The effect of soil moisture on the response by fungi and bacteria to nitrogen additions for N2O production

Lei Zhang , Junqiang Zheng , Xu Han , Junhui Zhang , Chengxu Li , Shicong Geng , Shijie Han

Journal of Forestry Research ›› 2020, Vol. 32 ›› Issue (5) : 2037 -2045.

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Journal of Forestry Research ›› 2020, Vol. 32 ›› Issue (5) : 2037 -2045. DOI: 10.1007/s11676-020-01262-z
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The effect of soil moisture on the response by fungi and bacteria to nitrogen additions for N2O production

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Abstract

In addition to bacteria, the contribution of fungi to nitrous oxide (N2O) production has been recognized but the responses of these two broad and unrelated groups of microorganisms to global environmental changes, atmospheric nitrogen (N) deposition, and precipitation in terms of N2O production are unclear. We studied how these two microbial-mediated N2O production pathways responded to soil moisture conditions and to N addition in an N-limited temperate forest. Soils from a long-term N addition experiment in Changbai Mountain, northeastern China were incubated. Varied concentrations of cycloheximide and streptomycin, both inhibitors of fungal and bacterial activity, were used to determine the contributions of both to N2O production in 66%, 98% and 130% water-filled pore spaces (WFPS). The results showed that N2O production decreased significantly with increasing cycloheximide concentration whereas streptomycin was only inhibiting N2O emissions at 98% and 130% WFPS. The bacterial pathway of N2O production in N-addition (Nadd) soil was significantly more dominant than that in untreated (Namb) soil. The difference in the fungal pathway of N2O production between the soil with nitrogen addition and the untreated soil was not significant. Net N2O emissions increased with increasing soil moisture, especially at 130% WFPS, a completely flooded condition. Bacteria dominated carbon dioxide (CO2) and N2O emissions in Nadd soil and at 130% WFPS regardless of N status, while fungi dominated CO2 and N2O emissions in soil without N addition at 66% and 98% WFPS. The results suggest that flooded soil is an important source of N2O emissions and that bacteria might be better adapted to compete in fertile soils under anoxic conditions.

Keywords

Nitrous oxide / Fungi / Bacteria / Nitrogen addition / Soil moisture conditions

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Lei Zhang, Junqiang Zheng, Xu Han, Junhui Zhang, Chengxu Li, Shicong Geng, Shijie Han. The effect of soil moisture on the response by fungi and bacteria to nitrogen additions for N2O production. Journal of Forestry Research, 2020, 32(5): 2037-2045 DOI:10.1007/s11676-020-01262-z

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References

[1]

Anderson JPE, Domsch KH. Quantification of bacterial and fungal contributions to soil respiration. Arch Mikrobiol, 1973, 93(2): 113-127.

[2]

Bai E, Li W, Li SL, Sun JF, Peng B, Dai W, Jiang P, Han SJ. Pulse increase of soil N2O emission in response to N addition in a temperate forest on Mt Changbai, northeast China. PLoS One, 2014 9 7

[3]

Bailey VL, Smith JL, Bolton H. Novel antibiotics as inhibitors for the selective respiratory inhibition method of measuring fungal: bacterial ratios in soil. Biol Fert Soils, 2003, 38(3): 154-160.

[4]

Basiliko N, Moore TR, Jeannotte R, Bubier JL. Nutrient input and carbon and microbial dynamics in an ombrotrophic bog. Geomicrobiol J, 2006, 23(7): 531-543.

[5]

Bateman EJ, Baggs EM. Contributions of nitrification and denitrification to N2O emissions from soils at different water-filled pore space. Biol Fert Soils, 2005, 41(6): 379-388.

[6]

Blackmer AM, Bremner JM. Inhibitory effect of nitrate on reduction of N2O to N2 by soil microorganisms. Soil Biol Biochem, 1979, 10(3): 187-191.

[7]

Blagodatskaya E, Dannenmann M, Gasche R, Butterbach-Bahl K. Microclimate and forest management alter fungal-to-bacterial ratio and N2O-emission during rewetting in the forest floor and mineral soil of mountainous beech forests. Biogeochemistry, 2010, 97(1): 55-70.

[8]

Blagodatskiy SA, Avksent’Ev AA, Davydova MA, Blagodatskaya EV, Kurakov AV. Nitrous oxide production in soils and the ratio of the fungal to bacterial biomass. Eurasian Soil Sci, 2008, 41(13): 1448-1455.

