Revisiting soil fungal biomarkers and conversion factors: Interspecific variability in phospholipid fatty acids, ergosterol and rDNA copy numbers

Tessa Camenzind , Heike Haslwimmer , Matthias C. Rillig , Liliane Ruess , Damien R. Finn , Christoph C. Tebbe , Stefan Hempel , Sven Marhan

Soil Ecology Letters ›› 2024, Vol. 6 ›› Issue (4) : 240243

PDF (2880KB)
Soil Ecology Letters ›› 2024, Vol. 6 ›› Issue (4) : 240243 DOI: 10.1007/s42832-024-0243-5
RESEARCH ARTICLE

Revisiting soil fungal biomarkers and conversion factors: Interspecific variability in phospholipid fatty acids, ergosterol and rDNA copy numbers

Author information +
History +
PDF (2880KB)

Abstract

The abundances of fungi and bacteria in soil are used as simple predictors for carbon dynamics, and represent widely available microbial traits. Soil biomarkers serve as quantitative estimates of these microbial groups, though not quantifying microbial biomass per se. The accurate conversion to microbial carbon pools, and an understanding of its comparability among soils is therefore needed. We refined conversion factors for classical fungal biomarkers, and evaluated the application of quantitative PCR (qPCR, rDNA copies) as a biomarker for soil fungi. Based on biomarker contents in pure fungal cultures of 30 isolates tested here, combined with comparable published datasets, we propose average conversion factors of 95.3 g fungal C g−1 ergosterol, 32.0 mg fungal C µmol−1 PLFA 18:2ω6,9 and 0.264 pg fungal C ITS1 DNA copy−1. As expected, interspecific variability was most pronounced in rDNA copies, though qPCR results showed the least phylogenetic bias. A modeling approach based on exemplary agricultural soils further supported the hypothesis that high diversity in soil buffers against biomarker variability, whereas also phylogenetic biases impact the accuracy of comparisons in biomarker estimates. Our analyses suggest that qPCR results cover the fungal community in soil best, though with a variability only partly offset in highly diverse soils. PLFA 18:2ω6,9 and ergosterol represent accurate biomarkers to quantify Ascomycota and Basidiomycota. To conclude, the ecological interpretation and coverage of biomarker data prior to their application in global models is important, where the combination of different biomarkers may be most insightful.

Graphical abstract

Keywords

soil fungal biomarkers / biomarker conversion factors / saprobic fungi / ITS copy numbers / ergosterol / phospholipid fatty acids

Highlight

● Refined conversion factors for soil fungal biomarkers are proposed.

● High interspecific variability is present in all fungal biomarkers.

● A modeling approach supports the validity of biomarker estimates in diverse soils.

● ITS1 copies vary strongly, but are fungal-specific with least phylogenetic bias.

● A combination of fungal biomarkers will reveal soil fungal physiology and activity.

Cite this article

Download citation ▾
Tessa Camenzind, Heike Haslwimmer, Matthias C. Rillig, Liliane Ruess, Damien R. Finn, Christoph C. Tebbe, Stefan Hempel, Sven Marhan. Revisiting soil fungal biomarkers and conversion factors: Interspecific variability in phospholipid fatty acids, ergosterol and rDNA copy numbers. Soil Ecology Letters, 2024, 6(4): 240243 DOI:10.1007/s42832-024-0243-5

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Andrade-Linares, D.R., Veresoglou, S.D., Rillig, M.C., 2016. Temperature priming and memory in soil filamentous fungi. Fungal Ecology21, 10–15.

[2]

Anthony, M.A., Bender, S.F., van der Heijden, M.G.A., 2023. Enumerating soil biodiversity. Proceedings of the National Academy of Sciences of the United States of America120, e2304663120.

[3]

Antibus, R.K., Sinsabaugh, R.L., 1993. The extraction and quantification of ergosterol from ectomycorrhizal fungi and roots. Mycorrhiza3, 137–144.

[4]

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 Ecology6, 1–11.

[5]

Bar-On, Y.M., Phillips, R., Milo, R., 2018. The biomass distribution on Earth. Proceedings of the National Academy of Sciences of the United States of America115, 6506–6511.

