Variation of carbon, nitrogen and phosphorus content in fungi reflects their ecology and phylogeny
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
38835487
PubMed Central
PMC11148331
DOI
10.3389/fmicb.2024.1379825
Knihovny.cz E-zdroje
- Klíčová slova
- ecological traits, fungal biomass composition, nutrient content variation, nutrient stoichiometry, phylogenetic signal,
- Publikační typ
- časopisecké články MeSH
Fungi are an integral part of the nitrogen and phosphorus cycling in trophic networks, as they participate in biomass decomposition and facilitate plant nutrition through root symbioses. Nutrient content varies considerably between the main fungal habitats, such as soil, plant litter or decomposing dead wood, but there are also large differences within habitats. While some soils are heavily loaded with N, others are limited by N or P. One way in which nutrient availability can be reflected in fungi is their content in biomass. In this study, we determined the C, N, and P content (in dry mass) of fruiting bodies of 214 fungal species to inspect how phylogeny and membership in ecological guilds (soil saprotrophs, wood saprotrophs, and ectomycorrhizal fungi) affect the nutrient content of fungal biomass. The C content of fruiting bodies (415 ± 25 mg g-1) showed little variation (324-494 mg g-1), while the range of N (46 ± 20 mg g-1) and P (5.5 ± 3.0 mg g-1) contents was within one order of magnitude (8-103 mg g-1 and 1.0-18.9 mg g-1, respectively). Importantly, the N and P contents were significantly higher in the biomass of soil saprotrophic fungi compared to wood saprotrophic and ectomycorrhizal fungi. While the average C/N ratio in fungal biomass was 11.2, values exceeding 40 were recorded for some fungi living on dead wood, typically characterized by low N content. The N and P content of fungal mycelium also showed a significant phylogenetic signal, with differences in nutrient content being relatively low within species and genera of fungi. A strong correlation was found between N and P content in fungal biomass, while the correlation of N content and the N-containing fungal cell wall biopolymer-chitin showed only weak significance. The content of macronutrients in fungal biomass is influenced by the fungal life style and nutrient availability and is also limited by phylogeny.
Institute of Geology of the Czech Academy of Sciences Prague Czechia
Mycology and Microbiology Center University of Tartu Tartu Estonia
Natural Resources Institute Finland Helsinki Finland
Nuclear Physiscs Institute of the Czech Academy of Sciences Husinec Řež Czechia
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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 Biol. Biochem. 149:107932. 10.1016/j.soilbio.2020.107932 DOI
Bai Z., Ye J., Wei Y. L., Yan S. K., Yuan H. S. (2021). Soil depth-dependent C/N stoichiometry and fungal and bacterial communities along a temperate forest succession gradient. Catena 207:105613. 10.1016/j.catena.2021.105613 DOI
Baldrian P., Bell-Dereske L., Lepinay C., Větrovský T., Kohout P. (2022). Fungal communities in soils under global change. Stud. Mycol. 103 1–24. 10.3114/sim.2022.103.01 PubMed DOI PMC
Baldrian P., López-Mondéjar R., Kohout P. (2023). Forest microbiome and global change. Nat. Rev. Microbiol. 21 487–501. 10.1038/s41579-023-00876-4 PubMed DOI
Batjes N. H. (1996). Total carbon and nitrogen in the soils of the world. Eur. J. Soil Sci. 47 151–163. 10.1111/j.1365-2389.1996.tb01386.x DOI
Blumenthal H. J., Saul R. (1957). Quantitative estimation of chitin in fungi. J. Bacteriol. 74 222–224. 10.1128/jb.74.2.222-224.1957 PubMed DOI PMC
