Effects of simulated nitrogen deposition on soil microbial biomass and community function in subtropical evergreen broad-leaved forest

Jingjing Wang, Jun Cui, Zhen Teng, Wei Fan, Mengran Guan, Xiaoya Zhao, Xiaoniu Xu

Abstract


Aim of the study: The aim of this study was to examine the effects of a 5-year simulated nitrogen (N) deposition on soil microbial biomass carbon (MBC), nitrogen (MBN), microbial community activity and diversity in subtropical old-growth forest ecosystems.

Area of study: The study was conducted in forest located at subtropical forest in Anhui, east China.

Material and methods: Three blocks with three fully randomized plots of 20 m × 20 m with similar forest community and soil conditions were established. The site applied ammonium nitrate (NH4NO3) to simulate N deposition (50 and 100 kg N ha−1 year −1). From three depths (0–10, 10–20 and 20–30 cm), were collected over four seasons (December, March, June and September), and then measured by community-level physiological profiles (CLPPs).

Main results: N addition had no significant effect on MBC and MBN. The spatiotemporal variations in MBC and MBN were controlled by seasonality and soil depth. Soil microbial activities and diversity in the growing season (June and September) were apparently higher than the dormant season (March and December), there were significantly lower diversity indices found following N addition in September. However, N addition enhanced microbial activities and increased diversity indices in the dormant season. Redundancy analysis showed that pH, soil moisture, NO3--N and total phosphorus were the most important factors controlling the spatial pattern of microbial metabolic activity.

Research highlights: These results suggest that soil microbial community function is more easily influenced than microbial biomass. The site has a trend of P-limited or near-N saturation, and will threaten the whole forest ecosystem with the increasing duration of N addition.

Keywords: Nitrogen deposition; Seasonality; Soil microbial biomass; Microbial community; Subtropical old-growth forest.

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References


Allison SD, Czimczik CI,Treseder KK, 2010. Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest. Glob Change Biol 14 (5): 1156-1168. https://doi.org/10.1111/j.1365-2486.2008.01549.x

Balser TC, Galloway J, Cowling E, Erisman JW, Wisniewski J, Jordan C, 2001. The impact of long-term nitrogen addition on microbial community composition in three Hawaiian forest soils. SCI World J. 1: 500. https://doi.org/10.1100/tsw.2001.450

Banning NC, Lalor BM, Cookson WR, Grigg AH, Murphy DV, 2012. Analysis of soil microbial community level physiological profiles in native and post-mining rehabilitation forest: Which substrates discriminate? Appl Soil Ecol 56 (1): 27-34. https://doi.org/10.1016/j.apsoil.2012.01.009

Bérarda A, Sévenier G, Pablo AL,Gros R, 2011. Resilience of soil microbial communities impacted by severe drought and high temperature in the context of Mediterranean heat waves. Eur J Soil Biol 47 (6): 333-342. https://doi.org/10.1016/j.ejsobi.2011.08.004

Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, 2010. Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl. 20 (1): 30-59. https://doi.org/10.1890/08-1140.1

Brackin R, Robinson N, Lakshmanan P, Schmidt S, 2013. Microbial function in adjacent subtropical forest and agricultural soil. Soil Biol Biochem 57 (3): 68-77. https://doi.org/10.1016/j.soilbio.2012.07.015

Brockett, Beth FT, Prescott CE,Grayston SJ, 2012. Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada. Soil Biol Biochem 44 (1): 9-20. https://doi.org/10.1016/j.soilbio.2011.09.003

Campbell CD, Chapman SJ, Cameron CM, Davidson MS, Potts JM, 2003. A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl Environ Microbiol. 69 (6): 3593. https://doi.org/10.1128/AEM.69.6.3593-3599.2003

Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E, 2013. The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob Chang Biol 19 (4): 988-995. https://doi.org/10.1111/gcb.12113

Cui J, Wang JJ, Xu J, Xu CH, Xu XN, 2017. Changes in soil bacterial communities in an evergreen broad-leaved forest in east China following 4 years of nitrogen addition. J Soil Sediment. 17 (8): 2156-2164. https://doi.org/10.1007/s11368-017-1671-y

Di T, Peng L, Fang W, Xu J, Luo Y, Yan Z, Zhu B, Wang J, Xu X, Fang J, 2017. Growth responses of trees and understory plants to nitrogen fertilization in a subtropical forest in China. Biogeosciences 14 (14): 1-19. https://doi.org/10.5194/bg-14-3461-2017

Du EZ, Zhou Z, Li P, Hu XY, Ma YC, Wang W, Zheng CY, Zhu JX, He JS, Fang JY, 2013. NEECF: a project of nutrient enrichment experiments in China's forests. J Plant Ecol 6 (5): 428-435. https://doi.org/10.1093/jpe/rtt008

Eisenhauer N, Cesarz S, Koller R, Worm K, Reich PB, 2012. Global change belowground: Impacts of elevated CO2, nitrogen, and summer drought on soil food webs and biodiversity. Glob Change Biol 18 (2): 435-447. https://doi.org/10.1111/j.1365-2486.2011.02555.x

