Abstract
Aims
Tree species and seasonal change influence N2O flux and microbial communities, but the mechanisms are unclear. We studied N2O flux in soils planted with slash pine and oil-seed camellia trees. We sampled on typical days of the four seasons. We tested whether N-cycling communities respond more to tree species or seasonal change. We assessed how tree species affect N2O flux.
Methods
We used qPCR and RFLP to determine abundance and community composition of amoA-containing bacteria (AOB) and archaea (AOA), and denitrifiers that contain the narG, nirK, nirS, and nosZ genes.
Results
N2O flux rate and soil characteristics varied significantly between forest soils and sampling seasons. Abundance of all detected genes, but not of the nirS gene, was significantly affected by tree species. Differences in gene abundance between days in different seasons were found only for narG, nirK, and nosZ. Functional microbial community composition in the soil varied between the tree species for most of the genes studied, but varied, not significantly, slightly among sampling days. Differences in the abundance and community composition of nitrifiers and denitrifiers between tree species depended on soil concentration of NH4+, NO3−, and dissolved organic carbon (DOC). N2O flux rate was affected by community composition, but not abundance of nitrifiers and denitrifiers. Temperature, NO3−, and DOC concentrations significantly affected N2O flux.
Conclusions
Tree species influenced N2O flux more than seasonal change, by altering community composition and environmental factors rather than nitrifier/denitrifier abundance.
Similar content being viewed by others
References
Ambus P, Zechmeister-Boltenstern S, Butterbach-Bahl K (2006) Sources of nitrous oxide emitted from European forest soils. Biogeosciences 3:135–145
Binkley D, Giardina C (1998) Why do tree species affect soils? The warp and woof of tree-soil interactions. Biogeochemistry 42:89–106
Brown JR, Blankinship JC, Niboyet A, van Groenigen KJ, Dijkstra P, Le Roux X, Leadley PW, Hungate BA (2012) Effects of multiple global change treatments on soil N2O fluxes. Biogeochmistry 109:85–100
Chen Z, Luo X, Hu RG, Wu MN, Wu J, 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
Cuhel J, Simek M, Laughlin RJ, Bru D, Chèneby D (2010) Insights into the effect of soil pH on N2O and N2 emission and denitrifier community size and activity. Appl Environ Microbiol 76:1870–1878
DeAngelis KM, Silver WL, Thompson AW, Firestone MK (2010) Microbial communities acclimate to recurring changes in soil redox potential status. Environ Microbiol 12:3137–3149
Di HJ, Cameron KC, Shen JP, Winefield CS, O'Callaghan M (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2:621–624
Friedl J, Scheer C, Rowlings DW, Mcintosh HV, Strazzabosco A (2016) Denitrification losses from an intensively managed sub-tropical pasture – impact of soil moisture on the partitioning of N2 and N2O emissions. Soil Biol Biochem 92:58–66
Fujita Y, Bodegom PMV, Venterink HO, Han R, Witte JPM (2013) Towards a proper integration of hydrology in predicting soil nitrogen mineralization rates along natural moisture gradients. Soil Biol Biochem 58:302–312
Guardia G, Abalos D, García-Marco S, Quemada M, Alonso-Ayuso M, Cárdenas LM, Dixon ER, Vallejo A (2016) Integrated soil fertility management drives the effect of cover crops on GHG emissions in an irrigated field. Biogeosci Discuss 13:5245–5257
IPCC (2014) In: Pachauri RK, Meyer LA (Eds) Climate change 2014: synthesis report. Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change, Geneva, Switzerland, p 151
Jia Z, Conrad R (2009) Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11:1658–1671
Ju X, Christie P (2011) Calculation of theoretical nitrogen rate for simple nitrogen recommendations in intensive cropping systems: a case study on the North China plain. Field Crop Res 124:450–458
Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809
Levy-Booth DJ, Prescott CE, Grayston SJ (2014) Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems. Soil Biol Biochem 75:11–25
Liu LL, Greaver TL (2009) A review of nitrogen enrichment effects on three biogenic GHGs: the CO2 sink may be largely offset by stimulated N2O and CH4 emission. Ecol Lett 12:1103–1117
Liu JB, Hou HJ, Sheng R, Chen Z, Zhu YJ, Qin HL, Wei WX (2012) Denitrifying communities differentially respond to flooding drying cycles in paddy soils. Appl Soil Ecol 62:155–162
Liu X, Chen CR, Wang WJ, Hughes JM, Lewis T, Hou EQ, Shen JP (2013) Soil environmental factors rather than denitrification gene abundance control N2O fluxes in a wet sclerophyll forest with different burning frequency. Soil Biol Biochem 57:292–300
Luo HD, Zhu CF, Zhang L, Hu DN, Tu SP, Guo XM, Niu DK (2016) Effects of phosphorus fertilization levels on vegetative growth in Camellia oleifera. Non-wood Forest Res 34:52–56
Ma L, Shan J, Yan XY (2015) Nitrite behavior accounts for the nitrous oxide peaks following fertilization in a fluvo-aquic soil. Biol Fertil Soils 51:563–572
Menyailo OV, Hungate BA (2015) Tree species and moisture effects on soil sources of N2O: quantifying contributions from nitrification and denitrification with 18-O isotopes. J Geophys Res Biogeosci 111(G2)
