ORIGINAL PAPER
Field-flow fractionation and gel permeation methods for total soil fungal mass determination
1
Institute of Agricultural Chemistry and Soil Science, University of Debrecen, Hungary
2
Department of Crop and Soil Science, Oregon State University, United States
3
Engineering and Nutrition, Faculty of Engineering, LTH, Department of Food Technology, Lund University, Sweden
4
Institute of Environmental Sciences, University of Nyiregyhaza, Hungary
Submission date: 2021-07-27
Final revision date: 2021-10-18
Acceptance date: 2021-11-12
Online publication date: 2022-02-03
Publication date: 2022-02-03
Corresponding author
Áron Béni
Institute of Agricultural Chemistry and Soil Science, University of Debrecen, Böszörményi u 138, 4032, Debrecen, Hungary
Institute of Agricultural Chemistry and Soil Science, University of Debrecen, Böszörményi u 138, 4032, Debrecen, Hungary
Soil Sci. Ann., 2021, 72(3)143901
KEYWORDS
ABSTRACT
Fungi are critical components of the soil food web. Fungi are important as organic matter decomposers, nutrient recyclers, and fungal hyphae play a role on the formation of soil aggregates that can increase water infiltration, improve water holding capacity, and sequester soil carbon (C). Ergosterol is a sterol found ubiquitously in cell membranes of filamentous fungi and is commonly used as a marker compound for fungal biomass. In contrast, the analysis of chitin is potentially effective way to monitor changes in total fungal mass (biomass and necromass) under different environmental conditions, because chitinis a more stable compound than ergosterol. By combining this analysis with our previously developed ergosterol method, we can determine both live fungal biomass and by subtraction, fungal necromass, thus providing useful information on the turnover dynamics of total fungal mass. We developed a sample preparation method based on extraction and conversion of chitin to chitosan, after which chitosan is measured by Asymmetrical Flow Field-Flow Fractionation (AF4). Our results show that this analytical method is a simple, fast, and cost-effective technique for the quantitative analysis of chitin from field-collected soils. The detection limit of this method is 6 μg g–1 chitin (chitosan) in dry soil. The final method linear range is 20 – 500 μg g–1 for chitin and 0.4 - 10 mg g–1 for fungal biomass. The developed chitin based and existing ergosterol based fungal estimation methods were used for the soil analysis. These methods can combine to determine the living and total fungal biomass.
REFERENCES (59)
1.
Abo Elsoud, M. M., El Kady, E. M., 2019. Current trends in fungal biosynthesis of chitin and chitosan. Bulletin of the National Research Centre 43(1), 59. https://doi.org/10.1186/s42269....
2.
Adamczyk, S., Larmola, T., Peltoniemi, K., Laiho, R., Näsholm, T., Adamczyk, B., 2020. An optimized method for studying fungal biomass and necromass in peatlands via chitin concentration. Soil Biology and Biochemistry 149, 107932. https://doi.org/10.1016/j.soil....
3.
Appuhn, A., Joergensen, R. G., 2006. Microbial colonisation of roots as a function of plant species. Soil Biology and Biochemistry 38(5), 1040-1051. https://doi.org/10.1016/j.soil....
4.
Averill, C., 2016. Slowed decomposition in ectomycorrhizal ecosystems is independent of plant chemistry. Soil Biology and Biochemistry 102, 52-54. https://doi.org/10.1016/j.soil....
5.
Axelsson, B.-O., Saraf, A., Larsson, L., 1995. Determination of ergosterol in organic dust by gas chromatography-mass spectrometry. Journal of Chromatography B: Biomedical Sciences and Applications 666(1), 77-84. https://doi.org/10.1016/0378-4....
6.
Baldrian, P., Větrovský, T., Cajthaml, T., Dobiášová, P., Petránková, M., Šnajdr, J., Eichlerová, I., 2013. Estimation of fungal biomass in forest litter and soil. Fungal Ecology 6(1), 1-11. https://doi.org/10.1016/j.fune....
7.
