Abstract
The impact of agricultural land-use on soil microbial community composition and enzyme activity has not been extensively investigated in Ultisols. We investigated soil health parameters by analyzing phospholipid fatty acids (PLFAs), extracellular enzyme activity, C and N stocks, and soil structure. Four land uses were established in a tropical climate region of Brazil: native Cerrado (savanna), monoculture pasture [Urochloa brizantha (Hochst. Ex A. Rich.) R. Webster 'Marandu'], an integrated crop-livestock system (ICLS), and maize (Zea mays)-fallow in a no-tillage system. Soil microbial biomass was 40% higher in the native Cerrado than in the monoculture pasture, ICLS, and no-tillage maize. Soil organic carbon was positively correlated with microbial community composition (MB; gram–; AC; AMF; Fungi; F: B ratio) and enzyme activity (bG, AP, NAG). Large macroaggregates were positively correlated with bG, AP, and AMF. In summary, the native Cerrado had a higher level of carbon at the soil surface and greater soil structure with increased microbial biomass, gram+ bacteria, AMF, fungi, and F:B ratio in a tropical region of Brazil. However, bG and AP enzyme activities were lower in the ICLS and no-till maize at the soil surface (0–5 cm) compared to the native Cerrado. The conversion of native Cerrado to agricultural systems shifted the soil microbial community composition, enzyme activity, C and N, and soil structure of this sandy soil of the Brazilian Cerrado.
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Acosta-Martínez V, Tabatabai MA (2001) Tillage and residue management effects on arylamidase activity in soils. Biol Fertil Soils 34:21–24. https://doi.org/10.1007/s003740100349
Acosta-Martínez V, Zobeck TM, Gill TE, Kennedy AC (2003) Enzyme activities and microbial community structure in semiarid agricultural soils. Biol Fertil Soils 38:216–227. https://doi.org/10.1007/s00374-003-0626-1
Acosta-Martínez V, Mikha M, Vigil MF (2007) Microbial communities and enzyme activities in soils under alternative crop rotations compared to wheat–fallow for the Central Great Plains. Appl Soil Ecol 37:41–52. https://doi.org/10.1016/j.apsoil.2007.03.009
Acosta-Martínez V, Lascano R, Calderón F, Booker JD, Zobeck TM, Upchurch DR (2011) Dryland cropping systems influence the microbial biomass and enzyme activities in a semiarid sandy soil. Biol Fertil Soils 47:655–667. https://doi.org/10.1007/s00374-011-0565-1
Alvares CA, Stape JL, Sentelhas PC, Moraes G, Leonardo J, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorol Z 22:711–728. https://doi.org/10.1127/0941-2948/2013/0507
Anache JA, Flanagan DC, Srivastava A, Wendland EC (2018) Land use and climate change impacts on runoff and soil erosion at the hillslope scale in the Brazilian Cerrado. Sci Total Environ 622:140–151. https://doi.org/10.1016/j.scitotenv.2017.11.257
Araujo JF, Castro AP, Costa MM, Togawa RC, Júnior GJP, Quirino BF, Bustamante MMC, Lynn W, Handelsman J, Krüger RH (2012) Characterizatio of soil bacterial assemblies in Brazilian savanna-like vegetation reveals acidobacteria dominance. Microb Ecol 64:760–770. https://doi.org/10.1007/s00248-012-0057-3
Ashagrie Y, Zech W, Guggenberger G, Mamo T (2007) Soil aggregation, and total and particulate organic matter following conversion of native forests to continuous cultivation in Ethiopia. Soil Tillage Res 94:101–108. https://doi.org/10.1016/j.still.2006.07.005
Assmann JM, Anghinoni I, Martins AP, Andrade SEVG, Cecagno D, Carlos FS, Faccio Carvalho PC (2014) Soil carbon and nitrogen stocks and fractions in a long-term integrated crop-livestock system under no-tillage in southern Brazil. Agric Ecosyst Environ 190:52–59. https://doi.org/10.1016/j.agee.2013.12.003
