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Microbial community and associated enzymes activity influence soil carbon chemical composition in Eucalyptus urophylla plantation with mixing N2-fixing species in subtropical China

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Abstract

Background and aims

Microbial communities and their associated enzyme activities affect the quantity and chemical quality of carbon in soil. We aimed to evaluate the biochemical mechanisms underlying how N2-fixing species influences soil organic carbon chemical composition through soil microbial functional groups and enzyme activities.

Methods

We examined the effects of N2-fixing species mixed with Eucalyptus on soil carbon storage, and the chemical composition of an 8-year-old pure Eucalyptus urophylla plantation (PP) and a mixed E.urophylla and Acacia mangium plantation (MP).

Results

The soil carbon stock and recalcitrant carbon chemical component significantly increased in surface soil in MP. The total PLFAs and bacterial PLFAs increased by 29.1% and 27.0% in cool-dry season, while in the warm-wet season, the total PLFAs and bacterial PLFAs increased by 13.1% and 27.3%, respectively. However, the fungal PLFAs decreased significantly in warm-wet season in MP. The total activity of the cellulose-degrading enzyme β-glucosidase was significantly greater with mixed N2-fixing species in both dry-cool and wet-warm season. The increase in the Alk-C/O-Alk-C ratio and SOC was strongly associated with both C-acquisition activity and bacterial community.

Conclusions

Our findings highlight the importance of N2-fixing species in regulating both soil microbial communities and their functioning in association with soil extracellular enzyme activities, which contribute to the increased soil carbon storage and recalcitrant carbon composition in Eucalyptus plantations.

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References

  • Acea MJ, Carballas T (1996) Microbial response to organic amendments in a forest soil. Bioresour Technol 57:193–199

    Article  CAS  Google Scholar 

  • Araújo ASF, Silva EFL, Nunes LAPL, Carneiro RFV (2010) The effect of converting tropical native savanna to Eucalyptus grandis forest on soil microbial biomass. Land Degrad Dev 21(6):540–545

    Article  Google Scholar 

  • Araújo ASF, Cesarz S, Leite LFC, Borges CD, Tsai SM, Eisenhauer N (2013) Soil microbial properties and temporal stability in degraded and restored lands of Northeast Brazil. Soil Biol Biochem 66:175–181

    Article  Google Scholar 

  • Arbuckle JL (2006) Amos (version 7.0) [computer program]. SPSS, Chicago

    Google Scholar 

  • Baldock JA, Preston CM (1995) Chemistry of carbon decomposition processes in forests as revealed by solid-state carbon-13 nuclear magnetic resonance. Carbon Forms Funct For Soils:89–117

  • Baldock JA, Oades JM, Nelson PN, Skene TM, Golchin A, Clarke P (1997) Assessing the extent of decomposition of natural organic materials using solid-state 13C NMR spectroscopy. Aust J Soil Res 35:1061–1083

    Article  Google Scholar 

  • Baldrian P (2009) Microbial enzyme-catalyzed processes in soils and their analysis. Plant Soil Environ 55:370–378

    CAS  Google Scholar 

  • Baldrian P, Šnajdr J, Merhautová V, Dobiášová P, Cajthaml T, Valášková V (2013) Responses of the extracellular enzyme activities in hardwood forest to soil temperature and seasonality and the potential effects of climate change. Soil Biol Biochem 56:60–68

    Article  CAS  Google Scholar 

  • Bardgett RD, McAlister E (1999) The measurement of soil fungal: bacterial biomass ratios as an indicator of ecosystem self-regulation in temperate meadow grasslands. Biol Fertil Soils 29:282–290

    Article  Google Scholar 

  • Beare MH, Neely CL, Coleman DC, Hargrove WL (1990) A substrate-induced respiration (SIR) method for measurement of fungal and bacterial biomass on plant residues. Soil Biol Biochem 22:585–594

    Article  Google Scholar 

  • Billings SA, Ziegler SE (2008) Altered patterns of soil carbon substrate usage and heterotrophic respiration in a pine forest with elevated CO2 and N-fertilization. Glob Chang Biol 14:1025–1036

    Article  Google Scholar 

  • Billings SA, Tiemann LK, Ballantyne IVF, Lehmeier CA, Min K (2015) Investigating microbial transformations of soil organic matter: synthesizing knowledge from disparate fields to guide new experimentation. Soil 1(1):313

