Fungi dominate denitrification when Chinese milk vetch green manure is used in paddy soil

Minghe Jiang, Luan Zhang, Ming Liu, Han Qiu, Shungui Zhou

PDF(838 KB)
PDF(838 KB)
Soil Ecology Letters ›› 2022, Vol. 4 ›› Issue (2) : 155-163. DOI: 10.1007/s42832-020-0064-0
RESEARCH ARTICLE
RESEARCH ARTICLE

Fungi dominate denitrification when Chinese milk vetch green manure is used in paddy soil

Author information +
History +

Highlights

• We evaluated effects of fungi on N2O emission in Chinese milk vetch-containing soils.

• Fungi to contributed to soil N2O production in CMV-amended soils.

• Fungi accounted for 56% of N2O emission in CMV-amended soils.

• Fungi may be important contributors to N2O production in CMV-amended soils.

Abstract

Fungi play an important role in soil nitrous oxide (N2O) emission in many agricultural soil systems. However, the effect of fungi on N2O emission in Chinese milk vetch (CMV)-containing soils has not been examined sufficiently. This study investigated the contribution of bacteria and fungi to soil N2O emission in CMV-amended soils. We compared soils from an experimental field in the Fujian Academy of Agricultural Sciences that had been treated with 30 000 kg of CMV per 667 m2 per year with one that was not treated with CMV. We incubated soil using cycloheximide and streptomycin to differentiate fungal and bacterial N2O emissions, respectively. Quantitative PCR (qPCR) was performed to investigate bacterial and fungal abundances in the two agricultural soil ecosystems. The contribution of fungi to soil N2O emission in CMV-amended soils was greater than that in non-CMV-amended paddy soils, with fungi accounting for more than 56% of the emissions in CMV-amended soils. Quantitative PCR showed that the ratio of the internal transcribed spacer to 16S rDNA was significantly higher in CMV-amended soils than in non-CMV-amended paddy soils. Furthermore, soil properties, such as pH (P<0.05) and NH4+ concentration (P<0.05), significantly and negatively affected N2O emission by fungi in soil, whereas the total organic carbon (P<0.05) and NO3- concentration (P<0.05) showed significant positive effects. Fungi may be important contributors to N2O production in CMV-amended soils, which may create challenges for mitigating N2O production.

Graphical abstract

Keywords

Fungi / Bacteria / Nitrous oxide / Chinese milk vetch / Paddy soil

Cite this article

Download citation ▾
Minghe Jiang, Luan Zhang, Ming Liu, Han Qiu, Shungui Zhou. Fungi dominate denitrification when Chinese milk vetch green manure is used in paddy soil. Soil Ecology Letters, 2022, 4(2): 155‒163 https://doi.org/10.1007/s42832-020-0064-0