Beheshti A, Raiesi F, Golchin A (2012) Soil properties, C fractions and their dynamics in land use conversion from native forests to croplands in northern Iran. Agric Ecosyst Environ 148:121–133. https://doi.org/10.1016/j.agee.2011.12.001
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Phys 37:911–917. https://doi.org/10.1139/o59-099
Caldwell BA (2005) Enzyme activities as a component of soil biodiversity: a review. Pedobiologia 49:637–644. https://doi.org/10.1016/j.pedobi.2005.06.003
Culman SW, Young-Mathews A, Hollander AD, Ferris H, Sánchez-Moreno S, O’Geen AT, Jackson LE (2010) Biodiversity is associated with indicators of soil ecosystem functions over a landscape gradient of agricultural intensification. Landsc Ecol 25:1333–1348. https://doi.org/10.1007/s10980-010-9511-0
Cusack DF, Silver WL, Torn MS, Burton SD, Firestone MK (2011) Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests. Ecology 92:621–632. https://doi.org/10.1890/10-0459.1
Danielson RE, Sutherland PL (1986) Porosity. In: Klute A (ed) Methods of soil analysis, physical and mineralogical methods (Part I). SSSA book series 5.1. Soil Science Society of America, Madison, pp 443–461
Eaton WD, Chassot O (2012) Characterization of soil ecosystems in Costa Rica using microbial community metrics. J Tropical Ecology 53:185–195
Eclesia RP, Jobbagy EG, Jackson RB, Biganzoli F, Piñeiro G (2012) Shifts in Soil organic carbon for plantation and pasture establishment in native forests and grasslands of South America. Glob Change Biol 18:3237–3251. https://doi.org/10.1111/j.1365-5412486.2012.02761.x
Embrapa (1997) Manual de métodos De Análises De Solo, 2nd edn. Centro Nacional de Pesquisa de Solos, Rio de Janeiro
Fabrizzi KP, Rice CW, Amado TJ, Fiorin J, Barbagelata P, Melchiori R (2009) Protection of soil organic C and N in temperate and tropical soils: effect of native and agroecosystems. Soil Biol Biochem 92:129–143. https://doi.org/10.1007/s10533-008-9261-0
Ferreira DF (2011) Sisvar: a computer statistical analysis system. Ciênc Agrotec 35:1039–1042. https://doi.org/10.1590/S1413-70542011000600001
Ferreira AO, Amado T, Rice CW, Diaz DAR, Keller C, Inagaki TM (2016) Can no–till grain production restore soil organic carbon to levels natural grass in a subtropical Oxisol? Agric Ecosyst Environ 229:13–20. https://doi.org/10.1016/j.agee.2016.05.016
Fierer N, Strickland MS, Liptzin D, Bradford MA, Cleveland CC (2009) Global patterns in belowground communities. Ecol Lett 12:1238–1249. https://doi.org/10.1111/j.1461-0248.2009.01360.x(Epub 2009 Aug 11)
Fisher MJ, Rao IM, Ayarza MA, Lascano CE, Sanz JI, Thomas RJ, Vera RR (1994) Carbon storage by introduced deep-rooted grasses in the South American savannas. Nature 371:236–238. https://doi.org/10.1038/371236a0
Gallo M, Amonette R, Lauber C, Sinsabaugh RL, Zak DR (2004) Microbial community structure and oxidative enzyme activity in nitrogen-amended north temperate forest soils. Microb Ecol 48:218–229. https://doi.org/10.1007/s00248-003-9001-x
Galloway JN, Dentener FJ, Capone DG et al (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226. https://doi.org/10.1007/s10533-004-0370-0
Garcia-Franco N, Martínez-Mena M, Goberna M, Albaladejo J (2015) Changes in soil aggregation and microbial community structure control carbon sequestration after afforestation of semiarid shrublands. Soil Biol Biochem 87:110–121. https://doi.org/10.1016/j.soilbio.2015.04.012