Feng W, Zou X, Schaefer D, 2009. Above- and belowground carbon inputs affect seasonal variations of soil microbial biomass in a subtropical monsoon forest of southwest China. Soil Biol Biochem 41 (5): 978-983. https://doi.org/10.1016/j.soilbio.2008.10.002

Frey SD, Ollinger S, Nadelhoffer K, Bowden R, Brzostek E, Burton A, Caldwell BA, Crow S, Goodale CL, Grandy AS, 2014. Chronic nitrogen additions suppress decomposition and sequester soil carbon in temperate forests. Biogeochemistry 121 (2): 305-316. https://doi.org/10.1007/s10533-014-0004-0

Garcia-Pausas J, Paterson E, 2011. Microbial community abundance and structure are determinants of soil organic matter mineralisation in the presence of labile carbon. Soil Biol Biochem 43 (8): 1705-1713. https://doi.org/10.1016/j.soilbio.2011.04.016

Garland JL, 1997. Analysis and interpretation of community-level physiological profiles in microbial ecology. FEMS Microbiol. Ecol. 24 (4): 289-300. https://doi.org/10.1016/S0168-6496(97)00061-5

Garland JL, Mills AL, 1991. Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57 (8): 2351-2359.

Gomez E, Ferreras L,Toresani S, 2006. Soil bacterial functional diversity as influenced by organic amendment application. Bioresour. Technol. 97 (13): 1484-1489. https://doi.org/10.1016/j.biortech.2005.06.021

Heijden MGA, Van Der, Bardgett RD, Straalen NM, Van, 2010. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol. Lett. 11 (3): 296-310. https://doi.org/10.1111/j.1461-0248.2007.01139.x

Högberg MN, Högberg P, Myrold DD, 2007. Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three? Oecologia 150 (4): 590-601. https://doi.org/10.1007/s00442-006-0562-5

Johannes R, Brookes PC, Erland BT, 2009. Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl Environ Microbiol. 75 (6): 1589-96. https://doi.org/10.1128/AEM.02775-08

Jing X, Chen X, Tang M, Ding Z, Jiang L, Li P, Ma S, Tian D, Xu L, Zhu J, Ji C, Shen H, Fang J, Zhu B, 2017. Nitrogen deposition has minor effect on soil extracellular enzyme activities in six Chinese forests. Sci Total Environ. 607-608:806-815. https://doi.org/10.1016/j.scitotenv.2017.07.060

Kaschuk G, Alberton O, Hungria M, 2010. Three decades of soil microbial biomass studies in Brazilian ecosystems: Lessons learned about soil quality and indications for improving sustainability. Soil Biol Biochem 42 (1): 1-13. https://doi.org/10.1016/j.soilbio.2009.08.020

Keeler BL, Hobbie SE, Kellogg LE, 2009. Effects of long-term nitrogen addition on microbial enzyme activity in eight forested and grassland sites: Implications for litter and soil organic matter decomposition. Ecosystems 12 (1): 1-15. https://doi.org/10.1007/s10021-008-9199-z

Kumar U, Shahid M, Tripathi R, Mohanty S, Nayak AK, 2016. Variation of functional diversity of soil microbial community insub-humid tropical rice-rice cropping system under long-termorganic and inorganic fertilization. Ecol Indic 1 (73): 536-543. https://doi.org/10.1016/j.ecolind.2016.10.014

Lal R, 2005. Forest soils and carbon sequestration. For Ecol Manage 220 (1): 242-258. https://doi.org/10.1016/j.foreco.2005.08.015

Leff JW, Jones SE, Prober SM, Albert B, Borer ET, Firn JL, W Stanley H, Hobbie SE, Hofmockel KS, Knops JMH, 2015. Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc Natl Acad Sci U S A 112 (35): 10967. https://doi.org/10.1073/pnas.1508382112

Lipson DA, Schmidt SK, Monson RK, 2000. Carbon availability and temperature control the post-snowmelt decline in alpine soil microbial biomass. Soil Biol Biochem 32 (4): 441-448. https://doi.org/10.1016/S0038-0717(99)00068-1

Mo J, Zhang W, Zhu W, Gundersen P, Fang Y, Li D, Wang H, 2010. Nitrogen addition reduces soil respiration in a mature tropical forest in southern China. Glob Change Biol 14 (2): 403-412. https://doi.org/10.1111/j.1365-2486.2007.01503.x

Nair A, Ngouajio M, 2012. Soil microbial biomass, functional microbial diversity, and nematode community structure as affected by cover crops and compost in an organic vegetable production system. Appl Soil Ecol 58 (58): 45-55. https://doi.org/10.1016/j.apsoil.2012.03.008

Nieder R, Harden T, Martens R, Benbi DK, 2010. Microbial biomass in arable soils of Germany during the growth period of annual crops. J Soil Sci Plant Nut 171 (6): 878-885. https://doi.org/10.1002/jpln.200700024

Oksanen J, Blanchet FG, Kindt R, Legendre P, Wagner H, 2012. Vegan: Community Ecology Package. R Package version 2.0-4.

