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Journal of Integrative Agriculture  2019, Vol. 18 Issue (11): 2605-2618    DOI: 10.1016/S2095-3119(19)62759-0
Agro-ecosystem & Environment Advanced Online Publication | Current Issue | Archive | Adv Search |
Soil macroaggregates and organic-matter content regulate microbial communities and enzymatic activity in a Chinese Mollisol
CHEN Xu1, HAN Xiao-zeng1, YOU Meng-yang1, YAN Jun1, LU Xin-chun1, William R. Horwath1, 2, ZOU Wen-xiu1  
1 Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Harbin 150081, P.R.China
2 Biogeochemistry and Nutrient Cycling Laboratory, Department of Land, Air and Water Resources, University of California Davis, CA 95616, USA
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Abstract  
The formation and turnover of macroaggregates are critical processes influencing the dynamics and stabilization of soil organic carbon (SOC).  Soil aggregate size distribution is directly related to the makeup and activity of microbial communities.  We incubated soils managed for >30 years as restored grassland (GL), farmland (FL) and bare fallow (BF) for 60 days using both intact and reduced aggregate size distributions (intact aggregate distribution (IAD)<6 mm; reduced aggregate distribution (RAD)<1 mm), in treatments with added glucose, alanine or inorganic N, to reveal activity and microbial community structure as a function of aggregate size and makeup.  Over a 60-day incubation period, the highest phospholipid fatty acid (PLFA) abundance was on day 7 for bacteria and fungi, on day 15 for actinomycete.  The majority of the variation in enzymatic activities was likely related to PLFA abundance.  GL had higher microbial abundance and enzyme activity.  Mechanically reducing macroaggregates (>0.25 mm) by 34.7% in GL soil with no substrate additions increased the abundance of PLFAs (average increase of 15.7%) and activities of β-glucosidase (increase of 17.4%) and N-acetyl-β-glucosaminidase (increase of 7.6%).  The addition of C substrates increased PLFA abundance in FL and BF by averages of 18.8 and 33.4%, respectively, but not in GL soil.  The results show that the effect of habitat destruction on microorganisms depends on the soil aggregates, due to a release of bioavailable C, and the addition of substrates for soils with limited nutrient availability.  The protection of SOC is promoted by larger size soil aggregate structures that are important to different aggregate size classes in affecting soil C stabilization and microbial community structure and activity. 
Keywords:  soil macroaggregates        soil organic carbon        PLFAs        enzyme activity       microbial community        Mollisol
 
  
Received: 12 March 2019   Accepted:
Fund: 
This study was funded by the National Key Research and Development Program of China (2016YFD0300806-1,
2016YFD0200309-6 and 2017YFD0300605-3), the National Natural Science Foundation of China (41771327 and 41571219), and the Young Scientists’ Group of North Institute of Geography and Agroecology, Chinese Academy of Sciences (DLSXZ1605).
Corresponding Authors:  Correspondence ZOU Wen-xiu, Tel: +86-451-86601048, Fax: +86-451-86603736, E-mail: zouwenxiu@iga.ac.cn   
About author:  CHEN Xu, E-mail: chen1280@163.com;

Cite this article: 

CHEN Xu, HAN Xiao-zeng, YOU Meng-yang, YAN Jun, LU Xin-chun, William R. Horwath, ZOU Wen-xiu . 2019. Soil macroaggregates and organic-matter content regulate microbial communities and enzymatic activity in a Chinese Mollisol. Journal of Integrative Agriculture, 18(11): 2605-2618.

Ai C, Liang G, Sun J, Wang X, Zhou W. 2012. Responses of extracellular enzyme activities and microbial community in both the rhizosphere and bulk soil to long-term fertilization practices in a fluvo-aquic soil. Geoderma, 173, 330–338.
Allison S D, Jastrow J D. 2006. Activities of extracellular enzymes in physically isolated fractions of restored grassland soils. Soil Biology & Biochemistry, 38, 3245–5326.
Allison V J, Condron L M, Peltzer D A, Richardson S J, Turner B L. 2007. Changes in enzyme activities and soil microbial community composition along carbon and nutrient gradients at the franz josef chronosequence, New Zealand. Soil Biology & Biochemistry, 39, 1770–1781.