    Article  Google Scholar 

  • Binkley D, Senock R, Bird S, Cole TG (2003) Twenty years of stand development in pure and mixed stands of Eucalyptus saligna and nitrogen-fixing Facaltaria moluccana. For Ecol Manag 182:93–102

    Article  Google Scholar 

  • Bossio DA, Scow KM (1998) Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microb Ecol 35(3–4):265–278

    Article  CAS  PubMed  Google Scholar 

  • Buyer JS, Maul JE (2016) Soil microbial communities following bush removal in a Namibian savanna. Soil 2(1):101

    Article  Google Scholar 

  • Carney KM, Hungate BA, Drake BG, Megonigal JP (2007) Altered soil microbial community at elevated CO2 leads to loss of soil carbon. P Nati Acad Sci USA 104:4990–4995

    Article  CAS  Google Scholar 

  • Chen CR, Xu ZH, Mathers NJ (2004) Soil carbon pools in adjacent natural and plantation forests of subtropical Australia. Soil Sci Soc Am J 68:282–291

    Article  CAS  Google Scholar 

  • Cox F, Barsoum N, Lilleskov EA, Bidartondo MI (2010) Nitrogen availability is a primary determinant of conifer mycorrhizas across complex environmental gradients. Ecol Lett 13:1103–1113

    Article  PubMed  Google Scholar 

  • Cusack DF, Silver WL, Torn MS, Burton SD, Firestone MK (2011) Changes in microbial community characteristics and soil organic matter with nitrogen addition in two tropical forests. Ecology 93:621–632

    Article  Google Scholar 

  • De Deyn GB, Cornelissen JHC, Bardgett RD (2008) Plant functional traits and soil carbon sequestration in contrasting biomes. Ecol Lett 11:516–531

    Article  PubMed  Google Scholar 

  • Djukic I, Zehetner F, Mentler A, Gerzabek MH (2010) Microbial community composition and activity in different alpine vegetation zones. Soil Biol Biochem 42(2):155–161

    Article  CAS  Google Scholar 

  • Fernandes SAP, Bettiol W, Cerri CC (2005) Effect of sewage sludge on microbial biomass, basal respiration, metabolic quotient and soil enzymatic activity. Appl Soil Ecol 30(1):65–77

    Article  Google Scholar 

  • Fierer N, Strickland M, Liptzin D, Bradford M, Cleveland C (2009) Global patterns in belowground communities. Ecol Lett 12:1238–1249

    Article  PubMed  Google Scholar 

  • Forrester DI, Bauhus J, Cowie AL (2005) On the success and failure of mixed-species tree plantations: lessons learned from a model system of Eucalyptus globulus and Acacia mearnsii. For Ecol Manag 209:147–155

    Article  Google Scholar 

  • Franklin RB, Mills AL (2009) Importance of spatially structured environmental heterogeneity in controlling microbial community composition at small spatial scales in an agricultural field. Soil Biol Biochem 41:1833–1840

    Article  CAS  Google Scholar 

  • Frey SD, Knorr M, Parrent JL, Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manag 196:159–171

    Article  Google Scholar 

  • Gallaher RN, Weldon CO, Boswell FC (1976) A semiautomated procedure for total nitrogen in plant and soil samples. Soil Sci Soc Am J 40:887–889

    Article  CAS  Google Scholar 

  • Golchin A, Baldock JA, Oades JM (1997) A model linking organic matter decomposition, chemistry, and aggregate dynamics. In: Soil processes and the carbon cycle. CRC Press, Boca Raton, pp. 245–266

    Google Scholar 

  • Grace JB (2006) Structural equation modeling and natural systems. New York

  • Grace JB, Michael Anderson T, Smith MD, Seabloom E, Andelman SJ, Meche G et al (2007) Does species diversity limit productivity in natural grassland communities? Ecol Lett 10(8):680–689

    Article  PubMed  Google Scholar 

  • Grayston SJ, Campbell CD, Bardgett RD, Mawdsley JL, Clegg CD, Ritz K et al (2004) Assessing shifts in microbial community structure across a range of grasslands of differing management intensity using CLPP, PLFA and community DNA techniques. Appl Soil Ecol 25:63–84