Priha O, Grayston SJ, Hiukka R, Pennanen T, Smolander A, 2001. Microbial community structure and characteristics of the organic matter in soils under Pinus sylvestris, Picea abies and Betula pendula at two forest sites. Biology & Fertility of Soils 33 (1): 17-24. https://doi.org/10.1007/s003740000281

Schimel JP, Bennett J, 2004. Nitrogen mineralization: challenges of a changing paradigm. Ecology 85 (3): 591-602. https://doi.org/10.1890/03-8002

Sradnick A, Murugan R, Oltmanns M, Raupp J, Joergensen RG, 2013. Changes in functional diversity of the soil microbial community in a heterogeneous sandy soil after long-term fertilization with cattle manure and mineral fertilizer. Appl Soil Ecol 63 (63): 23-28. https://doi.org/10.1016/j.apsoil.2012.09.011

Stevens CJ, David TI, Storkey J, 2018. Atmospheric nitrogen deposition in terrestrial ecosystems: Its impact on plant communities and consequences across trophic levels. Funct Ecol. 32: 1757-1769. https://doi.org/10.1111/1365-2435.13063

Treseder KK, 2010. Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett. 11 (10): 1111-1120. https://doi.org/10.1111/j.1461-0248.2008.01230.x

Van Diepen LTA, Lilleskov EA, Pregitzer KS, Miller RM, 2010. Simulated nitrogen deposition causes a decline of intra- and extraradical abundance of arbuscular mycorrhizal fungi and changes in microbial community structure in northern hardwood forests. Ecosystems 13 (5): 683-695. https://doi.org/10.1007/s10021-010-9347-0

Vance ED, Brookes PC, Jenkinson DS, 1987. An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19 (6): 703-707. https://doi.org/10.1016/0038-0717(87)90052-6

Wardle DA, 1998. Controls of temporal variability of the soil microbial biomass: A global-scale synthesis. Soil Biol Biochem 30 (13): 1627-1637. https://doi.org/10.1016/S0038-0717(97)00201-0

Wardle DA, Bardgett RD, Klironomos JN, Heikki SL, Putten WH, Van Der,Wall DH, 2004. Ecological linkages between aboveground and belowground biota. Science 304 (5677): 1629-1633. https://doi.org/10.1126/science.1094875

Xia JY, Wan SQ, 2008. Global response patterns of terrestrial plant species to nitrogen addition. New Phytol 179 (2): 428-439. https://doi.org/10.1111/j.1469-8137.2008.02488.x

Xia X, Zheng S, Li D, Rey A, Ruan H, Craine JM, Liang J, Zhou J, Luo Y, 2016. Soil properties control decomposition of soil organic carbon: Results from data-assimilation analysis. Geoderma 262: 235-242. https://doi.org/10.1016/j.geoderma.2015.08.038

Zechmeister-Boltenstern S, Michel K, Pfeffer M, 2011. Soil microbial community structure in European forests in relation to forest type and atmospheric nitrogen deposition. Plant Soil 343 (1-2): 37-50. https://doi.org/10.1007/s11104-010-0528-6

Zhang N, Wan S, Guo J, Han G, Gutknecht J, Schmid B, Yu L, Liu W, Bi J,Wang Z, 2015. Precipitation modifies the effects of warming and nitrogen addition on soil microbial communities in northern Chinese grasslands. Soil Biol Biochem 89 (6): 12-23. https://doi.org/10.1016/j.soilbio.2015.06.022

Zhang TA, Chen HYH, Ruan H, 2018. Global negative effects of nitrogen deposition on soil microbes. ISME J 12 (7): 1817-1825. https://doi.org/10.1038/s41396-018-0096-y

Zhang Y, Shen H, He X, Thomas BW, Lupwayi NZ, Hao X, Thomas MC, Shi X, 2017. Fertilization Shapes Bacterial Community Structure by Alteration of Soil pH. Front Microbiol 8: 1325. https://doi.org/10.3389/fmicb.2017.01325

Zhao HF, Yao XJ, Wang Q, Chen YS, Xu XN, 2013. Nitrogen deposition and soil nitrogen dynamics in subtropical evergreen broad-leaved stands along an age-sequence. J Soil Sci Plant Nut 13 (2): 237-250. https://doi.org/10.4067/S0718-95162013005000021

Zhao X, Wang Q,YoshitakaKakubari, 2011. Seasonal dynamics of soil microbial biomass C shows close correlation with environmental factors in natural Fagus crenata forests. Acta Agric Scand 61 (4): 322-332. https://doi.org/10.1080/09064710.2010.490536

Zhu LX, Xiao Q, Shen YF, Li SQ, 2017. Microbial functional diversity responses to 2 years since biochar application in silt-loam soils on the Loess Plateau. Ecotoxicol Environ Saf 144: 578-584. https://doi.org/10.1016/j.ecoenv.2017.06.075

Zhu Y, Shen R, He J, Wang Y, Han X, Jia Z, 2017. China Soil Microbiome Initiative: Progress and Perspective. BCAS 32 (6): 554-565.




DOI: 10.5424/fs/2019283-15404

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