Bödeker I., Lindahl B., Olson A., Clemmensen K. (2016). Mycorrhizal and saprotrophic fungal guilds compete for the same organic substrates but affect decomposition differently. Funct. Ecol. 30 1967–1978. 10.1111/1365-2435.12677 DOI
Brabcová V., Štursová M., Baldrian P. (2018). Nutrient content affects the turnover of fungal biomass in forest topsoil and the composition of associated microbial communities. Soil Biol. Biochem. 118 187–198. 10.1016/j.soilbio.2017.12.012 DOI
Camenzind T., Lehmann A., Ahland J., Rumpel S., Rillig M. C. (2020). Trait-based approaches reveal fungal adaptations to nutrient-limiting conditions. Environ. Microbiol. 22 3548–3560. 10.1111/1462-2920.15132 PubMed DOI
Camenzind T., Philipp Grenz K., Lehmann J., Rillig M. C. (2021). Soil fungal mycelia have unexpectedly flexible stoichiometric C:N and C:P ratios. Ecol. Lett. 24 208–218. 10.1111/ele.13632 PubMed DOI
Cleveland C. C., Liptzin D. (2007). C:N:P stoichiometry in soil: Is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85 235–252. 10.1007/s10533-007-9132-0 DOI
Cowling E. B., Merrill W. (1966). Nitrogen in wood and its role in wood deterioration. Can. J. Bot. 44 1539–1554. 10.1139/b66-167 DOI
Darriba D., Taboada G. L., Doallo R., Posada D. (2012). jModelTest 2: More models, new heuristics and parallel computing. Nat. Methods 9 772–772. PubMed PMC
Deng Q., McMahon D. E., Xiang Y., Yu C.-L., Jackson R. B., Hui D. (2017). A global meta-analysis of soil phosphorus dynamics after afforestation. New Phytol. 213 181–192. 10.1111/nph.14119 PubMed DOI
Du E., Terrer C., Pellegrini A. F. A., Ahlström A., van Lissa C. J., Zhao X., et al. (2020). Global patterns of terrestrial nitrogen and phosphorus limitation. Nat. Geosci. 13 221–226. 10.1038/s41561-019-0530-4 DOI
Fernandez C. W., Langley J. A., Chapman S., McCormack M. L., Koide R. T. (2016). The decomposition of ectomycorrhizal fungal necromass. Soil Biol. Biochem. 93 38–49. 10.1016/j.soilbio.2015.10.017 DOI
Gruber S., Seidl-Seiboth V. (2012). Self versus non-self: Fungal cell wall degradation in Trichoderma. Microbiology 158 26–34. 10.1099/mic.0.052613-0 PubMed DOI
Hall T. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp. Ser. 41 95–98. 10.1021/bk-1999-0734.ch008 DOI
Hibbett D. S., Vilgalys R. (1993). Phylogenetic relationships of Lentinus (Basidiomycotina) inferred from molecular and morphological characters. Syst. Bot. 18 409–433. 10.2307/2419417 DOI
Hůnová I., Kurfürst P., Stráník V., Modlík M. (2017). Nitrogen deposition to forest ecosystems with focus on its different forms. Sci. Total Environ. 575 791–798. 10.1016/j.scitotenv.2016.09.140 PubMed DOI
Huntington T. G., Ryan D. F., Hamburg S. P. (1988). Estimating soil nitrogen and carbon pools in a northern hardwood forest ecosystem. Soil Sci. Soc. Am. J. 52 1162–1167. 10.2136/sssaj1988.03615995005200040049x DOI
Johnson N. C. (2010). Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol. 185 631–647. 10.1111/j.1469-8137.2009.03110.x PubMed DOI
Kalač P. (2019). “Major essential elements,” in Mineral composition and radioactivity of edible mushrooms, ed. Kalač P. (Cambridge, MA: Academic Press; ), 25–74. 10.1016/B978-0-12-817565-1.00003-0 DOI
Kassambara A. (2020). ggpubr: “ggplot2” based publication ready plots. Available online at: https://CRAN.R-project.org/package=ggpubr (accessed May 5, 2024).
Kranabetter J. M., Harman-Denhoed R., Hawkins B. J. (2019). Saprotrophic and ectomycorrhizal fungal sporocarp stoichiometry (C: N: P) across temperate rainforests as evidence of shared nutrient constraints among symbionts. New Phytol. 221 482–492. 10.1111/nph.15380 PubMed DOI
Larsen S. (1967). “Soil phosphorus,” in Advances in agronomy, ed. Norman A. G. (Cambridge, MA: Academic Press; ), 151–210.