Anderson M J. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26, 32–46.
Balota E L, Machineski O, Hamid K I A, Yada I F U, Barbosa G M C, Nakatani A S, Coyne M S. 2014. Soil microbial properties after long-term swine slurry application to conventional and no-tillage systems in brazil. Science of the Total Environment, 490, 397–404.
Bimueller C, Kreyling O, Koelbl A, von Luetzow M, Koegel-Knabner I. 2016. Carbon and nitrogen mineralization in hierarchically structured aggregates of different size. Soil & Tillage Research, 160, 23–33.
Blagodatskaya E, Kuzyakov Y. 2008. Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: Critical review. Biology & Fertility of Soils, 45, 115–131.
Blagodatskaya E V, Blagodatsky S A, Anderson T H, Kuzyakov Y. 2007. Priming effects in chernozem induced by glucose and N in relation to microbial growth strategies. Applied Soil Ecology, 37, 95–105.
Bossio D A, Scow K M, Gunapala N, Graham K J. 1998. Determinants of soil microbial communities: effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microbial Ecology, 36, 1–12.
Bremer E, Vankessel C. 1992. Seasonal microbial biomass dynamics after addition of lentil and wheat residues. Soil Science Society of America Journal, 56, 1141–1146.
Bremner J M, Mulvaney C S. 1982. Nitrogen total. In: Page A L, Miller R H, Keeney D R, eds., Methods of Soil Analysis, Part 2: Chemical and Microbiological Properties. American Society of Agronomy and Soil Science Society of America, Madison, WI. pp. 885–891.
Bronick C J, Lal R. 2005. Soil structure and management: A review. Geoderma, 124, 3–22.
Cambardella C A, Elliott E T. 1994. Carbon and nitrogen dynamics of soil organic-matter fractions from cultivated grassland soils. Soil Science Society of America Journal, 58, 123–130.
Chen X, Li Z, Liu M, Jiang C, Che Y. 2015. Microbial community and functional diversity associated with different aggregate fractions of a paddy soil fertilized with organic manure and/or NPK fertilizer for 20 years. Journal of Soils and Sediments, 15, 292–301.
Chenu C, Hassink J, Bloem J. 2001. Short-term changes in the spatial distribution of microorganisms in soil aggregates as affected by glucose addition. Biology & Fertility of Soils, 34, 349–356.
Cheshire M V, Bedrock C N, Williams B L, Chapman S J, Solntseva I, Thomsen I. 1999. The immobilization of nitrogen by straw decomposing in soil. European Journal of Soil Science, 50, 329–341.
Deforest J L. 2009. The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and L-DOPA. Soil Biology & Biochemistry, 41, 1180–1186.
Ding X, Han X. 2014. Effects of long-term fertilization on contents and distribution of microbial residues within aggregate structures of a clay soil. Soil Biology & Biochemistry, 50, 549–554.
Ding X, Liang C, Zhang B, Yuan Y, Han X. 2015. Higher rates of manure application lead to greater accumulation of both fungal and bacterial residues in macroaggregates of a clay soil. Soil Biology & Biochemistry, 84, 137–146.
Djukic I, Zehetner F, Mentler A, Gerzabek M H. 2010. Microbial community composition and activity in different alpine vegetation zones. Soil Biology & Biochemistry, 42, 155–161.
Dorodnikov M, Blagodatskaya E, Blagodatsky S, Marhan S, Fangmeier A, Kuzyakov Y. 2009. Stimulation of microbial extracellular enzyme activities by elevated CO2 depends on soil aggregate size. Global Change Biology, 15, 1603–1614.
Drury C F, Yang X M, Reynolds W D, Tan C S. 2004. Influence of crop rotation and aggregate size on carbon dioxide production and denitritication. Soil & Tillage Research, 79, 87–100.
Dungait J A J, Hopkins D W, Gregory A S, Whitmore A P. 2012. Soil organic matter turnover is governed by accessibility not recalcitrance. Global Change Biology, 18, 1781–1796.
Elliott E T. 1986. Aggregate structure and carbon, nitrogen, and phosphorus in native and cultivated soils. Soil Science Society of America Journal, 50, 627–633.
