Fungal β-glucosidase gene and corresponding enzyme activity are positively related to soil organic carbon in unmanaged woody plantations

Maria Ludovica Saccà , Caputo Francesco , Ceotto Enrico , Fornasier Flavio

Soil Ecology Letters ›› 2024, Vol. 6 ›› Issue (4) : 240238

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Soil Ecology Letters ›› 2024, Vol. 6 ›› Issue (4) : 240238 DOI: 10.1007/s42832-024-0238-2
RESEARCH ARTICLE

Fungal β-glucosidase gene and corresponding enzyme activity are positively related to soil organic carbon in unmanaged woody plantations

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Abstract

● Soils from Poplar, Willow, Black locust plantations were compared to arable soil.

● Among five tested C cycle functional genes, three discriminated between treatments.

● Fungi contributed more than bacteria to the β-glucosidase enzyme activity.

● Fungal β-glucosidase gene may be considered an indicator of increased C storage.

Soil carbon sequestration is regulated by microbial extracellular enzymes. Insight into this process can be gained by studying the relationship between enzyme activity, soil organic carbon and microbial functional genes. The genetic potential of microorganisms to produce carbon cycling enzymes was evaluated in unmanaged plantations of Poplar, Willow, and Black locust, compared with a nearby arable soil. Bacterial and fungal functional genes encoding for cellulase, endoglucanase, endoxylanase and β-glucosidase enzymes were quantified by real-time PCR. The abundance of three out of five genes differed between the treatments. The fungal gene encoding β-glucosidase contributed to the corresponding enzyme activity more than the bacterial one, as evidenced by a positive correlation between gene abundance and enzyme activity (r = 0.42). This gene exhibited a positive correlation with soil organic carbon content (r = 0.42), with higher values in Willow (9 × 102 gene copies µL−1 and 1.4% SOC). These results suggest that the fungal β-glucosidase gene abundance can be regarded as an indicator of increased carbon storage, similarly to the corresponding enzyme activity. The integrated analysis of soil carbon enzyme activities and DNA-based techniques enhanced our comprehension of carbon dynamics by revealing distinct contributions of microbial taxonomic groups to carbon accrual.

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Keywords

carbon accrual / soil enzymes / β-glucosidase gene / genetic potential / microorganisms

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Maria Ludovica Saccà, Caputo Francesco, Ceotto Enrico, Fornasier Flavio. Fungal β-glucosidase gene and corresponding enzyme activity are positively related to soil organic carbon in unmanaged woody plantations. Soil Ecology Letters, 2024, 6(4): 240238 DOI:10.1007/s42832-024-0238-2

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References

[1]

Adetunji, A.T., Lewu, F.B., Mulidzi, R., Ncube, B., 2017. The biological activities of β-glucosidase, phosphatase and urease as soil quality indicators: a review. Journal of Soil Science and Plant Nutrition17, 794–807.

[2]

Bailey, V.L., Smith, J.L., Bolton, H. Jr, 2002. Fungal-to-bacterial ratios in soils investigated for enhanced C sequestration. Soil Biology & Biochemistry34, 997–1007.

[3]

Baldrian, P., 2014. Distribution of extracellular enzymes in soils: Spatial heterogeneity and determining factors at various scales. Soil Science Society of America Journal78, 11–18.

[4]

Barbi, F., Bragalini, C., Vallon, L., Prudent, E., Dubost, A., Fraissinet-Tachet, L., Marmeisse, R., Luis, P., 2014. PCR primers to study the diversity of expressed fungal genes encoding lignocellulolytic enzymes in soils using high-throughput sequencing. PLoS One9, e116264.

[5]

Barbi, F., Prudent, E., Vallon, L., Buée, M., Dubost, A., Legout, A., Marmeisse, R., Fraissinet-Tachet, L., Luis, P., 2016. Tree species select diverse soil fungal communities expressing different sets of lignocellulolytic enzyme-encoding genes. Soil Biology & Biochemistry100, 149–159.

[6]

Blonska, E., Lasota, J., da Silva, G.R.V., Vanguelova, E., Ashwood, F., Tibbett, M., Watts, K. and Lukac, M., 2020. Soil organic matter stabilization and carbon-cycling enzyme activity are affected by land management. Annals of Forest Research63, 71–86.

[7]

Bonan, G.B., 2008. Forests and climate change: Forcings, feedbacks, and the climate benefits of forests. Science320, 1444–1449.

