Abstract
The enzymatic stoichiometry allows assessing microbial C, N, and P acquisition, being used to indicate a nutrient limitation in soils. This study evaluated the enzymatic stoichiometry in soils from different physiognomies of the Brazilian Cerrado, trying to indicate a possible nutrient limitation in these areas. The enzymes β-glucosidase (BG), urease (U), and acid phosphatase (AP) were assessed in soil samples from three different physiognomies of Cerrado, namely, Campo Graminoide (CG), Cerrado Stricto Sensu (CSS), and Cerradão (CD). The activities of BG/U, BG/AP, and U/AP were used for calculating the enzymatic C/N, C/P, and N/P ratios, respectively. In addition, the vectors L and A, which are indirect indicators of P and N limitation to microbes, were assessed in soils. The enzymatic stoichiometry varied between physiognomies and seasons, with values of BG/U, BG/AP, and U/AP ratios being higher in the wet than the dry season. When comparing among physiognomies, the values of BG/U and BG/AP ratios increased from CG to CSS and CD. The vector A decreased from CG to CSS and CD. Together, the stoichiometry of enzymes approach and the analyses of vectors L and A suggest that soils from the different physiognomies of Cerrado could be P-limited. Thus, it requires further studies on P dynamics in Cerrado soils.
This is a preview of subscription content, log in via an institution to check access.
Data Availability
All data are available upon request.
References
Adetunji AT, Lewu FB, Mulidzi R, Ncube B (2017) The biological activities of β-glucosidase, phosphatase and urease as soil quality indicators: a review. J Soil Sci Plant Nutr 17:794–807
Araújo ASF, Cesarz S, Leite LFC et al (2013) Soil microbial properties and temporal stability in degraded and restored lands of Northeast Brazil. Soil Biol Biochem 66:175–181. https://doi.org/10.1016/j.soilbio.2013.07.013
Araujo ASF, Bezerra WM, dos Santos VM et al (2017) Distinct bacterial communities across a gradient of vegetation from a preserved Brazilian Cerrado. Antonie Van Leeuwenhoek, Int J Gen Mol Microbiol 110:457–469. https://doi.org/10.1007/s10482-016-0815-1
Araujo ASF, Mendes LW, Bezerra WM et al (2018a) Archaea diversity in vegetation gradients from the Brazilian Cerrado. Brazilian J Microbiol 49:522–528. https://doi.org/10.1016/j.bjm.2017.08.010
Araujo ASF, Mendes LW, Lemos LN, et al (2018b) Protist species richness and soil microbiome complexity increase towards climax vegetation in the Brazilian Cerrado. Commun Biol 1:135 https://doi.org/10.1038/s42003-018-0129-0
Araujo ASF, Oliveira LM de S, Melo VMM, et al (2021) Distinct taxonomic composition of soil bacterial community across a native gradient of Cerrado-Ecotone-Caatinga.Appl Soil Ecol 161:103874 https://doi.org/10.1016/j.apsoil.2020.103874
Bai X, Dippold MA, An S et al (2021) Extracellular enzyme activity and stoichiometry: the effect of soil microbial element limitation during leaf litter decomposition. Ecol Indic 121:107200. https://doi.org/10.1016/j.ecolind.2020.107200
Ben KJ, Hoosbeek MR, Taylor CR et al (2020) Soil C, N and P cycling enzyme responses to nutrient limitation under elevated CO2. Biogeochemistry 151:221–235. https://doi.org/10.1007/s10533-020-00723-1
Bremner JM (1996) Nitrogen total. In: Sparks DL, Page AL, Helmke PA, Loeppert RH, Soltanpour PN, Tabatabai MA, Johnston CT, Sumner ME (eds) Methods of Soil Analysis, Part 3: Chemical Methods, 5.3. Soil Science Society of America: Madison, Wisconsin, 1085–1121
Carvalho NS, Rocha SMB, Santos VM, Araujo FF, Araújo ASF (2018) Soil microbial biomass across a gradient of preserved native Cerrado. Floram 25:e20170536
Carvalho Mendes I, Fernandes MF, Chaer GM, dos Reis B, Junior F (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
Chen J, Luo Y, van Groenigen KJ, Hungate BA, Cao J, Zhou X, Wang R (2018) A keystone microbial enzyme for nitrogen control of soil carbon storage. Sci Adv 4:eaaq1689. https://doi.org/10.1126/sciadv.aaq1689
Chen H, Li DJ, Mao QG, **ao KC, Wang KL (2019) Resource limitation of soil microbes in karst ecosystems. Sci Total Environ 650:241–248. https://doi.org/10.1016/j.scitotenv.2018.09.036
Cordero I, Snell H, Bardgett RD (2019) High throughput method for measuring urease activity in soil. Soil Biol Biochem 134:72–77. https://doi.org/10.1016/j.soilbio.2019.03.014
Cruz Ruggiero PG, Batalha MA, Pivello VR, Meirelles ST (2002) Soil-vegetation relationships in cerrado (Brazilian savanna) and semideciduous forest, Southeastern Brazil. Plant Ecol 160:1–16. https://doi.org/10.1023/A:1015819219386