[9]

Bollag JM, Tung G. Nitrous oxide release by soil fungi. Soil Biol Biochem, 1972, 4(3): 271-276.

[10]

Boyle SA, Yarwood RR, Bottomley PJ, Myrold DD. Bacterial and fungal contributions to soil nitrogen cycling under Douglas fir and red alder at two sites in Oregon. Soil Biol Biochem, 2008, 40(2): 443-451.

[11]

Bragazza L, Buttler A, Habermacher J, Brancaleoni L, Gerdol R, Fritze H, Hanajík P, Laiho R, Johnson D. High nitrogen deposition alters the decomposition of bog plant litter and reduces carbon accumulation. Glob Chang Biol, 2012, 18(3): 1163-1172.

[12]

Butterbach-Bahl K, Baggs EM, Dannenmann M, Kiese R, Zechmeister-Boltenstern S. Nitrous oxide emissions from soils: how well do we understand the processes and their controls?. Philos Trans R Soc B, 2013 368 1621 20130122

[13]

Chen H, Mothapo NV, Shi W. The significant contribution of fungi to soil N2O production across diverse ecosystems. Appl Soil Ecol, 2014, 73(1): 70-77.

[14]

Chen H, Mothapo NV, Shi W. Soil moisture and pH control relative contributions of fungi and bacteria to N2O production. Microb Ecol, 2015, 69(1): 180-191.

[15]

Crenshaw CL, Lauber C, Sinsabaugh RL, Stavely LK. Fungal control of nitrous oxide production in semiarid grassland. Biogeochemistry, 2008, 87(1): 17-27.

[16]

Dendooven L, Anderson JM. Dynamics of reduction enzymes involved in the denitrification process in pasture soil. Soil Biol Biochem, 1994, 26(11): 1501-1506.

[17]

Dendooven L, Splatt P, Anderson JM. The use of chloramphenicol in the study of the denitrification process: some side-effects. Soil Biol Biochem, 1994, 26(7): 925-927.

[18]

Dobbie KE, Smith KA. The effect of water table depth on emissions of N2O from a grassland soil. Soil Use Manag, 2010, 22(1): 22-28.

[19]

Dobbie KE, Smith KA. The effects of temperature, water-filled pore space and land use on N2O emissions from an imperfectly drained gleysol. Eur J Soil Sci, 2010, 52(4): 667-673.

[20]

Geng S (2017) The study on soil nitrogen loss and its key processes in a broad-leaved Korean pine (Pinus koraiensis) mixed forest. Dissertation, University of Chinese Academy of Sciences, Beijing, China

[21]

Geng S, Chen Z, Han SJ, Wang F, Zhang JH. Rainfall reduction amplifies the stimulatory effect of nitrogen addition on N2O emissions from a temperate forest soil. Sci Rep, 2017, 7: 43329.

[22]

Hall SJ, Matson PA. Nitrogen oxide emissions after nitrogen additions in tropical forests. Nature, 1999, 400(400): 152-155.

[23]

Horwath WR. Paul EA. Carbon cycling and formation of soil organic matter. Soil microbiology ecology biochemistry, 2007 3 Oxford: Academic 303 339

[24]

IPCC Solomon S Climate change - the physical science basis. Contribution of Working Group I to the fourth assessment report of the intergovernmental panel on climate change, 2007, Cambridge University Press: Cambridge.

[25]

Iurii S, Neville M, G Philip R. Global meta-analysis of the nonlinear response of soil nitrous oxide (N2O) emissions to fertilizer nitrogen. Proc Natl Acad Sci U S A, 2014, 111(25): 9199-9204.

[26]

Jenssen M, Butterbachbahl K, Hofmann G, Papen H. Exchange of trace gases between soils and the atmosphere in Scots pine forest ecosystems of the northeastern German lowlands - 2. A novel approach to scale up N2O- and NO-fluxes from forest soils by modeling their relationships to vegetation structure. For Ecol Manag, 2002, 167(1): 123-134.

[27]

Jørgensen CJ, Elberling B. Effects of flooding-induced N2O production, consumption and emission dynamics on the annual N2O emission budget in wetland soil. Soil Biol Biochem, 2012, 53: 9-17.