[6]

Barajas-Aceves, M., Hassan, M., Tinoco, R., Vazquez-Duhalt, R., 2002. Effect of pollutants on the ergosterol content as indicator of fungal biomass. Journal of Microbiological Methods50, 227–236.

[7]

Brondz, I., Høiland, K., Ekeberg, D., 2004. Multivariate analysis of fatty acids in spores of higher basidiomycetes: a new method for chemotaxonomical classification of fungi. Journal of Chromatography B800, 303–307.

[8]

Camenzind, T., Mason-Jones, K., Mansour, I., Rillig, M.C., Lehmann, J., 2023. Formation of necromass-derived soil organic carbon determined by microbial death pathways. Nature Geoscience16, 115–122.

[9]

Camenzind, T., Philipp Grenz, K., Lehmann, J., Rillig, M.C., 2021. Soil fungal mycelia have unexpectedly flexible stoichiometric C:N and C:P ratios. Ecology Letters24, 208–218.

[10]

Camenzind, T., Weimershaus, P., Lehmann, A., Aguilar-Trigueros, C., Rillig, M.C., 2022. Soil fungi invest into asexual sporulation under resource scarcity, but trait spaces of individual isolates are unique. Environmental Microbiology24, 2962–2978.

[11]

Canarini, A., Fuchslueger, L., Schnecker, J., Metze, D., Nelson, D.B., Kahmen, A., Watzka, M., Pötsch, E.M., Schaumberger, A., Bahn, M., Richter, A., 2023. Soil fungi remain active and invest in storage compounds during drought independent of future climate conditions. bioRxiv, DOI: 10.1101/2023.10.23.563577

[12]

Charcosset, J.Y., Chauvet, E., 2001. Effect of culture conditions on ergosterol as an indicator of biomass in the aquatic hyphomycetes. Applied and Environmental Microbiology67, 2051–2055.

[13]

Chen, C., Chen, X.L., Chen, H.Y.H., 2023. Mapping N deposition impacts on soil microbial biomass across global terrestrial ecosystems. Geoderma433, 116429.

[14]

Crowther, T.W., van den Hoogen, J., Wan, J., Mayes, M.A., Keiser, A.D., Mo, L., Averill, C., Maynard, D.S., 2019. The global soil community and its influence on biogeochemistry. Science365, eaav0550.

[15]

Delmont, T.O., Prestat, E., Keegan, K.P., Faubladier, M., Robe, P., Clark, I.M., Pelletier, E., Hirsch, P.R., Meyer, F., Gilbert, J.A., Le Paslier, D., Simonet, P., Vogel, T.M., 2012. Structure, fluctuation and magnitude of a natural grassland soil metagenome. The ISME Journal6, 1677–1687.

[16]

Djajakirana, G., Joergensen, R.G., Meyer, B., 1996. Ergosterol and microbial biomass relationship in soil. Biology and Fertility of Soils22, 299–304.

[17]

Domsch, K.H., Gams, W., Anderson, T.H., 2007. Compendium of Soil Fungi. 2nd ed. Eching: IHW-Verlag

[18]

Ekblad, A., Mikusinska, A., Ågren, G.I., Menichetti, L., Wallander, H., Vilgalys, R., Bahr, A., Eriksson, U., 2016. Production and turnover of ectomycorrhizal extramatrical mycelial biomass and necromass under elevated CO2 and nitrogen fertilization. New Phytologist211, 874–885.

[19]

Federle, T.W., 1986. Microbial Distribution in Soil - New Techniques. In: Megusar, F., Gantar, M., eds. Perspectives in Microbial Ecology. Ljulbljana: Slovene Society for Microbiology, 493–498

[20]

Fierer, N., Jackson, J.A., Vilgalys, R., Jackson, R.B., 2005. Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Applied and Environmental Microbiology71, 4117–4120.

[21]

Frostegård, Å., Bååth, E., 1996. The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biology and Fertility of Soils22, 59–65.

[22]

Frostegård, Å., Tunlid, A., Bååth, E., 1991. Microbial biomass measured as total lipid phosphate in soils of different organic content. Journal of Microbiological Methods14, 151–163.