Fierer N, Schimel J P, Holden P A. 2003. Variations in microbial community composition through two soil depth profiles. Soil Biology & Biochemistry, 35, 167–176.
Fontaine S, Mariotti A, Abbadie L. 2003. The priming effect of organic matter: A question of microbial competition? Soil Biology & Biochemistry, 35, 837–843.
Frostegard A, Baath E. 1996. The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biology & Fertility of Soils, 22, 59–65.
Garcia-Franco N, Martinez-Mena M, Goberna M, Albaladejo J. 2015. Changes in soil aggregation and microbial community structure control carbon sequestration after afforestation of semiarid shrublands. Soil Biology & Biochemistry, 87, 110–121.
Geisseler D, Scow K M. 2014. Long-term effects of mineral fertilizers on soil microorganisms - a review. Soil Biology & Biochemistry, 75, 54–63.
Gregorich E G, Kachanoski R G, Voroney R P. 1989. Carbon mineralization in soil size fractions after various amounts of aggregate disruption. Journal of Soil Science, 40, 649–659.
Guggenberger G, Frey S D, Six J, Paustian K, Elliott E T. 1999. Bacterial and fungal cell-wall residues in conventional and no-tillage agroecosystems. Soil Science Society of America Journal, 63, 1188–1198.
Hassett J E, Zak D R. 2005. Aspen harvest intensity decreases microbial biomass, extracellular enzyme activity, and soil nitrogen cycling. Soil Science Society of America Journal, 69, 227–235.
Helgason B L, Walley F L, Germida J J. 2010. No-till soil management increases microbial biomass and alters community profiles in soil aggregates. Applied Soil Ecology, 46, 390–397.
Inglett K S, Inglett P W, Reddy K R. 2011. Soil microbial community composition in a restored calcareous subtropical wetland. Soil Science Society of America Journal, 75, 1731–1740.
Jackson M L. 1973. Soil Chemical Analysis. Prentice Hall of India Pvt, New Delhi.
Kleber M, Johnson M G. 2010. Advances in understanding the molecular structure of soil organic matter: Implications for interactions in the environment. Advances in Agronomy, 77–142.
Landi L, Valori F, Ascher J, Renella G, Falchini L, Nannipieri P. 2006. Root exudate effects on the bacterial communities, CO2 evolution, nitrogen transformations and ATP content of rhizosphere and bulk soils. Soil Biology & Biochemistry, 38, 509–516.
Li N, Yao S, Qiao Y, Zou W, You M, Han X, Zhang B. 2015. Separation of soil microbial community structure by aggregate size to a large extent under agricultural practices during early pedogenesis of a mollisol. Applied Soil Ecology, 88, 9–20.
Lynch J M, Bragg E. 1985. Microorganisms and soil aggregate stability. Advances in Soil Science, 2, 134–170.
Moreno-Cornejo J, Zornoza R, Doane T A, Faz A, Horwath W R. 2015. Influence of cropping system management and crop residue addition on soil carbon turnover through the microbial biomass. Biology & Fertility of Soils, 51, 839–845.
Munkholm L J, Kay B D. 2002. Effect of water regime on aggregate-tensile strength, rupture energy, and friability. Soil Science Society of America Journal, 66, 702–709.
Nannipieri P, Kandeler E, Ruggiero P. 2002. Enzyme activities and microbiological and biochemical processes in soils. In: Burns R G, Dick R P, eds., Enzymes in the Environment. Activity, Ecology and Applications. Marcel Dekker, New York. pp 1–33.
Olander L P, Vitousek P M. 2005. Short-term controls over inorganic phosphorus during soil and ecosystem development. Soil Biology & Biochemistry, 37, 651–659.
Olsen S R, Cole C V, Watanabe F S, Dean L A. 1954. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. In: USDA Circular No. 939. USA Goverment Print Office, Washington D.C., USA. pp. 1–19.
Qin S, Hu C, He X, Dong W, Cui J, Wang Y. 2010. Soil organic carbon, nutrients and relevant enzyme activities in particle-size fractions under conservational versus traditional agricultural management. Applied Soil Ecology, 45, 152–159.