Green VS, Stott DE, Cruz JC, Curi N (2007) Tillage impacts on soil biological activity and aggregation in a Brazilian Cerrado Oxisol. Soil Tillage Res 92:114–121. https://doi.org/10.1016/j.still.2006.01.004
Hansel CM, Fendorf S, Jardine PM (2008) Changes in bacterial and archaeal community structure and functional diversity along a geochemically variable soil profle. Appl Environ Microbiol 74:1620–1633. https://doi.org/10.1128/AEM.01787-07
Jobbágy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423–436. https://doi.org/10.1890/1051-0761(2000)010[0423:TVDOSO]2.0.CO;2
Kandeler E, Murer E (1993) Aggregate stability and soil microbial processes in a soil with different cultivation. Geoderma 56:503–513. https://doi.org/10.1016/B978-0-444-81490-6.50040-6
Kemper WD, Chepil WS (1965) Size distribution of aggregates. In: Blake CA, Evans DD, White JL, Ensminger LE, Clark FE (eds) Methods of soil analysis: physical and mineralogical properties, including statistics of measurement and sampling. American Society of Agronomy, Madison, pp 499–510
Kihara J, Martius C, Bationo A, Thuita M, Lesueur D, Herrmann L, Amelung W, Vlek PLG (2012) Soil aggregation and total diversity of bacteria and fungi in various tillage systems of sub-humid and semi-arid Kenya. Appl Soil Ecol 58:12–20. https://doi.org/10.1016/j.apsoil.2012.03.004
Lauber CL, Strickland MS, Bradford MA (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415. https://doi.org/10.1016/j.soilbio.2008.05.021
Leifeld J, Menichetti L (2018) The underappreciated potential of peatlands in global climate change mitigation strategies. Nat Commun 9:1–7. https://doi.org/10.1038/s41467-018-03406-6
Li N, Shao T, Zhu T, Long X, Gao X, Liu Z, Shao H, Rengel Z (2018) Vegetation succession influences soil carbon sequestration in coastal alkali-saline soils in southeast China. Sci Rep 8:1–12. https://doi.org/10.1038/s41598-018-28054-0
Lisboa FJG, Chaer G, Fernandes MF, Berbara RLL, Madari BE (2014) The match between microbial community structure and soil properties is modulated by land use types and sample origin within an integrated agroecosystem. Soil Biol Biochem 78:97–108. https://doi.org/10.1016/j.soilbio.2014.07.017
Liu L, Greaver TL (2010) A global perspective on belowground carbon dynamics under nitrogen enrichment. Ecol Lett 13:819–828
Lopes AAC, Sousa DMG, Chaer GM, Berbara RLL, Madari BE (2013) Interpretation of microbial soil indicators as a function of crop yield and organic carbon. Soil Sci Soc Am J 77:461–472. https://doi.org/10.2136/sssaj2012.0191
Lopes AAC, Sousa DMG, Reis Junior FB, Mendes IC (2015) Air-drying and long-term storage effects on β-glucosidase, acid phosphatase and arylsulfatase activities in a tropical savannah oxisol. Appl Soil Ecol 93:68–77. https://doi.org/10.1016/j.apsoil.2015.04.001
McGowan AR, Nicoloso RS, Diop HE, Roozeboom KL, Rice CW (2019) Soil organic carbon, aggregation, and microbial community structure in annual and perennial biofuel crops. Agron J 111:128–142. https://doi.org/10.2134/agronj2018.04.0284
McKinley VL, Peacock AD, White DC (2005) Microbial community PLFA and PHB responses to ecosystem restoration in tallgrass prairie soils. Soil Biol Biochem 37:1946–1958. https://doi.org/10.1016/j.soilbio.2005.02.033
Mendes IC, Fernandes MF, Chaer GM, Reis Junior FB (2012) Biological functioning of Brazilian Cerrado soils under different vegetation types. Plant Soil 359:183–195. https://doi.org/10.1007/s11104-012-1195-6
Mikha MM, Rice CW (2004) Tillage and manure effects on soil and aggregate-associated carbon and nitrogen. Soil Sci Soc Am J 68:809–816. https://doi.org/10.1016/10.2136/sssaj2004.0809