[23]

Frostegård, Å., Tunlid, A., Bååth, E., 1993. Phospholipid fatty-acid composition, biomass and activity of microbial communities from two soil types experimentally exposed to different heavy-metals. Applied and Environmental Microbiology59, 3605–3617.

[24]

Frostegård, Å., Tunlid, A., Bååth, E., 2011. Use and misuse of PLFA measurements in soils. Soil Biology & Biochemistry43, 1621–1625.

[25]

Gorka, S., Darcy, S., Horak, J., Imai, B., Mohrlok, M., Salas, E., Richter, A., Schmidt, H., Wanek, W., Kaiser, C., Canarini, A., 2023. Beyond PLFA: concurrent extraction of neutral and glycolipid fatty acids provides new insights into soil microbial communities. Soil Biology and Biochemistry187, 109205.

[26]

Green, C.T., Scow, K.M., 2000. Analysis of phospholipid fatty acids (PLFA) to characterize microbial communities in aquifers. Hydrogeology Journal8, 126–141.

[27]

Grimmett, I.J., Shipp, K.N., Macneil, A., Bärlocher, F., 2013. Does the growth rate hypothesis apply to aquatic hyphomycetes? Fungal Ecology 6, 493–500

[28]

He, L.Y., Lipson, D.A., Mazza Rodrigues, J.L., Mayes, M., Björk, R.G., Glaser, B., Thornton, P., Xu, X.F., 2021. Dynamics of fungal and bacterial biomass carbon in natural ecosystems: site-level applications of the CLM-microbe model. Journal of Advances in Modeling Earth Systems13, e2020MS002283.

[29]

Heaton, L.L.M., Jones, N.S., Fricker, M.D., 2016. Energetic constraints on fungal growth. The American Naturalist187, E27–E40.

[30]

Hsieh, C.W.C., Cannella, D., Jørgensen, H., Felby, C., Thygesen, L.G., 2014. Cellulase inhibition by high concentrations of monosaccharides. Journal of Agricultural and Food Chemistry62, 3800–3805.

[31]

Hungate, B.A., Mau, R.L., Schwartz, E., Caporaso, J.G., Dijkstra, P., van Gestel, N., Koch, B.J., Liu, C.M., McHugh, T.A., Marks, J.C., Morrissey, E.M., Price, L.B., 2015. Quantitative microbial ecology through stable isotope probing. Applied and Environmental Microbiology81, 7570–7581.

[32]

Joergensen, R.G., 2018. Amino sugars as specific indices for fungal and bacterial residues in soil. Biology and Fertility of Soils54, 559–568.

[33]

Joergensen, R.G., 2022. Phospholipid fatty acids in soil—drawbacks and future prospects. Biology and Fertility of Soils58, 1–6.

[34]

Joergensen, R.G., Emmerling, C., 2006. Methods for evaluating human impact on soil microorganisms based on their activity, biomass, and diversity in agricultural soils. Journal of Plant Nutrition and Soil Science169, 295–309.

[35]

Joergensen, R.G., Wichern, F., 2008. Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biology and Biochemistry40, 2977–2991.

[36]

Junicke, H., Abbas, B., Oentoro, J., van Loosdrecht, M., Kleerebezem, R., 2014. Absolute quantification of individual biomass concentrations in a methanogenic coculture. AMB Express4, 35.

[37]

Keck, F., Rimet, F., Bouchez, A., Franc, A., 2016. phylosignal: an R package to measure, test, and explore the phylogenetic signal. Ecology and Evolution6, 2774–2780.

[38]

Klamer, M., Bååth, E., 2004. Estimation of conversion factors for fungal biomass determination in compost using ergosterol and PLFA 18:2ω6,9. Soil Biology and Biochemistry36, 57–65.

[39]

Klein, D.A., Paschke, M.W., 2004. Filamentous fungi: the indeterminate lifestyle and microbial ecology. Microbial Ecology47, 224–235.

[40]

Kramer, S., Dibbern, D., Moll, J., Huenninghaus, M., Koller, R., Krueger, D., Marhan, S., Urich, T., Wubet, T., Bonkowski, M., Buscot, F., Lueders, T., Kandeler, E., 2016. Resource partitioning between bacteria, fungi, and protists in the detritusphere of an agricultural soil. Frontiers in Microbiology7, 1524.

