ammonia oxidizers and denitrifiers. Appl Environ Microbiol 68:5685–5692
Bárta J, Melichová T, Vaněk 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
Chen Z, Luo XQ, Hu RG, Wu MN, Wu JS, Wei WX (2010) Impact of long-term fertilization on the composition of denitrifier communities based on nitrite reductase analyses in a paddy soil. Microb Ecol 60:850–861
Chen YN, Zhou W, Li YP, Zhang JC, Zeng GM, Huang AZ, Huang JX (2014) Nitrite reductase genes as functional markers to investigate diversity of denitrifying bacteria during agricultural waste composting. Appl Microbiol Biotechnol 98:4233–4243
Chon K, Chang JS, Lee E, Lee J, Ryu J, Cho J (2011) Abundance of denitrifying genes coding for nitrate (narG), nitrite (nirS), and nitrous oxide (nosZ) reductases in estuarine versus wastewater effluent-fed constructed wetlands. Ecol Eng 37:64–69
Crutzen PJ (1981) Atmospheric chemical processes of the oxides of nitrogen, including nitrous oxide. In: Delwiche CC (ed) Denitrification, nitrification, and atmospheric nitrous oxide. Wiley, New York, pp 17–44
Crutzen PJ, Ehhalt DH (1977) Effects of nitrogen fertilizers and combustion on the stratospheric ozone layer. Ambio 6:112–117
Dambreville C, Hallet S, Nguyen C, Morvan T, Germon JC, Philippot L (2006) Structure and activity of the denitrifying community in a maize-cropped field fertilized with composted pig manure of ammonium nitrate. FEMS Microbiol Ecol 56:119–131
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
Dandie CE, Wertz S, Leclair CL, Goyer C, Burton D, 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
Deiglmayr K, Philippot L, Hartwig UA, Kandeler E (2004) Structure and activity of the nitrate-reducing community in the rhizosphere of Lolium perenne and Trifolium repens under long-term elevated atmospheric pCO2. FEMS Microbiol Ecol 49:445–454
Forster P, Ramaswamy V, Artaxo P, Berntsen T, Betts R, Fahey DW, Haywood J, Lean J, Lowe DC, Myhre G, Nganga J, Prinn R, Raga G, Schulz M, Van Dorland R (2007) Changes in atmospheric constituents and in radiative forcing. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate Change 2007: The physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 129–234
Fukumoto Y, Osada T, Hanajima D, Haga K (2003) Patterns and quantities of NH3, N2O and CH4 emissions during swine manure composting without forced aeration-effect of compost pile scale. Bioresour Technol 89:109–114
Gödde M, Conrad R (1999) Immediate and adaptational temperature effects on nitric oxide production and nitrous oxide release from nitrification and denitrification in two soils. Biol Fert Soils 30:33–40
Guo GX, Deng H, Qiao M, Yao HY, Zhu YG (2013) Effect of long-term wastewater irrigation on potential denitrification and denitrifying communities in soils at the watershed scale. Environ Sci Technol 47:3105–3113
Hallin S, Lindgren PE (1999) PCR detection of genes encoding nitrite reductase in denitrifying bacteria. Appl Environ Microbiol 65:1652–1657
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 76:2155–2164
Henry S, Bru D, Stres B, Hallet S, Philippot L (2006) Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundance of 16S rRNA, narG, nirK, and nosZ genes in soils. Appl Environ Microbiol 72:5181–5189
Holtan-Hartwig L, Dörsch P, Bakken LR (2002) Low temperature control of soil denitrifying communities: Kinetics of N2O production and reduction. Soil Biol Biochem 34:1797–1806
IPCC (2007) Climate Change 2007: Synthesis Report. An assessment of the intergovernmental panel on climate control. Intergovernmental Panel on Climate Change (IPCC), Geneva
Kalemelawa F, Nishihara E, Endo T, Ahmad Z, Yeasmin R, Tenywa MM, Yamamoto S (2012) An evaluation of aerobic and anaerobic composting of banana peels treated with different inoculums for soil nutrient replenishment. Bioresour Technol 126:375–382
Kandeler E, Deiglmayr K, Tscherko D, Bru D, Philippot L (2006) Abundance of narG, nirS, nirK, and nosZ genes of denitrifying bacteria during primary successions of a glacier foreland. Appl Environ Microbiol 72:5957–5962
Kemp MJ, Dodds WK (2002) The influence of ammonium, nitrate, and dissolved oxygen concentrations on uptake, nitrification, and denitrification rates associated with prairie stream substrata. Limnol Oceanogr 47:1380–1393
Kulcu R, Yaldiz O (2004) Determination of aeration rate and kinetics of composting some agricultural wastes. Bioresour Technol 93:49–57