R Core Team. 2016. R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Saiya-Cork K R, Sinsabaugh R L, Zak D R. 2002. The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biology & Biochemistry, 34, 1309–1315.
Schnecker J, Wild B, Hofhansl F, Alves R J E, Barta J, Capek P, Fuchslueger L, Gentsch N, Gittel A, Guggenberger G, Hofer A, Kienzl S, Knoltsch A, Lashchinskiy N, Mikutta R, Santruckova H, Shibistova O, Takriti M, Urich T, Weltin G, et?al. 2014. Effects of soil organic matter properties and microbial community composition on enzyme activities in cryoturbated arctic soils. PLoS ONE, 9, e94076.
Sinsabaugh R L, Antibus R K, Linkins A E, Mcclaugherty C A, Rayburn L, Repert D, Weiland T. 1993. Wood decomposition: Nitrogen and phosphorus dynamics in relation to extracellular enzyme-activity. Ecology, 74, 1586–1593.
Six J, Bossuyt H, Degryze S, Denef K. 2004. A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics. Soil & Tillage Research, 79, 7–31.
Six J, Elliott E T, Paustian K. 1999. Aggregate and soil organic matter dynamics under conventional and no-tillage systems. Soil Science Society of America Journal, 63, 1350–1358.
Six J, Frey S D, Thiet R K, Batten K M. 2006. Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Science Society of America Journal, 70, 555–569.
Smith A P, Marin-Spiotta E, de Graaff M A, Balser T C. 2014. Microbial community structure varies across soil organic matter aggregate pools during tropical land cover change. Soil Biology & Biochemistry, 77, 292–303.
Song C, Han X Z, Tang C X. 2007. Changes in phosphorus fractions, sorption and release in Udic Mollisols under different ecosystems. Biology and Fertility of Soils, 44, 37?47.
Strickland M S, Rousk J. 2010. Considering fungal:bacterial dominance in soils - Methods, controls, and ecosystem implications. Soil Biology & Biochemistry, 42, 1385–1395.
Tian J, Pausch J, Yu G, Blagodatskaya E, Gao Y, Kuzyakov Y. 2015. Aggregate size and their disruption affect 14C-labeled glucose mineralization and priming effect. Applied Soil Ecology, 90, 1–10.
Tian J, Pausch J, Yu G, Blagodatskaya E, Kuzyakov Y. 2016. Aggregate size and glucose level affect priming sources: A three-source-partitioning study. Soil Biology & Biochemistry, 97, 199–210.
Tisdall J M. 1991. Fungal hyphae and structural stability of soil. Australian Journal of Soil Research, 29, 729–743.
Tisdall J M, Oades J M. 2012. Landmark papers: No. 1. Organic matter and water-stable aggregates in soils. European Journal of Soil Science, 63, 8–21.
van der Wal A, de Boer W. 2017. Dinner in the dark: Illuminating drivers of soil organic matter decomposition. Soil Biology & Biochemistry, 105, 45–48.
White N A, Hallett P D, Feeney D, Palfreyman J W, Ritz K. 2000. Changes to water repellence of soil caused by the growth of white-rot fungi: Studies using a novel microcosm system. FEMS Microbiology Letters, 184, 73–77.
Wittmann C, Kahkonen M A, Ilvesniemi H, Kurola J, Salkinoja-Salonen M S. 2004. Areal activities and stratification of hydrolytic enzymes involved in the biochemical cycles of carbon, nitrogen, sulphur and phosphorus in podsolized boreal forest soils. Soil Biology & Biochemistry, 36, 425–433.
Zelles L. 1997. Phospholipid fatty acid profiles in selected members of soil microbial communities. Chemosphere, 35, 275–294.
Zhang H, Ding W, Yu H, He X. 2013. Carbon uptake by a microbial community during 30-day treatment with 13C-glucose of a sandy loam soil fertilized for 20 years with NPK or compost as determined by a GC-C-IRMS analysis of phospholipid fatty acids. Soil Biology & Biochemistry, 57, 228–236.
Zhang Q H, Zak J C. 1998. Effects of water and nitrogen amendment on soil microbial biomass and fine root production in a semi-arid environment in west texas. Soil Biology & Biochemistry, 30, 39–45.
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