[28]

Killham K, Prosser JI. 5 – The prokaryotes. Soil microbiology ecology biochemistry, 2007, Burlington, MA: Academic 119 144

[29]

Kolb S, Horn MA. Microbial CH4 and N2O consumption in acidic wetlands. Front Microbiol, 2012, 3: 78.

[30]

Kurakov AV, Nosikov AN, Skrynnikova EV, L’Vov NP. Nitrate reductase and nitrous oxide production by Fusarium oxysporum 11dn1 under aerobic and anaerobic conditions. Curr Microbiol, 2000 41 2 114

[31]

Kurakov AV, Zvygintsev DG, Lavrentev RB, Umarov MM (2002) Microscopic fungi isolated under anaerobic conditions from soils and their activity of nitrous oxide production. Simposia of the 17 World Congress of Soil Science. Bangkok, Thailand

[32]

Land L, Badalucco L, Pomarě F, Nannipieri P. Effectiveness of antibiotics to distinguish the contributions of fungi and bacteria to net nitrogen mineralization, nitrification and respiration. Soil Biol Biochem, 1993, 25(12): 1771-1778.

[33]

Laughlin RJ, Stevens RJ. Evidence for fungal dominance of denitrification and codenitrification in a grassland soil. Soil Sci Soc Am J, 2002, 66(5): 1540-1548.

[34]

Laughlin RJ, Rütting T, Müller C, Watson CJ, Stevens RJ. Effect of acetate on soil respiration, N2O emissions and gross N transformations related to fungi and bacteria in a grassland soil. Appl Soil Ecol, 2009, 42(1): 25-30.

[35]

Lavigne MB, Foster RJ, Goodine G. Seasonal and annual changes in soil respiration in relation to soil temperature, water potential and trenching. Tree Physiol, 2004, 24(4): 415-424.

[36]

Lavrent’ev RB, Zaitsev SA, Sudnitsyn II, Kurakov AV. Nitrous oxide production by fungi in soils under different moisture levels. Moscow Univ Soil Sci Bull, 2008, 63(4): 178-183.

[37]

Lee SH, Kim SY, Ding W, Kang H. Impact of elevated CO2 and N addition on bacteria, fungi, and archaea in a marsh ecosystem with various types of plants. Appl Microbiol Biotechnol, 2015, 99(12): 5295-5305.

[38]

Li BC, Wu QF, Zhang JL, Qian M, Qin H, Xu QF. Fungal and bacterial contribution to soil N2O production in and broadleaf forest ecosystems. J Zhejiang A&F Univ, 2014, 31(6): 919-925.

[39]

Lin Q, Brookes PC. Comparison of substrate induced respiration, selective inhibition and biovolume measurements of microbial biomass and its community structure in unamended, ryegrass-amended, fumigated and pesticide-treated soils. Soil Biol Biochem, 1999, 31(14): 1999-2014.

[40]

Madigan MT, Martinko JM, Parker J. Brock’s biology of microorganisms, 2000 9 Upper Saddle River: Prentice Hall.

[41]

Maeda K, Toyoda S, Philippot L, Hattori S, Nakajima K, Ito Y, Yoshida N. Relative contribution of nirK- and nirS- bacterial denitrifiers as well as fungal denitrifiers to nitrous oxide production from dairy manure compost. Environ Sci Technol, 2017, 51(24): 14083-14091.

[42]

Mclain JET, Martens DA. N2O production by heterotrophic N transformations in a semiarid soil. Appl Soil Ecol, 2006, 32(2): 253-263.

[43]

Moore T, Basiliko N. Wieder RK, Vitt DH. Decomposition in boreal peatlands. Boreal peatland ecosystems, 2006, Berlin: Springer 125 143

[44]

Myers B, Webster KL, Mclaughlin JW, Basiliko N. Microbial activity across a boreal peatland nutrient gradient: the role of fungi and bacteria. Wetl Ecol Manag, 2012, 20(2): 77-88.

[45]

Parkinson D, Gray TRG, Williams ST. Methods for studying the ecology of soil microorganisms, 1971, Oxford: Blackwell Scientific Publications 1 538

[46]

Rochette P, Tremblay N, Fallon E, Angers DA, Chantigny MH, Macdonald JD, Bertrand N, Parent . N2O emissions from an irrigated and non-irrigated organic soil in eastern Canada as influenced by N fertilizer addition. Eur J Soil Sci, 2010, 61(2): 186-196.