Kuroda K, Osada T, Yonaga M, Kanematu A, Nitta T, Mouri S, Kojima T (1996) Emissions of malodorous compounds and greenhouse gases from composting swine feces. Bioresour Technol 56:265–271
Liu XD, Tiquia SM, Holguin G, Wu LY, Nold SC, Devol AH, Luo K, Palumbo AV, Tiedje JM, Zhou JZ (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
Ma WK, Bedard-Haughn A, Siciliano SD, Farrell RE (2008) Relationship between nitrifier and denitrifier community composition and abundance in predicting nitrous oxide emissions from ephemeral wetland soils. Soil Biol Biochem 40:1114–1123
Maeda K, Toyoda S, Shimojima R, Osada T, Hanajima D, Morioka R, Yoshida N (2010a) Source of nitrous oxide emissions during the cow manure composting process as revealed by isotopomer analysis of and amoA abundance in Betaproteobacterial ammonia-oxidizing bacteria. Appl Environ Microbiol 76:1555–1562
Maeda K, Morioka R, Hanajima D, Osada T (2010b) The impact of using mature compost on nitrous oxide emission and the denitrifier community in the cattle manure composting process. Microb Ecol 59:25–36
Mergel A, Schmitz O, Mallmann T, Bothe H (2001) Relative abundance of denitrifying and dinitrogen-fixing bacteria in layers of a forest soil. FEMS Microbiol Ecol 36:33–42
Miller FC, Finstein MS (1985) Materials balance in the composting of wastewater sludge as affected by process control strategy. J Wat Pollut Contr Fed 57:122–127
Philippot L, Hallin S (2005) Finding the missing link between diversity and activity using denitrifying bacteria as a model functional community. Curr Opin Microbiol 8:234–239
Philippot L, Hallin S, Schloter M (2007) Ecology of denitrifying prokaryotes in agricultural soil. Adv Agron 96:249–305
Sommer SG, Møller HB (2000) Emission of greenhouse gases during composting of deep litter from pig production-effect of straw content. J Agric Sci Cambridge 134:327–335
Throbäck IN, Enwall K, Jarvis Å, 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
Tiquia SM (2002) Microbial transformation of nitrogen during composting. In: Insam HH (ed) Microbiology of composting and other biodegradation processes, Germany, pp 237–245
Wang C, Lu HH, Dong D, Deng H, Strong PJ, Wang HL, Wu WX (2013) Insight into the effects of biochar on manure composting: evidence supporting the relationship between N2O emission and denitrifying community. Environ Sci Technol 47:7341–7349
Warneck P (1999) Chemistry of the Natural Atmosphere. Academic, San Diego
Yoshida M, Ishii S, Otsuka S, Senoo K (2009) Temporal shifts in diversity and quantity of nirS and nirK in a rice paddy field soil. Soil Biol Biochem 41:2044–2051
Zeng GM, Zhang JC, Chen YN, Yu Z, Yu M, Li H, Liu ZF, Chen M, Lu LH, Hu CX (2011) Relative contributions of archaea and bacteria to microbial ammonia oxidation differ under different conditions during agricultural waste composting. Bioresour Technol 102:9026–9032
Zeng GM, Chen M, Zeng ZT (2013a) Risks of neonicotinoid pesticides. Science 340:1403
Zeng GM, Chen M, Zeng ZT (2013b) Shale gas: Surface water also at risk. Nature 499:154
Zhang JC, Zeng GM, Chen YN, Yu M, Yu Z, Li H, Yu Y, Huang HL (2011) Effects of physico-chemical parameters on the bacterial and fungal communities during agricultural waste composting. Bioresour Technol 102:2950–2956
Zhou ZF, Zheng YM, Shen JP, Zhang LM, He JZ (2011) Response of denitrification genes nirS, nirK and nosZ to irrigation water quality in a Chinese agricultural soil. Environ Sci Pollut Res 18:1644–1652
Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol R 61:533–536
Acknowledgments
This study was financially supported by the National Natural Science Foundation of China (51039001, 51378190, 51408219, 21407046, 51108423), the Hunan Provincial Natural Science Foundation of China (10JJ7005), the Zhejiang Provincial Natural Science Foundation of China (Y5100234).
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Zhang, L., Zeng, G., Zhang, J. et al. Response of denitrifying genes coding for nitrite (nirK or nirS) and nitrous oxide (nosZ) reductases to different physico-chemical parameters during agricultural waste composting. Appl Microbiol Biotechnol 99, 4059–4070 (2015). https://doi.org/10.1007/s00253-014-6293-3
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DOI: https://doi.org/10.1007/s00253-014-6293-3