[8]

Burns, R.G., DeForest, J.L., Marxsen, J., Sinsabaugh, R.L., Stromberger, M.E., Wallenstein, M.D., Weintraub, M.N., Zoppini, A., 2013. Soil enzymes in a changing environment: Current knowledge and future directions. Soil Biology & Biochemistry58, 216–234.

[9]

Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M.W., Shipley, G.L., Vandesompele, J., Wittwer, C.T., 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry55, 611–622.

[10]

Cañizares, R., Benitez, E., Ogunseitan, O.A., 2011. Molecular analyses of β-glucosidase diversity and function in soil. European Journal of Soil Biology47, 1–8.

[11]

Cañizares, R., Moreno, B., Benitez, E., 2012a. Biochemical characterization with detection and expression of bacterial β-glucosidase encoding genes of a Mediterranean soil under different long-term management practices. Biology and Fertility of Soils48, 651–663.

[12]

Cañizares, R., Moreno, B., Benitez, E., 2012b. Bacterial β-glucosidase function and metabolic activity depend on soil management in semiarid rainfed agriculture. Ecology and Evolution2, 727–731.

[13]

Ceotto, E., Di Candilo, M., 2011. Medium-term effect of perennial energy crops on soil organic carbon storage. Italian Journal of Agronomy6, e33–e33.

[14]

Chen, J., Sinsabaugh, R.L., 2021. Linking microbial functional gene abundance and soil extracellular enzyme activity: Implications for soil carbon dynamics. Global Change Biology27, 1322–1325.

[15]

Cowie, A.L., Lonergan, V.E., Rabbi, S.M.F., Fornasier, F., Macdonald, C., Harden, S., Kawasaki, A., Singh, B.K., 2013. Impact of carbon farming practices on soil carbon in northern New South Wales. Soil Research (Collingwood, Vic.)51, 707–718.

[16]

de Almeida, R.F., Naves, E.R., da Mota, R.P., 2015. Soil quality: Enzymatic activity of soil β-glucosidase. Global Journal of Agricultural Research and Reviews3, 146–150.

[17]

FAO, 2020. Global Forest Resources Assessment 2020– Key findings. Rome

[18]

Gil-Sotres, F., Trasar-Cepeda, C., Leirós, M.C., Seoane, S., 2005. Different approaches to evaluating soil quality using biochemical properties. Soil Biology & Biochemistry37, 877–887.

[19]

Hammer, Ø., Harper, D.A.T., Ryan, P.D., 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica4, 1–9.

[20]

He, Z., Gentry, T.J., Schadt, C.W., Wu, L., Liebich, J., Chong, S.C., Huang, Z., Wu, W., Gu, B., Jardine, P., Criddle, C., Zhou, J., 2007. GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes. The ISME Journal1, 67–77.

[21]

Ivashchenko, K., Sushko, S., Selezneva, A., Ananyeva, N., Zhuravleva, A., Kudeyarov, V., Makarov, M., Blagodatsky, S., 2021. Soil microbial activity along an altitudinal gradient: Vegetation as a main driver beyond topographic and edaphic factors. Applied Soil Ecology168, 104197.

[22]

Kellner, H., Luis, P., Schlitt, B., Buscot, F., 2009. Temporal changes in diversity and expression patterns of fungal laccase genes within the organic horizon of a brown forest soil. Soil Biology & Biochemistry41, 1380–1389.

[23]

Kellner, H., Vandenbol, M., 2010. Fungi unearthed: Transcripts encoding lignocellulolytic and chitinolytic enzymes in forest soil. PLoS One5, e10971.

[24]

Khamassi, A., Dumon, C., 2023. Enzyme synergy for plant cell wall polysaccharide degradation. Essays in Biochemistry67, 521–531.

[25]

Kozjek, K., Manoharan, L., Ahrén, D., Hedlund, K., 2022. Microbial functional genes influenced by short-term experimental drought across European agricultural fields. Soil Biology & Biochemistry168, 108650.

[26]

Liao, J., Dou, Y., Yang, X., An, S., 2023. Soil microbial community and their functional genes during grassland restoration. Journal of Environmental Management325, 116488.

[27]

Liu, M., Wei, Y., Lian, L., Wei, B., Bi, Y., Liu, N., Yang, G., Zhang, Y., 2023. Macrofungi promote SOC decomposition and weaken sequestration by modulating soil microbial function in temperate steppe. Science of the Total Environment899, 165556.