Lenardon M. D., Munro C. A., Gow N. A. R. (2010). Chitin synthesis and fungal pathogenesis. Curr. Opin. Microbiol. 13 416–423. 10.1016/j.mib.2010.05.002 PubMed DOI PMC
Lilleskov E. A., Hobbie E. A., Horton T. R. (2011). Conservation of ectomycorrhizal fungi: Exploring the linkages between functional and taxonomic responses to anthropogenic N deposition. Fungal Ecol. 4 174–183. 10.1016/j.funeco.2010.09.008 DOI
Lindahl B. D., Ihrmark K., Boberg J., Trumbore S. E., Högberg P., Stenlid J., et al. (2007). Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol. 173 611–620. 10.1111/j.1469-8137.2006.01936.x PubMed DOI
Lindahl B. O., Taylor A. F. S., Finlay R. D. (2002). Defining nutritional constraints on carbon cycling in boreal forests – towards a less “phytocentric” perspective. Plant Soil 242 123–135. 10.1023/A:1019650226585 DOI
López-Mondéjar R., Tláskal V., Větrovský T., Štursová M., Toscan R., Nunes, et al. (2020). Metagenomics and stable isotope probing reveal the complementary contribution of fungal and bacterial communities in the recycling of dead biomass in forest soil. Soil Biol. Biochem. 148:107875. 10.1016/j.soilbio.2020.107875 DOI
Martin F., Kohler A., Murat C., Veneault-Fourrey C., Hibbett D. S. (2016). Unearthing the roots of ectomycorrhizal symbioses. Nat. Rev. Microbiol. 14 760–773. 10.1038/nrmicro.2016.149 PubMed DOI
Marzluf G. A. (1996). “Regulation of nitrogen metabolism in mycelial fungi,” in Biochemistry and molecular biology, eds Brambl R., Marzluf G. A. (Berlin: Springer; ), 357–368. 10.1007/978-3-662-10367-8_16 DOI
Molina-Venegas R., Rodríguez M. A. (2017). Revisiting phylogenetic signal; strong or negligible impacts of polytomies and branch length information? BMC Evol. Biol. 17:53. 10.1186/s12862-017-0898-y PubMed DOI PMC
Mooshammer M., Wanek W., Zechmeister-Boltenstern S., Richter A. (2014). Stoichiometric imbalances between terrestrial decomposer communities and their resources: Mechanisms and implications of microbial adaptations to their resources. Front. Microbiol. 5:22. 10.3389/fmicb.2014.00022 PubMed DOI PMC
Morrison E. W., Frey S. D., Sadowsky J. J., van Diepen L. T. A., Thomas W. K., Pringle A. (2016). Chronic nitrogen additions fundamentally restructure the soil fungal community in a temperate forest. Fungal Ecol. 23 48–57. 10.1016/j.funeco.2016.05.011 DOI
Mouginot C., Kawamura R., Matulich K. L., Berlemont R., Allison S. D., Amend A. S., et al. (2014). Elemental stoichiometry of fungi and bacteria strains from grassland leaf litter. Soil Biol. Biochem. 76 278–285. 10.1016/j.soilbio.2014.05.011 DOI
Nelson D. W., Sommers L. E. (1996). “Total carbon, organic carbon, and organic matter,” in Methods of soil analysis, eds Sparks D. L., Page A. L., Helmke P. A., Loeppert R. H., Soltanpour P. N., Tabatabai M. A., et al. (New York, NY: Oxford University Press; ), 961–1010. 10.2136/sssabookser5.3.c34 DOI
No H. K., Meyers S. P. (1995). Preparation and characterization of chitin and chitosan– review. J. Aquat. Food Prod. Technol. 4 27–52. 10.1300/J030v04n02_03 DOI
Ogle D. H., Doll J. C., Wheeler P., Dinno A. (2022). Simple fisheries stock assessment methods. R package version 0.9.5. Available online at: https://CRAN.R-project.org/package=FSA (accessed May 5, 2024).
Ohno T., Zibilske L. M. (1991). Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Sci. Soc. Am. J. 55 892–895. 10.2136/sssaj1991.03615995005500030046x DOI
Piché-Choquette S., Tláskal V., Vrška T., Jiráska L., Větrovský T., Baldrian P. (2023). Continuous microhabitats as crossroads of fungal communities in a primeval temperate forest. Soil Biol. Biochem. 187:109187. 10.1016/j.soilbio.2023.109187 DOI
Põlme S., Abarenkov K., Henrik Nilsson R., Lindahl B. D., Clemmensen K. E., Kauserud H., et al. (2020). FungalTraits: A user-friendly traits database of fungi and fungus-like stramenopiles. Fungal Divers. 105 1–16. 10.1007/s13225-020-00466-2 DOI
Quinché J. P. (1997). Phosphorus and heavy metals in some species of fungi. Rev. Suisse Agric. 29 151–156.
R Core Team (2022). R: A language and environment for statistical computing. Vienna: R Core Team.
Ramirez K. S., Craine J. M., Fierer N. (2012). Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Glob. Change Biol. 18 1918–1927. 10.1111/j.1365-2486.2012.02639.x DOI
Rayner A., Boddy L. (1989). Fungal decomposition of wood. Its biology and ecology. Chichester: John Wiley & Sons Ltd.
Revell L. J. (2012). phytools: An R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3 217–223. 10.1111/j.2041-210X.2011.00169.x DOI
Revelle W. (2023). psych: Procedures for psychological, psychometric, and personality research. Available online at: https://CRAN.R-project.org/package=psych (accessed May 5, 2024).