[41]

Lavrinienko, A., Jernfors, T., Koskimäki, J.J., Pirttilä, A.M., Watts, P.C., 2021. Does intraspecific variation in rDNA copy number affect analysis of microbial communities? Trends in Microbiology 29, 19–27

[42]

Leckie, S.E., Prescott, C.E., Grayston, S.J., Neufeld, J.D., Mohn, W.W., 2004. Comparison of chloroform fumigation-extraction, phospholipid fatty acid, and DNA methods to determine microbial biomass in forest humus. Soil Biology and Biochemistry36, 529–532.

[43]

Lehmann, A., Zheng, W.S., Soutschek, K., Roy, J., Yurkov, A.M., Rillig, M.C., 2019. Tradeoffs in hyphal traits determine mycelium architecture in saprobic fungi. Scientific Reports9, 14152.

[44]

Lewe, N., Hermans, S., Lear, G., Kelly, L.T., Thomson-Laing, G., Weisbrod, B., Wood, S.A., Keyzers, R.A., Deslippe, J.R., 2021. Phospholipid fatty acid (PLFA) analysis as a tool to estimate absolute abundances from compositional 16S rRNA bacterial metabarcoding data. Journal of Microbiological Methods188, 106271.

[45]

Li, J., Wang, X., Wu, J.H., Sun, Y.X., Zhang, Y.Y., Zhao, Y.F., Huang, Z., Duan, W.H., 2023. Climate and geochemistry at different altitudes influence soil fungal community aggregation patterns in alpine grasslands. Science of the Total Environment881, 163375.

[46]

Liang, C., Amelung, W., Lehmann, J., Kästner, M., 2019. Quantitative assessment of microbial necromass contribution to soil organic matter. Global Change Biology25, 3578–3590.

[47]

Lofgren, L.A., Uehling, J.K., Branco, S., Bruns, T.D., Martin, F., Kennedy, P.G., 2019. Genome-based estimates of fungal rDNA copy number variation across phylogenetic scales and ecological lifestyles. Molecular Ecology28, 721–730.

[48]

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.

[49]

Manerkar, M.A., Seena, S., Bärlocher, F., 2008. Q-RT-PCR for assessing archaea, bacteria, and fungi during leaf decomposition in a stream. Microbial Ecology56, 467–473.

[50]

Mason-Jones, K., Breidenbach, A., Dyckmans, J., Banfield, C.C., Dippold, M.A., 2023. Intracellular carbon storage by microorganisms is an overlooked pathway of biomass growth. Nature Communications14, 2240.

[51]

Miltner, A., Bombach, P., Schmidt-Brücken, B., Kästner, M., 2012. SOM genesis: microbial biomass as a significant source. Biogeochemistry111, 41–55.

[52]

Moore, D., Robson, G., Trinci, A., 2021. 21st Century Guidebook to Fungi. 2nd ed. Cambridge: Cambridge University Press

[53]

Mouginot, C., Kawamura, R., Matulich, K.L., Berlemont, R., Allison, S.D., Amend, A.S., Martiny, A.C., 2014. Elemental stoichiometry of Fungi and Bacteria strains from grassland leaf litter. Soil Biology and Biochemistry76, 278–285.

[54]

Ngosong, C., Gabriel, E., Ruess, L., 2012. Use of the signature Fatty Acid 16:1ω5 as a tool to determine the distribution of arbuscular mycorrhizal fungi in soil. Journal of Lipids2012, 236807.

[55]

Niemenmaa, O., Galkin, S., Hatakka, A., 2008. Ergosterol contents of some wood-rotting basidiomycete fungi grown in liquid and solid culture conditions. International Biodeterioration & Biodegradation62, 125–134.

[56]

Nisha, A., Rastogi, N.K., Venkateswaran, G., 2011. Optimization of media components for enhanced arachidonic acid production by Mortierella alpina under submerged cultivation. Biotechnology and Bioprocess Engineering16, 229–237.

[57]

Nuccio, E.E., Blazewicz, S.J., Lafler, M., Campbell, A.N., Kakouridis, A., Kimbrel, J.A., Wollard, J., Vyshenska, D., Riley, R., Tomatsu, A., Hestrin, R., Malmstrom, R.R., Firestone, M., Pett-Ridge, J., 2022. HT-SIP: a semi-automated stable isotope probing pipeline identifies cross-kingdom interactions in the hyphosphere of arbuscular mycorrhizal fungi. Microbiome10, 199.