Mueller KE, Eissenstat DM, Hobbie SE, Oleksyn J, Jagodzinski AM, Reich PB, Chadwick OA, Chorover J (2012) Tree species effects on coupled cycles of carbon, nitrogen, and acidity in mineral soils at a common garden experiment. Biogeochemistry 111:601–614. https://doi.org/10.1007/s10533-011-9695-7
Öpik M, Moora M, Liira J, Zobel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94:778–790. https://doi.org/10.1111/j.1365-2745.2006.01136.x
Peixoto R, Chaer G, Franco N, Junior FR, Mendes IC, Rosado AS (2010) A decade of land use contributes to changes in the chemistry, biochemistry and bacterial community structures of soils in the Cerrado. Antonie Leeuwenhoek 98:403–413. https://doi.org/10.1007/s10482-010-9454-0
Pengthamkeerati P, Motavalli PP, Kremer RJ (2011) Soil microbial activity and functional diversity changed by compaction, poultry litter and cropping in a claypan soil. Appl Soil Ecol 48:71–80. https://doi.org/10.1016/j.apsoil.2011.01.005
Pires CAB, Amado TJC, Reimche G, Schwalbert R, Sarto MVM, Nicoloso RS, Fiorin JE, Rice CW (2020) Diversified crop rotation with no-till changes microbial distribution with depth and enhances activity in a subtropical Oxisol. Eur J Soil Sci. https://doi.org/10.1111/ejss.12981
Powlson DS, Stirling CM, Thierfelder C, White RP, Jat ML (2016) Does conservation agriculture deliver climate change mitigation through soil carbon sequestration in tropical agro-ecosystems? Agric Ecosyst Environ 220:164–174. https://doi.org/10.1016/j.agee.2016.01.005
Raiesi F, Beheshti A (2014) Soil specific enzyme activity shows more clearly soil responses to paddy rice cultivation than absolute enzyme activity in primary forests of northwest Iran. Appl Soil Ecol 75:63–70. https://doi.org/10.1016/j.apsoil.2013.10.012
Rousk J, Brookes PC, Bååth E (2010) Investigating the mechanisms for the opposing pH relationships of fungal and bacterial growth in soil. Soil Biol Biochem 42:926–934. https://doi.org/10.1016/j.soilbio.2010.02.009
Sanz-Cobena A, Lassaletta L, Aguilera E et al (2017) Strategies for greenhouse gas emissions mitigation in Mediterranean agriculture: a review. Agric Ecosyst Environ 238:5–24. https://doi.org/10.1016/j.agee.2016.09.038
Sarto MV, Borges WL, Sarto JR, Rice CW, Rosolem CA (2020a) Root and shoot interactions in a tropical integrated crop–livestock–forest system. Agric Syst 181:1–11. https://doi.org/10.1016/j.agsy.2020.102796
Sarto MVM, Borges WLB, Sarto JRW, Pires CAB, Rice CW, Rosolem CA (2020b) Soil microbial community and activity in a tropical integrated crop–livestock system. Appl Soil Ecol 145:103350. https://doi.org/10.1016/j.apsoil.2019.08.012
Scott DA, Baer SG, Blair JM (2017) Recovery and relative influence of root, microbial, and structural properties of soil on physically sequestered carbon stocks in restored grassland. Soil Sci Soc Am J 81:50–60. https://doi.org/10.2136/sssaj2016.05.0158
Sinsabaugh RL, Antibus R, Linkins A, McClaugherty CA, Rayburn L, Repert D, Weiland T (1993) Wood decomposition: nitrogen and phosphorus dynamics in relation to extracellular enzyme activity. Ecology 74:1586–1593. https://doi.org/10.2307/1940086
Sinsabaugh RL, Lauber CL, Weintraub MN et al (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264. https://doi.org/10.1111/j.1461-0248.2008.01245.x
Six J, Conant RT, Paul EA, Paustian K (2002) Stabilization mechanisms of soil organic carbon: implications for C-saturation of soils. Plant Soil 241:155–176. https://doi.org/10.1023/A:1016125726789
Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–569. https://doi.org/10.2136/sssaj2004.0347
Soil Survey Staff (2014) Keys to soil taxonomy, 12th edn. USDA-Natural 695 Resources Conservation Service, Washington, DC.