    Article  Google Scholar 

  • Hamman ST, Burk IC, Stromberger ME (2007) Relationship between microbial community structure and soil environmental conditions in a recently burned system. Soil Biol Biochem 39:1703–1711

    Article  CAS  Google Scholar 

  • Högberg M, Chen Y, Högberg P (2007) Gross nitrogen mineralisation and heterotrophic respiration in a pine forest with elevated CO2 and N-fertilization. Glob Chang Biol 14:1025–1036

    Google Scholar 

  • Huang ZQ, Xu ZH, Chen CR (2008a) Interactions among soil organic matter fractions, microbial communities and nitrogen transformations in two hardwood plantation of subtropical Australia: effect of mulch. Appl Soil Ecol 40:229–239

    Article  Google Scholar 

  • Huang XM, Liu SR, Wang H, Hu ZD, Li ZG, You YM (2014) Changes of soil microbial biomass carbon and community composition through mixing nitrogen-fixing species with Eucalyptus Urophylla in subtropical China. Soil Biol Biochem 73:42–48

    Article  CAS  Google Scholar 

  • James R, Del Lungo A (2005) The potential for fast-growing commercial forest plantations to supply high-value roundwood. Planted forests and trees working papers, working paper 33. Forest resources development service, forest resources division. FAO, Rome, Italy

  • Jangid K, Williams MA, Franzluebbers AJ, Sanderlin JS, Reeves JH, Jenkins MB et al (2008) Relative impacts of land-use, management intensity and fertilization upon soil microbial community structure in agricultural systems. Soil Biol Biochem 40:2843–2853

    Article  CAS  Google Scholar 

  • Jin HM, Sun OJ, Liu JF (2010) Changes in soil microbial biomass and community structure with addition of contrasting types of plant litter in a semiarid grassland ecosystem. J Plant Ecol 3:209–217

    Article  Google Scholar 

  • Katsalirou ES, Deng DL, Nofziger A, Gerakis A, Fuhlendorf SD (2010) Spatial structure of microbial biomass and activity in prairie soil ecosystems. Eur J Soil Biol 46:181–189

    Article  Google Scholar 

  • Kaye JP, Resh SC, Kaye MW, Chimner RA (2000) Nutrient and carbon dynamicsin a replacement series of Eucalyptus and Albizia trees. Ecology 81:3267–3273

    Article  Google Scholar 

  • Kögel-Knabner I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34(2):139–162

    Article  Google Scholar 

  • Kölbl A, Kögel-Knabner I (2004) Content and composition of free and occluded particulate organic matter in a differently textured arable Cambisol as revealed by solid-state 13C NMR spectroscopy. J Plant Nutr Soil Sci 167:45–53

    Article  Google Scholar 

  • Leifeld J, Siebert S, Kögel-Knabner I (2002) Changes in the chemical composition of soil organic matter after application of compost. Eur J Soil Sci 53:299–309

    Article  Google Scholar 

  • Li Q, Allen HL, Wilson CA, Wollum AG (2004) Microbial biomass and bacterial functional diversity in forest soils: effects of organic matter removal, compaction, and vegetation control, soil Biol. Biochemist 36:571–579

    CAS  Google Scholar 

  • Li X, Han S, Guo Z, Shao D, Xin L (2010) Changes in soil microbial biomass carbon and enzyme activities under elevated CO 2 affect fine root decomposition processes in a Mongolian oak ecosystem. Soil Biol Biochem 42(7):1101–1107

    Article  CAS  Google Scholar 

  • Lilleskov EA, Fahey TJ, Horton TR, Lovett GM (2002) Belowground ectomy corrhizal fungal community change over a nitrogen deposition gradient in Alaska. Ecology 83:104–115

    Article  Google Scholar 

  • Lino IAN, Santos VM, Escobar IEC, Silva DKA, Araújo ASF, Maia LC (2016) Soil enzymatic activity in Eucalyptus grandis plantations of different ages. Land Degrad Dev 27:77–82

    Article  Google Scholar 

  • Liu SR, Li XM, Niu LM (1998) The degradation of soil fertility in pure larch plantation in the northeastern part of China. Ecol Eng 10:75–86