[28]

Malik, A.A., Chowdhury, S., Schlager, V., Oliver, A., Puissant, J., Vazquez, P.G.M., Jehmlich, N., von Bergen, M., Griffiths, R.I., Gleixner, G., 2016. Soil fungal: Bacterial ratios are linked to altered carbon cycling. Frontiers in Microbiology7, 1247.

[29]

Manoharan, L., Kushwaha, S.K., Hedlund, K., Ahrén, D., 2015. Captured metagenomics: large-scale targeting of genes based on “sequence capture” reveals functional diversity in soils. DNA Research22, 451–460.

[30]

Martinez, D., Challacombe, J., Morgenstern, I., Hibbett, D., Schmoll, M., Kubicek, C.P., Ferreira, P., Ruiz-Duenas, F.J., Martinez, A.T., Kersten, P., Hammel, K.E., Vanden Wymelenberg, A., Gaskell, J., Lindquist, E., Sabat, G., Splinter BonDurant, S., Larrondo, L.F., Canessa, P., Vicuna, R., Yadav, J., Doddapaneni, H., Subramanian, V., Pisabarro, A.G., Lavín, J.L., Oguiza, J.A., Master, E., Henrissat, B., Coutinho, P.M., Harris, P., Magnuson, J.K., Baker, S.E., Bruno, K., Kenealy, W., Hoegger, P.J., Kües, U., Ramaiya, P., Lucas, S., Salamov, A., Shapiro, H., Tu, H., Chee, C.L., Misra, M., Xie, G., Teter, S., Yaver, D., James, T., Mokrejs, M., Pospisek, M., Grigoriev, I.V., Brettin, T., Rokhsar, D., Berka, R., Cullen, D., 2009. Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proceedings of the National Academy of Sciences of the United States of America106, 1954–1959.

[31]

Martinović T., Mašínová T., López-Mondéjar, R., Jansa, J., Štursová M., Starke, R., Baldrian, P., 2022. Microbial utilization of simple and complex carbon compounds in a temperate forest soil. Soil Biology & Biochemistry173, 108786.

[32]

Merlin, C., Besaury, L., Niepceron, M., Mchergui, C., Riah, W., Bureau, F., Gattin, I., Bodilis, J., 2014. Real-time PCR for quantification in soil of glycoside hydrolase family 6 cellulase genes. Letters in Applied Microbiology59, 284–291.

[33]

Moreno, B., Cañizares, R., Nuñez, R., Benitez, E., 2013. Genetic diversity of bacterial β-glucosidase-encoding genes as a function of soil management. Biology and Fertility of Soils49, 735–745.

[34]

Nannipieri, P., Giagnoni, L., Renella, G., Puglisi, E., Ceccanti, B., Masciandaro, G., Fornasier, F., Moscatelli, M.C., Marinari, S., 2012. Soil enzymology: classical and molecular approaches. Biology and Fertility of Soils48, 743–762.

[35]

Kimble, J., Lal, R., Follett, R., 2002. Application of a Management Decision Aid for Sequestration of Carbon and Nitrogen in Soil. In: Olness, A., Lopez, D., Cordes, J., eds. Agricultural Practices and Policies for Carbon Sequestration in Soil. Lewis Publisher, CRC press LLC, Boca Raton, FL, USA, pp. 245–253

[36]

Page, A.L., Miller, R.H., Keeney, D.R.,1982. Methods of Soil Analysis. Part 2, 2nd edn. American Society of Agronomy, Soil Science Society of America, Madison, Wisconsin

[37]

Pathan, S.I., Žifčáková L., Ceccherini, M.T., Pantani, O.L., Větrovský T., Baldrian, P., 2017. Seasonal variation and distribution of total and active microbial community of β-glucosidase encoding genes in coniferous forest soil. Soil Biology & Biochemistry105, 71–80.

[38]

Rocca, J.D., Hall, E.K., Lennon, J.T., Evans, S.E., Waldrop, M.P., Cotner, J.B., Nemergut, D.R., Graham, E.B., Wallenstein, M.D., 2015. Relationships between protein-encoding gene abundance and corresponding process are commonly assumed yet rarely observed. The ISME Journal9, 1693–1699.

[39]

SAS Institute, 2015. SAS/STAT 14.1 User’s Guide. Available at the webpage of SAS

[40]

Schmidt, J.E., Kent, A.D., Brisson, V.L., Gaudin, A.C.M., 2019. Agricultural management and plant selection interactively affect rhizosphere microbial community structure and nitrogen cycling. Microbiome7, 146.