Baldrian, P., Voříšková, J., Dobiášová, P., Merhautová, V., Lisá, L., Valášková, V., 2011. Production of extracellular enzymes and degradation of biopolymers by saprotrophic microfungi from the upper layers of forest soil. Plant and Soil 338(1), 111-125. https://doi.org/10.1007/s11104....
8.
Bayart, C., Jean, E., Paillagot, M., Renoud, A., Raillard, A., Paladino, J., Le Borgne, M., 2019. Comparison of SEC and AF4 analytical tools for size estimation of typhoid Vi polysaccharides. Analytical Methods 11(37), 4851-4858. https://doi.org/10.1039/C9AY00....
9.
Beare, M. H., Hu, S., Coleman, D. C., Hendrix, P. F., 1997. Influences of mycelial fungi on soil aggregation and organic matter storage in conventional and no-tillage soils. Applied Soil Ecology 5(3), 211-219. https://doi.org/10.1016/S0929-....
10.
Beni, Á., Lajtha, K., Kozma, J., Fekete, I., 2017. Application of a Stir Bar Sorptive Extraction sample preparation method with HPLC for soil fungal biomass determination in soils from a detrital manipulation study. Journal of Microbiological Methods 136, 1-5. https://doi.org/10.1016/j.mime....
11.
Beni, A., Soki, E., Lajtha, K., Fekete, I., 2014. An optimized HPLC method for soil fungal biomass determination and its application to a detritus manipulation study. Journal of Microbiological Methods 103, 124-130. https://doi.org/10.1016/j.mime....
12.
Bhuiyan, R. M. A., Shaid, A., Bashar, M. M., Haque, P., Hannan, M. A., 2013. A novel approach of dyeing jute fiber with reactive dye after treating with chitosan. Open Journal of Organic Polymer Materials 3, 87-91. https://doi.org/10.4236/ojopm.....
13.
Blumenthal, H. J., Roseman, S., 1957. Quantitative estimation of chitin in fungi. J Bacteriol 74(2), 222-224.
14.
Boer, W. d., Folman, L. B., Summerbell, R. C., Boddy, L., 2005. Living in a fungal world: impact of fungi on soil bacterial niche development. Federation of European Microbiological Societies - Microbiology Reviews 29(4), 795-811. https://doi.org/10.1016/j.fems....
15.
Brzostek, E. R., Dragoni, D., Brown, Z. A., Phillips, R. P., 2015. Mycorrhizal type determines the magnitude and direction of root-induced changes in decomposition in a temperate forest. New Phytologist 206(4), 1274-1282. https://doi.org/10.1111/nph.13....
16.
Chen, G. C., Johnson, B. R., 1983. Improved colorimetric determination of cell wall chitin in wood decay fungi. Appl Environ Microbiol 46(1), 13-16. https://doi.org/10.1128/aem.46....
17.
Debode, J., De Tender, C., Soltaninejad, S., Van Malderghem, C., Haegeman, A., Van der Linden, I., Cottyn, B., Heyndrickx, M., Maes, M., 2016. Chitin Mixed in Potting Soil Alters Lettuce Growth, the Survival of Zoonotic Bacteria on the Leaves and Associated Rhizosphere Microbiology. Frontiers in Microbiology 7(565). https://doi.org/10.3389/fmicb.....
18.
Ekblad, A., Näsholm, T., 1996. Determination of chitin in fungi and mycorrhizal roots by an improved HPLC analysis of glucosamine. Plant and Soil 178(1), 29-35. https://doi.org/10.1007/BF0001....
19.
Ekblad, A., Wallander, H., Godbold, D. L., Cruz, C., Johnson, D., Baldrian, P., Björk, R. G., Epron, D., Kieliszewska-Rokicka, B., Kjøller, R., Kraigher, H., Matzner, E., Neumann, J., Plassard, C., 2013. The production and turnover of extramatrical mycelium of ectomycorrhizal fungi in forest soils: role in carbon cycling. Plant and Soil 366(1), 1-27. https://doi.org/10.1007/s11104....
20.
Fekete, I., Berki, I., Béni, Á., Balláné, K. A., Madarász, B., Várbíró, G., Makádi, M., Demeter, I., Juhos, K., 2020a. Carbon-sequestration of Hungarian zonal types of deciduous oak forest soils, studied with different annual precipitation values,. Talajvédelem (in Hungarian), 176-190.