[58]

Nurika, I., Eastwood, D.C., Barker, G.C., 2018. A comparison of ergosterol and PLFA methods for monitoring the growth of ligninolytic fungi during wheat straw solid state cultivation. Journal of Microbiological Methods148, 49–54.

[59]

Olsson, P.A., Johansen, A., 2000. Lipid and fatty acid composition of hyphae and spores of arbuscular mycorrhizal fungi at different growth stages. Mycological Research104, 429–434.

[60]

Osburn, E.D., McBride, S.G., Kupper, J.V., Nelson, J.A., McNear, D.H., McCulley, R.L., Barrett, J.E., 2022. Accurate detection of soil microbial community responses to environmental change requires the use of multiple methods. Soil Biology and Biochemistry169, 108685.

[61]

Parikh, S.J., James, B.R., 2012. Soil: the foundation of agriculture. Nature Education Knowledge3, 2.

[62]

Pasanen, A.L., Yli-Pietila, K., Pasanen, P., Kalliokoski, P., Tarhanen, J., 1999. Ergosterol content in various fungal species and biocontaminated building materials. Applied and Environmental Microbiology65, 138–142.

[63]

Pawłowska, J., Okrasińska, A., Kisło, K., Aleksandrzak-Piekarczyk, T., Szatraj, K., Dolatabadi, S., Muszewska, A., 2019. Carbon assimilation profiles of mucoralean fungi show their metabolic versatility. Scientific Reports9, 11864.

[64]

Pérez-Guzmán, L., Phillips, L.A., Acevedo, M.A., Acosta-Martínez, V., 2021. Comparing biological methods for soil health assessments: EL-FAME, enzyme activities, and qPCR. Soil Science Society of America Journal85, 636–653.

[65]

Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., R Core Team, 2021. nlme: linear and nonlinear mixed effects models. R package version 3.1–152, available at the website CRAN. R-project

[66]

Pusztahelyi, T., Molnár, Z., Emri, T., Klement, É., Miskei, M., Kerékgyártó, J., Balla, J., Pócsi, I., 2006. Comparative studies of differential expression of chitinolytic enzymes encoded by chiA, chiB, chiC and nagA genes in Aspergillus nidulans. Folia Microbiologica51, 547–554.

[67]

R Core Team, 2021. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing

[68]

Ruess, L., Chamberlain, P.M., 2010. The fat that matters: Soil food web analysis using fatty acids and their carbon stable isotope signature. Soil Biology and Biochemistry42, 1898–1910.

[69]

Ruess, L., Häggblom, M.M., Garcı́a Zapata, E.J., Dighton, J., 2002. Fatty acids of fungi and nematodes—possible biomarkers in the soil food chain? Soil Biology and Biochemistry 34, 745–756

[70]

Ruess, L., Schütz, K., Migge-Kleian, S., Häggblom, M.M., Kandeler, E., Scheu, S., 2007. Lipid composition of Collembola and their food resources in deciduous forest stands—Implications for feeding strategies. Soil Biology and Biochemistry39, 1990–2000.

[71]

Sae-Tun, O., Maftukhah, R., Noller, C., Remlinger, V.I., Meyer-Laker, V., Sørensen, A.C.T., Sustic, D., Socianu, S.I., Bernardini, L.G., Mentler, A., Keiblinger, K.M., 2020. Comparison of commonly used extraction methods for ergosterol in soil samples. International Agrophysics34, 425–432.

[72]

Schliep, K.P., 2011. phangorn: phylogenetic analysis in R. Bioinformatics27, 592–593.

[73]

Song, Z.W., Vail, A., Sadowsky, M.J., Schilling, J.S., 2014. Quantitative PCR for measuring biomass of decomposer fungi in planta. Fungal Ecology7, 39–46.

[74]

Stahl, P.D., Klug, M.J., 1996. Characterization and differentiation of filamentous fungi based on fatty acid composition. Applied and Environmental Microbiology62, 4136–4146.