References

[1]
Ai, C., Liang, G., Wang, X., Sun, J., He, P., Zhou, W., 2017. A distinctive root-inhabiting denitrifying community with high N2O/(N2O+ N2) product ratio. Soil Biology & Biochemistry 109, 118–123
CrossRef Google scholar
[2]
Anderson, J.P.E., Domsch, K.H., 1973. Quantification of bacterial and fungal contributions to soil respiration. Archives of Microbiology 93, 113–127.
[3]
Badalucco, L., Pomare, F., Grego, S., Landi, L., Nannipieri, P., 1994. Activity and degradation of streptomycin and cycloheximide in soil. Biology and Fertility of Soils 18, 334–340
CrossRef Google scholar
[4]
Baggs, E.M., Smales, C.L., Bateman, E.J., 2010. Changing pH shifts the microbial sourceas well as the magnitude of N2O emission from soil. Biology and Fertility of Soils 46, 793–805
CrossRef Google scholar
[5]
Beare, M.H., Neely, C.L., Coleman, D.C., Hargrove, W.L., 1990. A substrate-induced respiration (SIR) method for measurement of fungal and bacterial biomass on plant residues. Soil Biology & Biochemistry 22, 585–594
CrossRef Google scholar
[6]
Bolan, N., Hedley, M., White, R., 1991. Processes of soil acidification during nitrogen cycling with emphasis on legume based pastures. Plant and Soil 134, 53–63
CrossRef Google scholar
[7]
Bouwman, A., 1998. Environmental science: Nitrogen oxides and tropical agriculture. Nature 392, 866–867
CrossRef Google scholar
[8]
Butterbach-Bahl, K., Baggs, E.M., Dannenmann, M., Kiese, R., Zechmeister-Boltenstern, S., 2013. Nitrous oxide emissions from soils: how well do we understand the processes and their controls? Philosophical Transactions of the Royl Society B, Biological Sciences 368, 20130122
[9]
Cabello, P., Roldan, M.D., Moreno-Vivian, C., 2004. Nitrate reduction and the nitrogen cycle in archaea. Microbiol-Sgm 150, 3527–3546
CrossRef Google scholar
[10]
Chen, H., Mothapo, N.V., Shi, W., 2014. The significant contribution of fungi to soil N2O production across diverse ecosystems. Applied Soil Ecology 73, 70–77
CrossRef Google scholar
[11]
Chen, H.H., Mothapo, N.V., Shi, W., 2015. Fungal and bacterial N2O production regulated by soil amendments of simple and complex substrates. Soil Biology & Biochemistry 84, 116–126
CrossRef Google scholar
[12]
Chen, Y.F., Hu, N., Zhang, Q.Z., Lou, Y.L., Li, Z.F., Tang, Z., Kuzyakov, Y., Wang, Y.D., 2019. Impacts of green manure amendment on detritus micro-food web in a double-rice cropping system. Applied Soil Ecology 138, 32–36
CrossRef Google scholar
[13]
Crenshaw, C.L., Lauber, C., Sinsabaugh, R.L., Stavely, L.K., 2008. Fungal control of nitrous oxide production in semiarid grassland. Biogeochemistry 87, 17–27
CrossRef Google scholar
[14]
Davidson, E.A., 1991. Fluxes of nitrous oxide and nitric oxide from terrestrial ecosystems. In: Rogers, J.E., Whitman, W.B., eds. Microbial Production and Consumption of Greenhouse Gases: Methane, Nitrogen Oxides, and halomethanes, American Society for Microbiology, Washington, DC, pp. 219–235.
[15]
Davidson, E.A., Kanter, D., 2014. Inventories and scenarios of nitrous oxide emissions. Environmental Research Letters 9, 105012
CrossRef Google scholar
[16]
de Boer, W., Folman, L.B., Summerbell, R.C., Boddy, L., 2005. Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiology Reviews 29, 795–811
CrossRef Google scholar
[17]
Dolling, P., 1995. Effect of lupins and location on soil acidification rates. Australian Journal of Experimental Agriculture 35, 753–763
CrossRef Google scholar
[18]
Hadas, A., Kautsky, L., Goek, M., Kara, E.E., 2004. Rates of decomposition of plant residues and available nitrogen in soil, related to residue composition through simulation of carbon and nitrogen turnover. Soil Biology & Biochemistry 36, 255–266
CrossRef Google scholar
[19]
Hoben, J.P., Gehl, R.J., Millar, N., Grace, P.R., Robertson, G.P., 2011. Nonlinear nitrous oxide (N2O) response to nitrogen fertilizer in on-farm corn crops of the US Midwest. Global Change Biolology. 17, 1140–1152
CrossRef Google scholar
[20]