21.
Fekete, I., Berki, I., Lajtha, K., Trumbore, S., Francioso, O., Gioacchini, P., Montecchio, D., Várbíró, G., Béni, Á., Makádi, M., Demeter, I., Madarász, B., Juhos, K., Kotroczó, Z., 2020b. How will a drier climate change carbon sequestration in soils of the deciduous forests of Central Europe? Biogeochemistry. https://doi.org/10.1007/s10533....
22.
Fekete, I., Halász, J., Kramoperger, Z.Krausz, E., 2008. Study of litter decomposition intensity in litter manipulative trials in síkfőkút cambisols. Cereal Research Communications 36, 1779-1782.
23.
Fekete, I., Lajtha, K., Kotroczó, Z., Várbíró, G., Varga, C., Tóth, J. A., Demeter, I., Veperdi, G., Berki, I., 2017. Long-term effects of climate change on carbon storage and tree species composition in a dry deciduous forest. Global Change Biology 23(8), 3154-3168. https://doi.org/10.1111/gcb.13....
24.
Fernandez, C. W., See, C. R., Kennedy, P. G., 2020. Decelerated carbon cycling by ectomycorrhizal fungi is controlled by substrate quality and community composition. New Phytologist 226(2), 569-582. https://doi.org/10.1111/nph.16....
25.
Frąc, M., Hannula, S. E., Bełka, M., Jędryczka, M., 2018. Fungal Biodiversity and Their Role in Soil Health. Frontiers in Microbiology 9(707). https://doi.org/10.3389/fmicb.....
26.
Frey, B., Vilarino, A., Schuepp, H., Arines, J., 1994. Chitin and ergosterol content of extraradical and intraradical mycelium of the vesicular-arbuscular mycorrhizal fungus Glomus intraradices. Soil Biology and Biochemistry 26(6), 711-717. https://doi.org/10.1016/0038-0....
27.
Fuentes, C., Saari, H., Choi, J., Lee, S., Sjöö, M., Wahlgren, M., Nilsson, L., 2019. Characterization of non-solvent precipitated starch using asymmetrical flow field-flow fractionation coupled with multiple detectors. Carbohydrate Polymers 206, 21-28. https://doi.org/10.1016/j.carb....
28.
González-Espinosa, Y., Sabagh, B., Moldenhauer, E., Clarke, P., Goycoolea, F. M., 2019. Characterisation of chitosan molecular weight distribution by multi-detection asymmetric flow-field flow fractionation (AF4) and SEC. International Journal of Biological Macromolecules 136, 911-919. https://doi.org/10.1016/j.ijbi....
29.
Gooday, G. W., 1990. The Ecology of Chitin Degradation. In: K. C. Marshall (Eds.), Advances in Microbial Ecology. Springer US, Boston, MA. 387-430.
30.
Goodell, B., Qian, Y., Jellison, J., 2008. Fungal Decay of Wood: Soft Rot-Brown Rot-White Rot. In: T. P. Schultz, H. Militz, M. H. Freeman, B. Goodell and D. D. Nicholas (Eds.), Development of Commercial Wood Preservatives. American Chemical Society, Washingthon, DC. 9-31.
31.
Guo, P., Li, Y., An, J., Shen, S., Dou, H., 2019. Study on structure-function of starch by asymmetrical flow field-flow fractionation coupled with multiple detectors: A review. Carbohydrate Polymers 226, 115330. https://doi.org/10.1016/j.carb....
32.
Hansson, K., Laclau, J.-P., Saint-André, L., Mareschal, L., van der Heijden, G., Nys, C., Nicolas, M., Ranger, J., Legout, A., 2020. Chemical fertility of forest ecosystems. Part 1: Common soil chemical analyses were poor predictors of stand productivity across a wide range of acidic forest soils. Forest Ecology and Management 461, 117843. https://doi.org/10.1016/j.fore....
33.
Jacquiod, S., Franqueville, L., Cécillon, S., M. Vogel, T., Simonet, P., 2013. Soil Bacterial Community Shifts after Chitin Enrichment: An Integrative Metagenomic Approach. Public Library of Science One 8(11), e79699. https://doi.org/10.1371/journa....