[41]

Soil Survey Staff, 2006. Keys to Soil Taxonomy. USDA Natural Resources Conservation Service, 10 th. Washington, USA

[42]

Stott, D.E., Andrews, S.S., Liebig, M.A., Wienhold, B.J., Karlen, D.L., 2010. Evaluation of β-glucosidase activity as a soil quality indicator for the soil management assessment framework. Soil Science Society of America Journal74, 107–119.

[43]

Tao, F., Huang, Y., Hungate, B.A., Manzoni, S., Frey, S.D., Schmidt, M.W.I., Reichstein, M., Carvalhais, N., Ciais, P., Jiang, L., Lehmann, J., Wang, Y.P., Houlton, B.Z., Ahrens, B., Mishra, U., Hugelius, G., Hocking, T.D., Lu, X., Shi, Z., Viatkin, K., Vargas, R., Yigini, Y., Omuto, C., Malik, A.A., Peralta, G., Cuevas-Corona, R., Di Paolo, L.E., Luotto, I., Liao, C., Liang, Y.S., Saynes, V.S., Huang, X., Luo, Y., 2023. Microbial carbon use efficiency promotes global soil carbon storage. Nature618, 981–985.

[44]

Trivedi, P., Delgado-Baquerizo, M., Trivedi, C., Hu, H., Anderson, I.C., Jeffries, T.C., Zhou, J., Singh, B.K., 2016. Microbial regulation of the soil carbon cycle: evidence from gene–enzyme relationships. ISME Journal10, 2593–2604.

[45]

Trivedi, P., Wallenstein, M.D., Delgado-Baquerizo, M., Singh, B.K., 2018. Chapter 3−Microbial Modulators and Mechanisms of Soil Carbon Storage. In: Singh, B.K., ed. Soil Carbon Storage. Academic Press, pp. 73–115

[46]

Voegel, T.M., Larrabee, M.M., Nelson, L.M., 2021. Development of droplet digital PCR assays to quantify genes involved in nitrification and denitrification, comparison with quantitative real-time PCR and validation of assays in vineyard soil. Canadian Journal of Microbiology67, 174–187.

[47]

Wallenstein, M.D., Weintraub, M.N., 2008. Emerging tools for measuring and modeling the in situ activity of soil extracellular enzymes. Soil Biology & Biochemistry40, 2098–2106.

[48]

Xu, S., Su, F., Sayer, E.J., Lam, S.K., Lu, X., Liu, C., Lai, D.Y.F., 2023. Fine root litter quality regulates soil carbon storage efficiency in subtropical forest soils. Soil Ecology Letters5, 230182.

[49]

Xue, K., Wu, L., Deng, Y., He, Z., Van Nostrand, J., Robertson, P.G., Schmidt, T.M., Zhou, J., 2013. Functional gene differences in soil microbial communities from conventional, low-input, and organic farmlands. Applied and Environmental Microbiology79, 1284–1292.

[50]

Yang, X., Ni, K., Shi, Y., Yi, X., Ji, L., Wei, S., Jiang, Y., Zhang, Y., Cai, Y., Ma, Q., Tang, S., Ma, L., Ruan, J., 2023. Metagenomics reveals N-induced changes in carbon-degrading genes and microbial communities of tea (Camellia sinensis L. ) plantation soil under long-term fertilization. Science of the Total Environment856, 159231.

[51]

Yu, L., Luo, S., Xu, X., Gou, Y., Wang, J., 2020. The soil carbon cycle determined by GeoChip 5.0 in sugarcane and soybean intercropping systems with reduced nitrogen input in South China. Applied Soil Ecology155, 103653.

[52]

Zeng, Q., Mei, T., Wang, M., Tan, W., 2022. Intensive citrus plantations suppress the microbial profiles of the β-glucosidase gene. Agriculture, Ecosystems & Environment323, 1–9.

[53]

Zhang, J., Viikari, L., 2014. Impact of xylan on synergistic effects of xylanases and cellulases in enzymatic hydrolysis of lignocelluloses. Applied Biochemistry and Biotechnology174, 1393–1402.

[54]

Zhao, F., Wang, J., Li, Y., Xu, X., He, L., Wang, J., Ren, C., Guo, Y., 2022. Microbial functional genes driving the positive priming effect in forest soils along an elevation gradient. Soil Biology & Biochemistry165, 108498.

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