Menyailo OV, Hungate BA, Zech W (2002) The effect of single tree species on soil microbial activities related to C and N cycling in the siberian artificial afforestation experiment: tree species and soil microbial activities. Plant Soil 242:183–196
Morishita T, Aizawa S, Yoshinaga S, Kaneko S (2011) Seasonal change in N2O flux from forest soils in a forest catchment in Japan. J For Res 16:386–393
Oura N, Shindo J, Fumoto T, Toda H, Kawashima H (2001) Effects of nitrogen deposition on nitrous oxide emissions from the forest floor. Water Air Soil Pollut 130:673–678
Phillips RL, McMillan AMS, Palmada T, Dando J, Giltrap D (2014) Temperature effects on N2O and N2 denitrification end-products for a New Zealand pasture soil. N Z J Agric Res 58:89–95
Qin HL, Yuan HZ, Zhang H, Zhu YJ, Yin CM, Tan ZJ, Wu JS, Wei WX (2013) Ammonia-oxidizing archaea are more important than ammonia-oxidizing bacteria in nitrification and NO3 −-N loss in acidic soil of sloped land. Biol Fertil Soils 49:767–776
Ravishankara AR, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125
Schindlbacher A, Zechmeister-Boltenstern S, Butterbach-Bahl SK (2004) Effects of soil moisture and temperature on NO, NO2, and N2O emissions from European forest soils. J Geophys Res Atmos 109:302
Schleper C (2010) Ammonia oxidation: different niches for bacteria and archaea? ISME J 4:1092–1094
Szukics U, Abell GCJ, Hodl V, Mitter B, Sessitsch A, Hackl E, Zechmeister-Boltenstern S (2010) Nitrifiers and denitrifiers respond rapidly to changed moisture and increasing temperature in a pristine forest soil. FEMS Microbiol Ecol 72:395–406
Wang L, Sheng R, Yang HC, Wang Q, Zhang WZ, Hou HJ, Wu JS, Wei WX (2017) Stimulatory effect of exogenous nitrate on soil denitrifiers and denitrifying activities in submerged paddy soil. Geoderma 286:64–72
Watanabe T, Kimura M, Asakawa S (2009) Distinct members of a stable methanogenic archaeal community transcribe mcrA genes under flooded and drained conditions in Japanese paddy field soil. Soil Biol Biochem 41:276–285
Wolf I, Brumme R (2002) Contribution of nitrification and denitrification sources for seasonal N2O emissions in an acid German forest soil. Soil Biol Biochem 34:741–744
Xu Y, Yang J, Chen W, Hou HJ, Li WH, Chen CL, Qin HL (2018) Bacterial community structure and abundance of plantation ecosystem soil response to seasonal change in red soil hilly region of southern. J Sou Agr 49:1289–1296
Yang CD, Wu J, Tan HL, Liu YX, Xiong LM, Zhou LQ, Xie RL, Huang GQ, Zhao QG (2014) Comparison on soil microbial activities and bacterial diversity between Betula alnoides and Pinus massoniana plantations in red soil region. Ecol Environ Sci 23:415–422
Yang O, Norton JM, Stark JM, Reeve JR, Habteselassie MY (2016) Ammonia-oxidizing bacteria are more responsive than archaea to nitrogen source in an agricultural soil. Soil Biol Biochem 96:4–15
Zhang GB, Ji Y, Ma J, Xu H, Cai ZC, Yagic K (2012) Intermittent irrigation changes production, oxidation, and emission of CH4 in paddy fields determined with stable carbon isotope technique. Soil Biol Biochem 52:108–116
Zhang Y, Ji GD, Wang RJ (2016) Functional gene groups controlling nitrogen transformation ratesin a groundwater-restoring denitrification biofilter under hydraulicretention time constraints. Ecol Eng 87:45–52
Zhang ZX, Zhang WZ, Yang HC, Sheng R, Wei WX, Qin HL (2017) Elevated N2O emission by the rice roots: based on the abundances of narG and bacterial amoA genes. Environ Sci Pollut Res 24:2116–2125
Zheng H, Ouyang ZY, Zhao TQ, Wang XK, Miao H, Peng YB (2006) Effect of different forest restoration approaches on soil biological properties. Chin J App Environ Biol 12:36–43
Zheng XH, Mei BL, Wang YH, Xie BH, Wang YS, Dong HB, Xu H, Chen GX, Cai ZC, Yue J (2008) Quantification of N2O fluxes from soil–plant systems may be biased by the applied gas chromatograph methodology. Plant Soil 311:211–234
Acknowledgments
This research was financially supported by the National Key Research and Development Program of China (2016YFD0200307), the National Natural Science Foundation of China (41771335, 41271280) and Hunan Provincial Natural Science Foundation of China (2016JJ3133). We would like to thank Editage [www.editage.cn] for English language editing.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Elizabeth M Baggs.
Highlights
• Tree species sharply affected in situ N2O flux and functional microbe community
• Abundance and structure of nitrifiers and denitrifiers varied between tree species depending on soil substrate availability
• Community structure of nitrifiers and denitrifiers was more affected by tree species than by seasonal change
• Microbial community composition rather than abundance determined N2O flux in acid forest soils
Electronic supplementary material
Supplementary Fig. 1
(DOCX 17 kb)
Supplementary Table 1
(DOCX 23 kb)
Rights and permissions
About this article
Cite this article
Qin, H., Xing, X., Tang, Y. et al. Linking soil N2O emissions with soil microbial community abundance and structure related to nitrogen cycle in two acid forest soils. Plant Soil 435, 95–109 (2019). https://doi.org/10.1007/s11104-018-3863-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-018-3863-7