34.
Kotroczó, Z., Koncz, G., Halász, L. J., Fekete, I., Krakomperger, Z., Tóth, D. M., Balázsy, S., Tóth, J. A., 2009. Litter decomposition intensity and soil organic matter accumulation in síkfőkút dirt site. Acta Microbiologica et Immunologica Hungarica 56, 53-54. https://doi.org/10.1556/amicr.....
35.
Kyaschenko, J., Clemmensen, K. E., Karltun, E., Lindahl, B. D., 2017. Below-ground organic matter accumulation along a boreal forest fertility gradient relates to guild interaction within fungal communities. Ecology Letters 20(12), 1546-1555. https://doi.org/10.1111/ele.12....
36.
Lau, A. P. S., Lee, A. K. Y., Chan, C. K., Fang, M., 2006. Ergosterol as a biomarker for the quantification of the fungal biomass in atmospheric aerosols. Atmospheric Environment 40(2), 249-259. https://doi.org/10.1016/j.atmo....
37.
Li, N., Xu, Y.-Z., Han, X.-Z., He, H.-B., Zhang, X.-D., Zhang, B., 2015. Fungi contribute more than bacteria to soil organic matter through necromass accumulation under different agricultural practices during the early pedogenesis of a Mollisol. European Journal of Soil Biology 67, 51-58. https://doi.org/10.1016/j.ejso....
38.
Looby, C. I., Treseder, K. K., 2018. Shifts in soil fungi and extracellular enzyme activity with simulated climate change in a tropical montane cloud forest. Soil Biology and Biochemistry 117, 87-96. https://doi.org/10.1016/j.soil....
39.
Makádi, M., 2010: Microbiological properties of sandy soils in the Nyírség region (Hungary), affected by organic and inorganic additives (Ph.D dissertation). Szent István University, Gödöllő.
40.
Malik, M. I., Pasch, H., 2016. Field-flow fractionation: New and exciting perspectives in polymer analysis. Progress in Polymer Science 63, 42-85. https://doi.org/10.1016/j.prog....
41.
Mayer, M., Rewald, B., Matthews, B., Sandén, H., Rosinger, C., Katzensteiner, K., Gorfer, M., Berger, H., Tallian, C., Berger, T. W., Godbold, D. L., 2021. Soil fertility relates to fungal-mediated decomposition and organic matter turnover in a temperate mountain forest. New Phytologist 231(2), 777-790. https://doi.org/10.1111/nph.17....
42.
Medina, A., Probanza, A., Gutierrez Mañero, F. J., Azcón, R., 2003. Interactions of arbuscular-mycorrhizal fungi and Bacillus strains and their effects on plant growth, microbial rhizosphere activity (thymidine and leucine incorporation) and fungal biomass (ergosterol and chitin). Applied Soil Ecology 22(1), 15-28. https://doi.org/10.1016/S0929-....
43.
Nilsson, K., Bjurman, J., 1998. Chitin as an indicator of the biomass of two wood-decay fungi in relation to temperature, incubation time, and media composition. Canadian Journal of Microbiology 44(6), 575-581. https://doi.org/10.1139/w98-03....
44.
Olsson, P. A., Larsson, L., Bago, B., Wallander, H., Van Aarle, I. M., 2003. Ergosterol and fatty acids for biomass estimation of mycorrhizal fungi. New Phytologist 159(1), 7-10. https://doi.org/10.1046/j.1469....
45.
Ravi Kumar, M. N. V., 2000. A review of chitin and chitosan applications. Reactive and Functional Polymers 46(1), 1-27. https://doi.org/10.1016/S1381-....
46.
Sharp, R. G., 2013. A Review of the Applications of Chitin and Its Derivatives in Agriculture to Modify Plant-Microbial Interactions and Improve Crop Yields. Agronomy 3, 757-793. https://doi.org/10.3390/agrono....
47.