Ronquist F., Teslenko M., van der Mark P., Ayres D. L., Darling A., Höhna S., et al. (2012). MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61 539–542. 10.1093/sysbio/sys029 PubMed DOI PMC
Root R. B. (1967). The niche exploitation pattern of the blue-gray gnatcatcher. Ecol. Monogr. 37 317–350. 10.2307/1942327 DOI
Schneider K., Resl P., Westberg M., Spribille T. (2015). A new, highly effective primer pair to exclude algae when amplifying nuclear large ribosomal subunit (LSU) DNA from lichens. Lichenologist 47 269–275. 10.1017/S002428291500016X DOI
Schoch C. L., Seifert K. A., Huhndorf S., Robert V., Spouge J. L., Levesque C., et al. (2012). From the cover: Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc. Natl. Acad. Sci. U.S.A. 109 6241–6246. 10.1073/pnas.1117018109 PubMed DOI PMC
Smith S., Read D. J. (2008). Mycorrhizal symbiosis. London: Academic Press Publishers.
Starke R., Morais D., Větrovský T., López Mondéjar R., Baldrian P., Brabcová V. (2020). Feeding on fungi: Genomic and proteomic analysis of the enzymatic machinery of bacteria decomposing fungal biomass. Environ. Microbiol. 22 4604–4619. 10.1111/1462-2920.15183 PubMed DOI
Tracey M. V. (1955). “Chitin,” in Modern methods of plant analysis / Moderne methoden der pflanzenanalyse, eds Paech K., Tracey M. V. (Berlin: Springer; ), 2. 10.1007/978-3-642-64955-4_9 DOI
Trocha L. K., Rudy E., Chen W., Dabert M., Eissenstat D. M. (2016). Linking the respiration of fungal sporocarps with their nitrogen concentration: Variation among species, tissues and guilds. Funct. Ecol. 30 1756–1768. 10.1111/1365-2435.12688 DOI
van Breemen N., van Dijk H. F. G. (1988). Ecosystem effects of atmospheric deposition of nitrogen in The Netherlands. Environ. Pollut. 54 249–274. 10.1016/0269-7491(88)90115-7 PubMed DOI
van der Linde S., Suz L. M., Orme C. D. L., Cox F., Andreae H., Asi E., et al. (2018). Environment and host as large-scale controls of ectomycorrhizal fungi. Nature 558 243–248. 10.1038/s41586-018-0189-9 PubMed DOI
Vilgalys R., Hester M. (1990). Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J. Bacteriol. 172 4238–4246. 10.1128/jb.172.8.4238-4246.1990 PubMed DOI PMC
Vogt K. A., Edmonds R. L., Grier C. C. (1981). Biomass and nutrient concentrations of sporocarps produced by mycorrhizal and decomposer fungi in Abies amabilis stands. Oecologia 50 170–175. 10.1007/BF00348033 PubMed DOI
Watkinson S., Bebber D., Darrah P., Fricker M., Tlalka M., Boddy L. (2006). “The role of wood decay fungi in the carbon and nitrogen dynamics of the forest floor,” in Fungi in biogeochemical cycles, ed. Gadd G. M. (Cambridge: Cambridge University Press; ), 151–181. 10.1017/CBO9780511550522.008 DOI
White S., McIntyre M., Berry D. R., McNeil B. (2002). The autolysis of industrial filamentous fungi. Crit. Rev. Biotechnol. 22 1–14. 10.1080/07388550290789432 PubMed DOI
White T. J., Bruns T., Lee S., Taylor J. (1990). “Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics,” in PCR protocols: A guide to methods and applications, eds Innis M. A., Gelfand D. H., Sninsky J. J., White T. J. (New York, NY: Academic Press; ), 315–322.
Wickham H. (2016). ggplot2: Elegant graphics for data analysis. New York, NY: Springer-Verlag.
Zanne A. E., Abarenkov K., Afkhami M. E., Aguilar-Trigueros C. A., Bates S., Bhatnagar, et al. (2020). Fungal functional ecology: Bringing a trait-based approach to plant-associated fungi. Biol. Rev. 95 409–433. 10.1111/brv.12570 PubMed DOI
Zhang J., Elser J. J. (2017). Carbon:nitrogen:phosphorus stoichiometry in fungi: A meta-analysis. Front. Microbiol. 8:1281. 10.3389/fmicb.2017.01281 PubMed DOI PMC
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. 10.1016/j.soilbio.2017.09.015 DOI