[75]

Stahl, P.D., Parkin, T.B., Eash, N.S., 1995. Sources of error in direct microscopic methods for estimation of fungal biomass in soil. Soil Biology and Biochemistry27, 1091–1097.

[76]

Sterner, R.W., Elser, J.J., 2002. Ecological Stoichiometry: the Biology of Elements from Molecules to the Biosphere. Princeton: Princeton University Press

[77]

Stigler, S.M., 1997. Regression towards the mean, historically considered. Statistical Methods in Medical Research6, 103–114.

[78]

Strickland, M.S., Rousk, J., 2010. Considering fungal: bacterial dominance in soils - Methods, controls, and ecosystem implications. Soil Biology and Biochemistry42, 1385–1395.

[79]

Taube, R., Fabian, J., Van den Wyngaert, S., Agha, R., Baschien, C., Gerphagnon, M., Kagami, M., Krüger, A., Premke, K., 2019. Potentials and limitations of quantification of fungi in freshwater environments based on PLFA profiles. Fungal Ecology41, 256–268.

[80]

Tedersoo, L., Anslan, S., Bahram, M., Drenkhan, R., Pritsch, K., Buegger, F., Padari, A., Hagh-Doust, N., Mikryukov, V., Gohar, D., Amiri, R., Hiiesalu, I., Lutter, R., Rosenvald, R., Rähn, E., Adamson, K., Drenkhan, T., Tullus, H., Jürimaa, K., Sibul, I., Otsing, E., Põlme, S., Metslaid, M., Loit, K., Agan, A., Puusepp, R., Varik, I., Kõljalg, U., Abarenkov, K., 2020. Regional-scale in-depth analysis of soil fungal diversity reveals strong pH and plant species effects in northern Europe. Frontiers in Microbiology11, 1953.

[81]

Tedersoo, L., Mikryukov, V., Zizka, A., Bahram, M., Hagh-Doust, N., Anslan, S., Prylutskyi, O., Delgado-Baquerizo, M., Maestre, F.T., Pärn, J., Öpik, M., Moora, M., Zobel, M., Espenberg, M., Mander, Ü., Khalid, A.N., Corrales, A., Agan, A., Vasco-Palacios, A.M., Saitta, A., Rinaldi, A.C., Verbeken, A., Sulistyo, B.P., Tamgnoue, B., Furneaux, B., Ritter, C.D., Nyamukondiwa, C., Sharp, C., Marín, C., Gohar, D., Klavina, D., Sharmah, D., Dai, D.Q., Nouhra, E., Biersma, E.M., Rähn, E., Cameron, E.K., De Crop, E., Otsing, E., Davydov, E.A., Albornoz, F.E., Brearley, F.Q., Buegger, F., Zahn, G., Bonito, G., Hiiesalu, I., Barrio, I.C., Heilmann-Clausen, J., Ankuda, J., Kupagme, J.Y., Maciá-Vicente, J.G., Fovo, J.D., Geml, J., Alatalo, J.M., Alvarez-Manjarrez, J., Põldmaa, K., Runnel, K., Adamson, K., Bråthen, K.A., Pritsch, K., Tchan, K.I., Armolaitis, K., Hyde, K.D., Newsham, K.K., Panksep, K., Lateef, A.A., Tiirmann, L., Hansson, L., Lamit, L.J., Saba, M., Tuomi, M., Gryzenhout, M., Bauters, M., Piepenbring, M., Wijayawardene, N., Yorou, N.S., Kurina, O., Mortimer, P.E., Meidl, P., Kohout, P., Nilsson, R.H., Puusepp, R., Drenkhan, R., Garibay-Orijel, R., Godoy, R., Alkahtani, S., Rahimlou, S., Dudov, S.V., Põlme, S., Ghosh, S., Mundra, S., Ahmed, T., Netherway, T., Henkel, T.W., Roslin, T., Nteziryayo, V., Fedosov, V.E., Onipchenko, V.G., Yasanthika, W.A.E., Lim, Y.W., Soudzilovskaia, N.A., Antonelli, A., Kõljalg, U., Abarenkov, K., 2022. Global patterns in endemicity and vulnerability of soil fungi. Global Change Biology28, 6696–6710.