Simpson, R. T., Frey, S. D., Six, J., Thiet, R. K., 2004. Preferential Accumulation of Microbial Carbon in Aggregate Structures of No-Tillage Soils. Soil Science Society of America Journal 68(4), 1249-1255. https://doi.org/10.2136/sssaj2....
48.
Stahl, P. D., Parkin, T. B., 1996. Relationship of soil ergosterol concentration and fungal biomass. Soil Biology and Biochemistry 28(7), 847-855. https://doi.org/10.1016/0038-0....
49.
Steffen, K. T., Cajthaml, T., Šnajdr, J., Baldrian, P., 2007. Differential degradation of oak (Quercus petraea) leaf litter by litter-decomposing basidiomycetes. Research in Microbiology 158(5), 447-455. https://doi.org/10.1016/j.resm....
50.
Sun, J.-M., Irzykowski, W., Jedryczka, M., Han, F.-X., 2005. Analysis of the Genetic Structure of Sclerotinia sclerotiorum (Lib.) de Bary Populations from Different Regions and Host Plants by Random Amplified Polymorphic DNA Markers. Journal of Integrative Plant Biology 47(4), 385-395. https://doi.org/10.1111/j.1744....
51.
Świtoniak, M., Novák, T. J., Charzyński, P., Zalewska, K., Bednarek, R., 2014. Forested hilly landscape of Bükkalja Foothill (Hungary). In: M. Świtoniak and P. Charzyński (Eds.), Soil sequences atlas. Nicolaus Copernicus University Press, Torun. 169–181.
52.
Teste, F. P., Laliberté, E., Lambers, H., Auer, Y., Kramer, S., Kandeler, E., 2016. Mycorrhizal fungal biomass and scavenging declines in phosphorus-impoverished soils during ecosystem retrogression. Soil Biology and Biochemistry 92, 119-132. https://doi.org/10.1016/j.soil....
53.
Voříšková, J., Brabcová, V., Cajthaml, T., Baldrian, P., 2014. Seasonal dynamics of fungal communities in a temperate oak forest soil. New Phytologist 201(1), 269-278. https://doi.org/10.1111/nph.12....
54.
Wallander, H., Ekblad, A., Godbold, D. L., Johnson, D., Bahr, A., Baldrian, P., Björk, R. G., Kieliszewska-Rokicka, B., Kjøller, R., Kraigher, H., Plassard, C., Rudawska, M., 2013. Evaluation of methods to estimate production, biomass and turnover of ectomycorrhizal mycelium in forests soils – A review. Soil Biology and Biochemistry 57, 1034-1047. https://doi.org/10.1016/j.soil....
55.
Wang, B., An, S., Liang, C., Liu, Y., Kuzyakov, Y., 2021a. Microbial necromass as the source of soil organic carbon in global ecosystems. Soil Biology and Biochemistry 162, 108422. https://doi.org/10.1016/j.soil....
56.
Wang, B., Liang, C., Yao, H., Yang, E., An, S., 2021b. The accumulation of microbial necromass carbon from litter to mineral soil and its contribution to soil organic carbon sequestration. CATENA 207, 105622. https://doi.org/10.1016/j.cate....
57.
Weil, R. R., Brady, N. C., 2017. The Nature and Properties of Soils (15th Edition) Pearson Education, London.
58.
Yeul, V. S., Rayalu, S. S., 2013. Unprecedented Chitin and Chitosan: A Chemical Overview. Journal of Polymers and the Environment 21(2), 606-614. https://doi.org/10.1007/s10924....
59.
Zhang, X., Dai, G., Ma, T., Liu, N., Hu, H., Ma, W., Zhang, J.-B., Wang, Z., Peterse, F., Feng, X., 2020. Links between microbial biomass and necromass components in the top- and subsoils of temperate grasslands along an aridity gradient. Geoderma 379, 114623. https://doi.org/10.1016/j.geod....
| eISSN: | 2300-4975 |
| ISSN: | 2300-4967 |
We process personal data collected when visiting the website. The function of obtaining information about users and their behavior is carried out by voluntarily entered information in forms and saving cookies in end devices. Data, including cookies, are used to provide services, improve the user experience and to analyze the traffic in accordance with the Privacy policy. Data are also collected and processed by Google Analytics tool (more).
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