    Article  Google Scholar 

  • Liu L, Gundersen P, Zhang T, Mo JM (2012) Effects of phosphorus addition on soil microbial biomass and community composition in three forest types in tropical China. Soil Biol Biochem 44:31–38

    Article  Google Scholar 

  • Lorenz K, Lal R, Preston CM, Nierop KGJ (2007) Strengthening the soil organic carbon pool by increasing contributions fromrecalcitrant aliphatic bio(macro) molecules. Geoderma 142:1–10

    Article  CAS  Google Scholar 

  • Milcu A, Thebault E, Scheu S, Eisenhauer N (2010) Plant diversity enhances the reliability of belowground processes. Soil Biol Biochem 42:2102–2110

    Article  CAS  Google Scholar 

  • Minoshima H, Jackson LE, Cavagnaro TR, Sánchez-Moreno S, Ferris H, Temple SR et al (2007) Soil food webs and carbon dynamics in response to conservation tillage in California. Soil Sci Soc Am J 71:952–963

    Article  CAS  Google Scholar 

  • Myers RT, Zak DR, White DC, Peacock A (2001) Landscape, level patterns of microbial composition and substrate use in upland forest ecosystems. Soil Sci Soc Am J 65:359–367

    Article  CAS  Google Scholar 

  • Nannipieri P, Ascher J, Ceccherini MT, Landi CL, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670

    Article  Google Scholar 

  • Nelson DW, Sommers LE (1982) Total carbon, organic carbon, and organic matter. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. American Society of Agronomy and Soil Science Society of American, Madison, pp. 101–129

    Google Scholar 

  • Nemergut DR, Townsend AR, Sattin SR, Freeman KR, Fierer N, Neff JC et al (2008) The effects of chronic nitrogen fertilization on alpine tundra soil microbial communities: implications for carbon and nitrogen cycling. Environ Microbiol 10:3093–3105

    Article  CAS  PubMed  Google Scholar 

  • Ostertag R, Marín-Spiotta E, Silver WL, Schulten J (2008) Litterfall and decomposition in relation to soil carbon pools along a secondary forest chronosequence in Puerto Rico. Ecosystems 11(5):701–714

    Article  CAS  Google Scholar 

  • Parham JA, Deng SP (2000) Detection, quantification and characterization of β-glucosaminidase activity in soil. Soil Biol Biochem 32(8):1183–1190

    Article  CAS  Google Scholar 

  • Quideau SA, Chadwick OA, Benesi A, Grahama RC, Anderson MA (2001) A direct link between forest vegetation type and soil organic matter composition. Geoderma 104:41–60

    Article  CAS  Google Scholar 

  • Resh SC, Binkley D, Parrotta JA (2002) Greater soil carbon sequestration under nitrogen-fixing trees compared with Eucalyptus species. Ecosystems 5:217–231

    Article  CAS  Google Scholar 

  • Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA et al (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56

    Article  CAS  PubMed  Google Scholar 

  • Sicardi M, García-Pérchac F, Frioni L (2004) Soil microbial indicators sensitive to land use conversion from pastures to commercial Eucalyptus grandis (hill ex maiden) plantations in Uruguay. Appl Soil Ecol 27(2):125–133

    Article  Google Scholar 

  • Sinsabaugh RL, Antibus RK, Linkins AE, McClaugherty CA, Rayburn L, Repert D, Weiland T (1993) Wood decomposition: nitrogen and phosphorus dynamics in relation to extracellular enzyme activity. Ecology 74(5):1586–1593

    Article  CAS  Google Scholar 

  • Six J, Connant RT, Paul EA, Paustian K (2002) Stabilization mechanisms of soil organic matter: implications for C-saturation of soils. Plant Soil 241:155–176

    Article  CAS  Google Scholar 

  • Skjemstad JO, Clarke P, Golchin A, Oades JM (1997) Characterization of soil organic matter by solid-state 13C NMR spectroscopy. In: Cadisch G, Giller KE (eds) Driven by nature – plant litter quality and decomposition. CAB International, Oxford, pp. 253–271

    Google Scholar 

  • Soil Survey Staff of USDA (2006) Keys to soil taxonomy. United States Department of Agriculture (USDA), Natural Resources Conservation Service, Washington

    Google Scholar 

  • Spielvogel S, Prietzel J, Kögel-Knabner I (2006) Soil organic matter changes in a spruce ecosystem 25 years after disturbance. Soil Sci Soc Am J 70:2130–2145