[82]

Thijs, S., Op De Beeck, M., Beckers, B., Truyens, S., Stevens, V., Van Hamme, J.D., Weyens, N., Vangronsveld, J., 2017. Comparative evaluation of four bacteria-specific primer pairs for 16S rRNA gene surveys. Frontiers in Microbiology8, 494.

[83]

Thorn, R.G., Reddy, C.A., Harris, D., Paul, E.A., 1996. Isolation of saprophytic basidiomycetes from soil. Applied and Environmental Microbiology62, 4288–4292.

[84]

Van der Westhuizen, J.P.J., Kock, J.L.F., Botha, A., Botes, P.J., 1994. The distribution of the ω3- and ω6-series of cellular long-chain fatty acids in fungi. Systematic and Applied Microbiology17, 327–345.

[85]

Venables, W.N., Ripley, B.D., 2002. Modern Applied Statistics with S. 4th ed. New York: Springer

[86]

Vestal, J.R., White, D.C., 1989. Lipid analysis in microbial ecology: quantitative approaches to the study of microbial communities. BioScience39, 535–541.

[87]

Větrovský, T., Baldrian, P., 2013. The variability of the 16S rRNA gene in bacterial genomes and its consequences for bacterial community analyses. PLoS One8, e57923.

[88]

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 Biochemistry57, 1034–1047.

[89]

Wang, S.N., Cheng, J.K., Li, T., Liao, Y.C., 2020. Response of soil fungal communities to continuous cropping of flue-cured tobacco. Scientific Reports10, 19911.

[90]

Weete, J.D., 1980. Lipid Biochemistry of Fungi and Other Organisms. New York: Springer

[91]

Weete, J.D., Abril, M., Blackwell, M., 2010. Phylogenetic distribution of fungal sterols. PLoS One5, e10899.

[92]

White, T.J., Bruns, T., Lee, S., Taylor, J., 1990. Amplification and direct sequencing of fungal ribosomal rna genes for phylogenetics. In: Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T.J., eds. PCR Protocols: A Guide to Methods and Applications. San Diego: Academic Press, pp. 315–322

[93]

Willers, C., van Rensburg, P.J.J., Claassens, S., 2015. Phospholipid fatty acid profiling of microbial communities–a review of interpretations and recent applications. Journal of Applied Microbiology119, 1207–1218.

[94]

Wright, E.S., 2016. Using DECIPHER v2.0 to Analyze Big Biological Sequence Data in R. The R Journal 8, 352–359

[95]

Yu, K.L., van den Hoogen, J., Wang, Z.Q., Averill, C., Routh, D., Smith, G.R., Drenovsky, R.E., Scow, K.M., Mo, F., Waldrop, M.P., Yang, Y.H., Tang, W.Z., De Vries, F.T., Bardgett, R.D., Manning, P., Bastida, F., Baer, S.G., Bach, E.M., García, C., Wang, Q.K., Ma, L.N., Chen, B.D., He, X.J., Teurlincx, S., Heijboer, A., Bradley, J.A., Crowther, T.W., 2022. The biogeography of relative abundance of soil fungi versus bacteria in surface topsoil. Earth System Science Data14, 4339–4350.

[96]

Zelles, L., 1997. Phospholipid fatty acid profiles in selected members of soil microbial communities. Chemosphere35, 275–294.

[97]

Zhang, Z.J., Qu, Y.Y., Li, S.Z., Feng, K., Wang, S., Cai, W.W., Liang, Y.T., Li, H., Xu, M.Y., Yin, H.Q., Deng, Y., 2017. Soil bacterial quantification approaches coupling with relative abundances reflecting the changes of taxa. Scientific Reports7, 4837.

[98]

Zheng, W.S., Lehmann, A., Ryo, M., Vályi, K.K., Rillig, M.C., 2020. Growth rate trades off with enzymatic investment in soil filamentous fungi. Scientific Reports10, 11013.

RIGHTS & PERMISSIONS

The Author(s) 2024. This article is published with open access at link.springer.com and journal.hep.com.cn

AI Summary AI Mindmap
PDF (2880KB)

Supplementary files

SEL-00243-OF-TC_suppl_1

SEL-00243-OF-TC_suppl_2

653

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/