Hu, H.W., Zhang, L.M., Dai, Y., Di, H.J., He, J.Z., 2013. pH-dependent distribution of soil ammonia oxidizers across a large geographical scale as revealed by high-throughput pyrosequencing. Journal of Soils and Sediments 13, 1439–1449
CrossRef Google scholar
[21]
Huang, Y., Xiao, X., Long, X., 2017. Fungal denitrification contributes significantly to N2O production in a highly acidic tea soil. Journal of Soils and Sediments 17, 1599–1606
CrossRef Google scholar
[22]
Jirout, J., Šimek, M., Elhottová, D., 2013. Fungal contribution to nitrous oxide emissions from cattle impacted soils. Chemosphere 90, 565–572
CrossRef Google scholar
[23]
Khalil, M., Baggs, E., 2005. CH4 oxidation and N2O emissions at varied soil water-filled pore spaces and headspace CH4 concentrations. Soil Biology & Biochemistry 37, 1785–1794
CrossRef Google scholar
[24]
Kinney, C.A., Mosier, A.R., Ferrer, I., Furlong, E.T., Mandernack, K.W., 2004. Effects of the fungicides mancozeb and chlorothalonil on fluxes of CO2, N2O, and CH4 in a fertilized Colorado grassland soil. Journal of Geophysical Research. Atmospheres109, D05303.
[25]
Lassey, K., Harvey, M., 2007. Nitrous oxide: the serious side of laughing gas. Water Atmos 15, 10–11.
[26]
Laughlin, R.J., Rutting, T., Mueller, C., Watson, C.J., Stevens, R.J., 2009. Effect of acetate on soil respiration, N2O emissions and gross N transformations related to fungi and bacteria in a grassland soil. Applied Soil Ecology 42, 25–30
CrossRef Google scholar
[27]
Laughlin, R.J., Stevens, R.J., 2002. Evidence for fungal dominance of denitrification and codenitrification in a grassland soil. Soil Science Society of America Journal 66, 1540–1548
CrossRef Google scholar
[28]
Laughlin, R.J., Stevens, R.J., Muller, C., Watson, C.J., 2008. Evidence that fungi can oxidize NH4+ to NO3- in a grassland soil. European Journal of Soil Science 59, 285–291
CrossRef Google scholar
[29]
Liang, C., Schimel, J.P., Jastrow, J.D., 2017. The importance of anabolism in microbial control over soil carbon storage. Nature Microbiology 2, 2
CrossRef Google scholar
[30]
McNeill, A.M., Zhu, C., Fillery, I.R., 1997. Use of in situ 15N-labelling to estimate the total below-ground nitrogen of pasture legumes in intact soil–plant systems. Australian Journal of Agricultural Research 48, 295–304
CrossRef Google scholar
[31]
Mothapo, N., Chen, H., Cubeta, M.A., Grossman, J.M., Fuller, F., Shi, W., 2015. Phylogenetic, taxonomic and functional diversity of fungal denitrifiers and associated N2O production efficacy. Soil Biology & Biochemistry 83, 160–175
CrossRef Google scholar
[32]
Mothapo, N.V., Chen, H.H., Cubeta, M.A., Shi, W., 2013. Nitrous oxide producing activity of diverse fungi from distinct agroecosystems. Soil Biology & Biochemistry 66, 94–101
CrossRef Google scholar
[33]
Noble, A., Zenneck, I., Randall, P., 1996. Leaf litter ash alkalinity and neutralisation of soil acidity. Plant and Soil 179, 293–302
CrossRef Google scholar
[34]
Poll, C., Marhan, S., Ingwersen, J., Kandeler, E., 2008. Dynamics of litter carbon turnover and microbial abundance in a rye detritusphere. Soil Biology & Biochemistry 40, 1306–1321
CrossRef Google scholar
[35]
Ravishankara, A., Daniel, J.S., Portmann, R.W., 2009. Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326, 123–125
CrossRef Google scholar
[36]
Rousk, J., Baath, E., Brookes, P.C., Lauber, C.L., Lozupone, C., Caporaso, J.G., Knight, R., Fierer, N., 2010. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME Journal 4, 1340–1351
CrossRef Google scholar
[37]
Rutting, T., Huygens, D., Boeckx, P., Staelens, J., Klemedtsson, L., 2013. Increased fungal dominance in N2O emission hotspots along a natural pH gradient in organic forest soil. Biology and Fertility of Soils 49, 715–721
CrossRef Google scholar
[38]
Soares, M., Rousk, J., 2019. Microbial growth and carbon use efficiency in soil: Links to fungal-bacterial dominance, SOC-quality and stoichiometry. Soil Biology & Biochemistry 131, 195–205
CrossRef Google scholar
[39]