Das SK, Varma A (2010) Role of enzymes in maintaining soil health. Springer, Berlin, Heidelberg, pp 25–42
de Castro A, Lopes A, Gomes de Sousa DM, Chaer GM et al (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
Eivazi F, Tabatabai MAA (1988) Glucosidases and galactosidases in soils. Soil Biol Biochem 20:601–606. https://doi.org/10.1016/0038-0717(88)90141-1
Empresa Brasileira de Pesquisa Agropequária – Embrapa (1997) Manual de métodos de análise de solo. 2ed. Rio de Janeiro, 212p
Ferreira A de S, Espíndola SP, Rita MCC (2016) Assessment and kinetics of soil phosphatase in Brazilian Savanna systems. An Acad Bras Cienc 88:1035–1044. https://doi.org/10.1590/0001-3765201620140033
Furley PA (1999) The nature and diversity of neotropical savanna vegetation with particular reference to the Brazilian cerrados. Glob Ecol Biogeogr 8:223–241. https://doi.org/10.1046/j.1365-2699.1999.00142.x
Gunina A, Kuzyakov Y (2015) Sugars in soil and sweets for microorganisms: review of origin, content, composition and fate. Soil Biol Biochem 90:87–100
Hammer Ø, Harper DAT a. T, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):1–9.https://doi.org/10.1016/j.bcp.2008.05.025
Hill BH, Elonen CM, Seifert LR, May AA, Tarquinio E (2012) Microbial enzyme stoichiometry and nutrient limitation in US streams and rivers. Ecol Indicators 18:540–551. https://doi.org/10.1016/j.ecolind.2012.01.007
Hill BH, Elonen CM, Jicha TM, Kolka RK, Lehto LLP, Sebestyen SD (2014) Ecoenzymatic stoichiometry and microbial processing of organic matter in northern bogs and fens reveals a common P-limitation between peatland types. Biogeochemistry 120:203–224
Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fert Soils 6:68–72. https://doi.org/10.1007/BF00257924
Loeppmann S, Breidenbach A, Spielvogel S, Dippold MA and Blagodatskaya E (2020) Organic nutrients induced coupled C- and P-Cycling enzyme activities during microbial growth in forest soils. Front For Glob Change 3:100
Lopes AAC, Sousa DMG, Chaer GM, Reis Junior FB, Goedert WJ, Mendes IC (2013) Interpretation of microbial soil indicators as a function of crop yield and organic carbon. Soil Sci Soc Am J 77:461–472
Liu J, Chen J, Chen G et al (2020) Enzyme stoichiometry indicates the variation of microbial nutrient requirements at different soil depths in subtropical forests. PLoS ONE 15:1–17. https://doi.org/10.1371/journal.pone.0220599
Liu L, Zhu K, Wurzburger N, Zhang J (2020b) Relationships between plant diversity and soil microbial diversity vary across taxonomic groups and spatial scales. Ecosphere 11:e02999. https://doi.org/10.1002/ecs2.2999
Machuca A, Cuba-Díaz M, Córdova C (2015) Enzymes in the rhizosphere of plants growing in the vicinity of the polish arctowski antarctic station. J Soil Sci Plant Nutr 15:833–838. https://doi.org/10.4067/S0718-95162015005000057
Margalef O, Sardans J, Fernández-Martínez M et al (2017) Global patterns of phosphatase activity in natural soils. Sci Rep 7:1–13. https://doi.org/10.1038/s41598-017-01418-8
Mendes LW, Braga LPP, Navarrete AA et al (2017) Using metagenomics to connect microbial community biodiversity and functions. Curr Issues Mol Biol 24:103–118. https://doi.org/10.21775/cimb.024.103
Moorhead DL, Sinsabaugh RL, Hill BH, Weintraub MN (2016) Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics. Soil Biol Biochem 93:1–7. https://doi.org/10.1016/j.soilbio.2015.10.019
Mukumbareza C, Muchaonyerwa P, Chiduza C (2016) Bicultures of oat (Avena sativa L.) and grazing vetch (Vicia dasycarpa L.) cover crops increase contents of carbon pools and activities of selected enzymes in a loam soil under warm temperate conditions. Soil Sci Plant Nutr 62:447–455. https://doi.org/10.1080/00380768.2016.1206833
Myers N, Mittermeier RA, Mittermeier CG et al (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. https://doi.org/10.1038/35002501
Nardoto GB, Da Cunha Bustamante MM, Pinto AS, Klink CA (2006) Nutrient use efficiency at ecosystem and species level in savanna areas of Central Brazil and impacts of fire. J Trop Ecol 22:191–201. https://doi.org/10.1017/S0266467405002865
Oliveira MEA, Martins FR, Castro AAJF, Santos JR (2007) Classes de cobertura vegetal do Parque Nacional de Sete Cidades (transição campo-floresta) utilizando imagens TM/Landsat, NE do Brasil. In: Simpósio Brasileiro de Sensoriamento Remoto, 13. Florianópolis. Anais (Proceedings), 13:1775–1783 (In Portuguese)
Paul EA (2006) Soil microbiology, ecology, and biochemistry, 3rd edn. Academic press, London