Sotomayor-Ramírez D, Espinoza Y, Acosta-Martínez V (2009) Land use effects on microbial biomass C, β-glucosidase and β-glucosaminidase activities, and availability, storage, and age of organic C in soil. Biol Fertil Soils 45:487–497. https://doi.org/10.1007/s00374-009-0359-x
Souza RC, Mendes IC, Reis-Junior FB, Carvalho FM, Nogueira MA, Vasconcelos ATR, Vicente VA, Hungria M (2016) Shifts in taxonomic and functional microbial diversity with agriculture: How fragile is the Brazilian Cerrado? BMC Microbiol 16:1–15. https://doi.org/10.1186/s12866-016-0657-z
Tabatabai MA (1994) Soil enzymes. In: Weaver RW, Scott A, Bottomeley PJ (eds) Methods of soil analysis: microbiological and biochemical properties. Soil Science Society of America, Madison, pp 778–835
Tonucci RG, Nair VD, Nair PKR, Garcia R (2017) Grass vs. tree origin of soil organic carbon under different land-use systems in the Brazilian Cerrado. Plant Soil 419:281–292. https://doi.org/10.1007/s11104-017-3347-1
Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11:1111–1120. https://doi.org/10.1111/j.1461-0248.2008.01230.x
van Raij B, Andrade JC, Cantarella H, Quaggio JA (2001) Análise química para avaliação da fertilidade de solos tropicais. Instituto Agronômico, Campinas
Wakelin SA, Macdonald LM, Rogers SL (2008) Habitat selective factors influencing the structural composition and functional capacity of microbial communities in agricultural soils. Soil Biol Biochem 40:803–813. https://doi.org/10.1016/j.soilbio.2005.02.033
Wang C, Lu X, Mori T, Mao Q, Zhou K, Zhou G, Nie Y, Mo J (2018) Responses of soil microbial community to continuous experimental nitrogen additions for 13 years in a nitrogen-rich tropical forest. Soil Biol Biochem 121:103–112. https://doi.org/10.1016/j.soilbio.2018.03.009
Waring BG, Weintraub SR, Sinsabaugh RL (2014) Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry 117:101–113. https://doi.org/10.1007/s10533-013-9849-x
White PM, Rice CW (2009) Tillage effects on microbial and carbon dynamics during plant residue decomposition. Soil Sci Soc Am J 73:1–8. https://doi.org/10.2136/sssaj2007.0384
Wilson GWT, Rice CW, Rillig MC, Springer A, Hartnett DC (2009) Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments. Ecol Lett 12:452–461. https://doi.org/10.1111/j.1461-0248.2009.01303.x
Yang Y, Tilman D, Furey G, Lehman C (2019) Soil carbon sequestration accelerated by restoration of grassland biodiversity. Nat Commun 10:1–7. https://doi.org/10.1038/s41467-019-08636-w
Yoder RE (1936) A direct method of aggregate analysis of soil and a study of the physical nature of soil erosion losses. Soil Sci Soc Am J 28:337–351. https://doi.org/10.2134/agronj1936.00021962002800050001x
Zeglin LH, Bottomley PJ, Jumpponen A, Rice CW, Arango M, Lindsley A, McGowan A, Mfombep P, Myrold DD (2013) Altered precipitation regime affects the function and composition of soil microbial communities on multiple time scales. Ecology 94:2334–2345. https://doi.org/10.1890/12-2018.1
Zhang Q, Wu J, Yang F (2016) Alterations in soil microbial community composition and biomass following agricultural land use change. Sci Rep 6:1–10. https://doi.org/10.1038/srep36587
Zhou Z, Wang C, Zheng M, Jiang L, Luo Y (2017) Patterns and mechanisms of responses by soil microbial communities to nitrogen addition. Soil Biol Biochem 115:433–441. https://doi.org/10.1016/j.soilbio.2017.09.015
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To Coordination for the Improvement of Higher Education Personnel (CAPES). To FAPESP (São Paulo Research Foundation) for financial support of this research (Registry numbers: 2014/10656-3 and 2016/14323-4) and CNPq (Brazilian National Council for Scientific and Technological Development).
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Coordination for the Improvement of Higher Education Personnel (CAPES). To FAPESP (São Paulo Research Foundation) for financial support of this research (Registry numbers: 2014/10656-3 and 2016/14323-4) and CNPq (Brazilian National Council for Scientific and Technological Development).
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Sarto, M.V.M., Borges, W.L.B., Bassegio, D. et al. Soil microbial community, enzyme activity, C and N stocks and soil aggregation as affected by land use and soil depth in a tropical climate region of Brazil. Arch Microbiol 202, 2809–2824 (2020). https://doi.org/10.1007/s00203-020-01996-8
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DOI: https://doi.org/10.1007/s00203-020-01996-8