Tang, C., Yu, Q., 1999. Impact of chemical composition of legume residues and initial soil pH on pH change of a soil after residue incorporation. Plant and Soil 215, 29–38
CrossRef Google scholar
[40]
Thiet, R.K., Frey, S.D., Six, J., 2006. Do growth yield efficiencies differ between soil microbial communities differing in fungal: bacterial ratios? Reality check and methodological issues. Soil Biology & Biochemistry 38, 837–844
CrossRef Google scholar
[41]
Thomson, A.J., Giannopoulos, G., Pretty, J., Baggs, E.M., Richardson, D.J., 2012. Biological sources and sinks of nitrous oxide and strategies to mitigate emissions. Philos T R Soc B 367, 1157–1168
CrossRef Google scholar
[42]
Van den Heuvel, R.N., Bakker, S.E., Jetten, M.S.M., Hefting, M.M., 2011. Decreased N2O reduction by low soil pH causes high N2O emissions in a riparian ecosystem. Geobiology 9, 294–300
CrossRef Google scholar
[43]
Wang, Y.F., Tang, C.X., Wu, J.J., Liu, X.M., Xu, J.M., 2013. Impact of organic matter addition on pH change of paddy soils. Journal of Soils and Sediments 13, 12–23
CrossRef Google scholar
[44]
Xie, Z.J., Zhou, C.H., Shah, F., Iqbal, A., Ni, G.R. (2018) The role of Chinese Milk Vetch as cover crop in complex soil nitrogen dynamics in rice rotation system of South China. Sci Rep-Uk 8
[45]
Xu, J.M., Tang, C., Chen, Z.L., 2006a. Chemical composition controls residue decomposition in soils differing in initial pH. Soil Biology & Biochemistry 38, 544–552
CrossRef Google scholar
[46]
Xu, J.M., Tang, C., Chen, Z.L., 2006b. The role of plant residues in pH change of acid soils differing in initial pH. Soil Biology & Biochemistry 38, 709–719
CrossRef Google scholar
[47]
Xu, R.K., Coventry, D.R., 2003. Soil pH changes associated with lupin and wheat plant materials incorporated in a red-brown earth soil. Plant and Soil 250, 113–119
CrossRef Google scholar
[48]
Yanai, Y., Toyota, K., Morishita, T., Takakai, F., Hatano, R., Limin, S.H., Darung, U., Dohong, S., 2007. Fungal N2O production in an arable peat soil in Central Kalimantan, Indonesia. Soil Science and Plant Nutrition 53, 806–811
CrossRef Google scholar
[49]
Yang, Z.P., Zheng, S.X., Nie, J., Liao, Y.L., Xie, J., 2014. Effects of long-term winter planted green manure on distribution and storage of organic carbon and nitrogen in water-stable aggregates of reddish paddy soil under a double-rice cropping system. Journal of Integrative Agriculture 13, 1772–1781
CrossRef Google scholar
[50]
Zhang, L., Jiang, M., Ding, K., Zhou, S., 2019. Iron oxides affect denitrifying bacterial communities with the nirS and nirK genes and potential N2O emission rates from paddy soil. European Journal of Soil Biology 93, 103093
CrossRef Google scholar
[51]
Zhang, X., Guan, P., Wang, Y., Li, Q., Zhang, S., Zhang, Z., Bezemer, T.M., Liang, W., 2015. Community composition, diversity and metabolic footprints of soil nematodes in differently-aged temperate forests. Soil Biology & Biochemistry 80, 118–126
CrossRef Google scholar
[52]
Zhao, S.C., Qiu, S.J., Xu, X.P., Ciampitti, I.A., Zhang, S.Q., He, P., 2019. Change in straw decomposition rate and soil microbial community composition after straw addition in different long-term fertilization soils. Applied Soil Ecology 138, 123–133
CrossRef Google scholar
[53]
Zhong, L., Bowatte, S., Newton, P.C.D., Hoogendoorn, C.J., Luo, D.W., 2018. An increased ratio of fungi to bacteria indicates greater potential for N2O production in a grazed grassland exposed to elevated CO2. Agriculture, Ecosystems & Environment 254, 111–116
CrossRef Google scholar
[54]
Zumft, W.G., 1997. Cell biology and molecular basis of denitrification. Microbiology and Molecular Biology Reviews 61, 533–616
CrossRef Google scholar

Acknowledgments

The research was funded by the National Natural Science Foundation of China (Project No. 31600425). We also thank Fujian Academy of Agricultural Sciences for providing the soil samples for our analysis.

RIGHTS & PERMISSIONS

2020 Higher Education Press
AI Summary AI Mindmap
PDF(838 KB)

Accesses

Citations

Detail

Sections
Recommended

/