Pavinato PS, Merlin A, Rosolem CA (2009) Phosphorus fractions in Brazilian Cerrado soils as affected by tillage. Soil Tillage Res 105:149–155. https://doi.org/10.1016/j.still.2009.07.001
Pavinato PS, Rocha GC, Cherubin MR et al (2020) Map of total phosphorus content in native soils of Brazil. Sci Agric 78:1–5. https://doi.org/10.1590/1678-992x-2020-0077
Peng X, Wang W (2016) Stoichiometry of soil extracellular enzyme activity along a climatic transect in temperate grasslands of northern China. Soil Biol Biochem 98:74–84. https://doi.org/10.1016/j.soilbio.2016.04.008
Piotrowska-Długosz A, Charzyński P (2015) The impact of the soil sealing degree on microbial biomass, enzymatic activity, and physicochemical properties in the Ekranic Technosols of Toruń (Poland). J Soils Sediments 15:47–59. https://doi.org/10.1007/s11368-014-0963-8
Procópio L, Barreto C (2021) The soil microbiomes of the Brazilian Cerrado. J Soils Sediments 21: 2327–2342. https://doi.org/10.1007/s11368-021-02936-9
Qin L, Freeman C, Jia X, Zhang Z, Liu B, Zhang S, Jiang M (2021) Microbial enzyme activity and stoichometry signal the effects of agricultural intervention on nutrient cycling in peatlands. Ecol Ind 122:107242. https://doi.org/10.1016/j.ecolind.2020.107242
Resende JCF, Markewitz D, Klink CA et al (2011) Phosphorus cycling in a small watershed in the Brazilian Cerrado: impacts of frequent burning. Biogeochemistry 105:105–118. https://doi.org/10.1007/s10533-010-9531-5
Rocha SMB, Antunes JEL, Araujo FF, Araujo ASF (2019) Soil microbial C:N:P ratio across physiognomies of Brazilian cerrado. An Acad Bras Ci 91:e20190049. https://doi.org/10.1590/0001-3765201920190049
Schade JD, Espeleta JF, Klausmeier CA et al (2005) A conceptual framework for ecosystem stoichiometry: balancing resource supply and demand. Oikos 109:40–51. https://doi.org/10.1111/j.0030-1299.2005.14050.x
Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798. https://doi.org/10.1038/nature08632
Sommers LE, Nelson DW (1972) Determination of total phosphorus in soils: a rapid perchloric acid digestion procedure. Soil Sci Soc Am J 36:902–904
Tabatabai MA, Bremner JM (1969) Use of p-nitrophe- nyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307
Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707. https://doi.org/10.1016/0038-0717(87)90052-6
Wallenstein M, Allison SD, Ernakovich J et al (2010) Controls on the temperature sensitivity of soil enzymes: a key driver of in situ enzyme activity rates. Springer, Berlin, Heidelberg, pp 245–258
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
Xu Z, Yu G, Zhang X et al (2017) Soil enzyme activity and stoichiometry in forest ecosystems along the North-South Transect in eastern China (NSTEC). Soil Biol Biochem 104:152–163. https://doi.org/10.1016/j.soilbio.2016.10.020
Yeomans JC, Bremner JM (1998) A rapid and precise method for routine determimation of organic carbon in soil. Comm Soil Sci Pl Anal 19:467–1476
Zhang Y, Chen L, Wu Z, Sun C (2011) Kinetic parameters of soil β-glucosidase response to environmental temperature and moisture regimes. Rev Bras Ci Solo 35:1285–1291. https://doi.org/10.1590/s0100-06832011000400022
Zhang T, Wan S, Kang Y, Feng H (2014) Urease activity and its relationships to soil physiochemical properties in a highly saline-sodic soil. J Soil Sci Plant Nutr 14:304–315. https://doi.org/10.4067/S0718-95162014005000025
Zhou L, Liu S, Shen H et al (2020) Soil extracellular enzyme activity and stoichiometry in China’s forests. Funct Ecol 34:1461–1471. https://doi.org/10.1111/1365-2435.13555
Funding
This study was funded by Fundacao de Amparo a Pesquisa do Estado do Piauí – FAPEPI and Conselho Nacional de Desenvolvimento Científico e Tecnologico – CNPq (grant 305069/2018–1). Sandra Mara Barbosa Rocha thanks FAPEPI/CAPES for her fellowship. Ademir S. F. Araujo, Fabio F. Araujo, and Erika V. Medeiros thank CNPq for their fellowship of research. Lucas W. Mendes thanks FAPESP (grant 2020/12890–4) for his fellowship.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics Approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Consent to Participate
Not applicable.
Consent for Publication
Not applicable.
Competing Interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Araujo, A.S.F., Bonifacio, A., Pereira, A.P.d.A. et al. Enzymatic Stoichiometry in Soils from Physiognomies of Brazilian Cerrado. J Soil Sci Plant Nutr 22, 2735–2742 (2022). https://doi.org/10.1007/s42729-022-00840-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42729-022-00840-w