    Article  CAS  Google Scholar 

  • Sterner RW, Elsner JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  • Stone AG, Traina SJ, Hoitink HAJ (2001) Particulate organic matter composition and Pythium damping-off of cucumber. Soil Sci Soc Am J 65(3):761–770

    Article  CAS  Google Scholar 

  • Thoms C, Gattinger A, Jacob M, Thomas FM, Gleixner G (2010) Direct and indirect effects of tree diversity drive soil microbial diversity in temperate deciduous forest. Soil Biol Biochem 42:1558–1565

    Article  CAS  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  • Von Lützow M, Kögel-Knabner I, Ekschmitt K, Matzner E, Guggenberger G, Marschner B, Flessa H (2006) Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions - a review. Eur J Soil Sci 57:426–445

    Article  Google Scholar 

  • Waldrop MP, Firestone MK (2004) Altered utilization patterns of young and old soil carbon by microorganisms caused by temperature shifts and nitrogen additions. Biogeochemistry 67:235–248

    Article  CAS  Google Scholar 

  • Wang H, Liu SR, Mo JM, Wang JX, Makeschin F, Wolff M (2010a) Soil organic carbon stock and chemical composition in four plantation of indigenous tree species in subtropical China. Ecol Res 25:1071–1079

    Article  CAS  Google Scholar 

  • Wang H, Liu SR, Mo JM, Zhang T (2010b) Soil-atmosphere exchange of green-house gases in subtropical plantations of indigenous tree species. Plant Soil 335:213–227

    Article  CAS  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setälä H, Van Der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304(5677):1629–1633

    Article  CAS  PubMed  Google Scholar 

  • You YM, Wang J, Huang XM, Tang ZX, Liu SR, Sun OJ (2014) Relating microbial community structure to functioning in forest soil organic carbon transformation and turnover. Ecol Evol 4:633–647

    Article  PubMed  PubMed Central  Google Scholar 

  • Zelles L (1999) Fatty acid patterns of phospholipids and liposaccharides in the characterisation of microbial communities in soil: a review. Biol Fertil Soils 29:111–129

    Article  CAS  Google Scholar 

  • Zhang SX, Li Q, Lü Y, Zhang XP, Liang WJ (2013) Contributions of soil biota to C sequestration varied with aggregate fractions under different tillage systems. Soil Biol Biochem 62:147–156

    Article  CAS  Google Scholar 

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Acknowledgments

We gratefully acknowledge the supports from Yi Wang, JiaXu, and Yuan Wen, for their assistance in field sampling and data collection. We also gratefully acknowledge the supports by the Experimental Center of Tropical Forestry, Chinese Academy of Forestry. This study was jointly supported by the National Natural Science Foundation of China (31290223, 31470627, and 31560201), the Ministry of Science and Technology (2015DFA31440), the Lecture and Study Program for Outstanding Scholars from Home and Abroad (CAFYBB2011007), the Ministry of Finance (201404201), and Guangxi Natural Science Foundation under Grant No. 2014GXNSFBA118100. We were also supported by the CFERN & GENE Award Funds on Ecological Paper. We are grateful to Dr. Junwei Luan and Dr. Zongda Hu for their assistance in statistical analyses and useful discussions on the manuscripts.

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Authors and Affiliations

  1. College of Forestry, Guangxi University, Nanning, 530004, China

    Xueman Huang, Yeming You & Yuanguang Wen

  2. State Forestry Administration’s Key Laboratory of Forest Ecology and Environment, Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing, 100091, China

    Xueman Huang, Shirong Liu & Hui Wang

  3. Division of Forestry and Natural Resources, West Virginia University, P.O. Box 6215, Morgantown, WV, 26506-6125, USA

    Jingxin Wang

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  1. Xueman Huang
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  2. Shirong Liu
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  3. Yeming You
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Correspondence to Shirong Liu.

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Huang, X., Liu, S., You, Y. et al. Microbial community and associated enzymes activity influence soil carbon chemical composition in Eucalyptus urophylla plantation with mixing N2-fixing species in subtropical China. Plant Soil 414, 199–212 (2017). https://doi.org/10.1007/s11104-016-3117-5

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