[47]

Rogers JE, Whitman WB. Microbial production and consumption of greenhouse gases: methane, nitrogen oxides, and halomethanes. J Environ Qual, 1991, 23(1): 211-212.

[48]

Rudaz AO, Wälti E, Kyburz G, Lehmann P, Fuhrer J. Temporal variation in N2O and N2 fluxes from a permanent pasture in Switzerland in relation to management, soil water content and soil temperature. Agric Ecosyst Environ, 1999, 73(1): 83-91.

[49]

Ruser R, Flessa H, Russow R, Schmidt G, Buegger F, Munch JC. Emission of N2O, N2 and CO2 from soil fertilized with nitrate: effect of compaction, soil moisture and rewetting. Soil Biol Biochem, 2006, 38(2): 263-274.

[50]

Schindlbacher A, Zechmeister-Boltenstern S, Butterbach-Bahl K (2004) Effects of soil moisture and temperature on NO, NO2, and N2O emissions from European forest soils. J Geophys Res-Atmos 109(D17302). https://doi.org/10.1029/2004JD004590

[51]

Schönwiese CD, Houghton JT, Meira Filho LG, Callander BA, Harris N, Kattenberg A, Maskell K. Climate change 1995, the science of climate change. J Atmos Chem, 1997, 27(1): 105-106.

[52]

Scott-Denton L, Rosenstiel T, Monson R. Differential controls by climate and substrate over the heterotrophic and rhizospheric components of soil respiration. Glob Chang Biol, 2010, 12(2): 205-216.

[53]

Skiba U, Smith KA, Fowler D. Nitrification and denitrification as sources of nitric oxide and nitrous oxide in a sandy loam soil. Soil Biol Biochem, 1993, 25(11): 1527-1536.

[54]

Smith KA, Thomson PE, Clayton H, Mctaggart IP, Conen F. Effects of temperature, water content and nitrogen fertilisation on emissions of nitrous oxide by soils. Atmos Environ, 1998, 32(19): 3301-3309.

[55]

Stevens RJ, Laughlin RJ, Malone JP. Soil pH affects the processes reducing nitrate to nitrous oxide and di-nitrogen. Soil Biol Biochem, 1998, 30(8–9): 1119-1126.

[56]

Velvis H. Evaluation of the selective respiratory inhibition method for measuring the ratio of fungal: bacterial activity in acid agricultural soils. Biol Fert Soils, 1997, 25(4): 354-360.

[57]

Vries FTD, Groenigen JWV, Hoffland E, Bloem J. Nitrogen losses from two grassland soils with different fungal biomass. Soil Biol Biochem, 2011, 43(5): 997-1005.

[58]

Wang WJ, Dalal RC, Moody PW, Smith CJ. Relationships of soil respiration to microbial biomass, substrate availability and clay content. Soil Biol Biochem, 2003, 35(2): 273-284.

[59]

Wang Q, Liu YR, Zhang CJ, Zhang LM, Han LL, Shen JP. Responses of soil nitrous oxide production and abundances and composition of associated microbial communities to nitrogen and water amendment. Biol Fert Soils, 2017, 1: 1-11.

[60]

Xing L (2017) Effect of soil water content on N2O diffusion process and reduction process. Dissertation, Shanxi Normal University, Shanxi, China

[61]

Xu J (2018a) Comparative study on the field capacity based on different test methods. Dissertation, Jilin University, Jilin, China

[62]

Xu TT (2018b) Responses of soil nitrogen transformation and underlying microbial mechanisms to nitrogen deposition and rainfall reduction in Changbai Forests. Dissertation, University of Chinese Academy of Sciences, Beijing, China

[63]

Zhou Z, Takaya N, Sakairi MAC, Shoun H. Oxygen requirement for denitrification by the fungus Fusarium oxysporum. Arch Microbiol, 2001, 175(1): 19-25.

[64]

Zhu TB, Meng TZ, Zhang JB, Zhong WH, Müller C, Cai ZC. Fungi-dominant heterotrophic nitrification in a subtropical forest soil of China. J Soils Sediments, 2015, 15(3): 705-709.

[65]

Zumft WG. Cell biology and molecular basis of denitrification. J Microbiol Mol Biol Rev, 1997, 61(4): 533-536.

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