Transcriptomic markers of fungal growth, respiration and carbon-use efficiency

. 2021 Aug 19 ; 368 (15) : .

Jazyk angličtina Země Anglie, Velká Británie Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid34338746

Fungal metabolic carbon acquisition and its subsequent partitioning between biomass production and respiration, i.e. the carbon-use efficiency (CUE), are central parameters in biogeochemical modeling. However, current available techniques for estimating these parameters are all associated with practical and theoretical shortcomings, making assessments unreliable. Gene expression analyses hold the prospect of phenotype prediction by indirect means, providing new opportunities to obtain information about metabolic priorities. We cultured four different fungal isolates (Chalara longipes, Laccaria bicolor, Serpula lacrymans and Trichoderma harzianum) in liquid media with contrasting nitrogen availability and measured growth rates and respiration to calculate CUE. By relating gene expression markers to measured carbon fluxes, we identified genes coding for 1,3-β-glucan synthase and 2-oxoglutarate dehydrogenase as suitable markers for growth and respiration, respectively, capturing both intraspecific variation as well as within-strain variation dependent on growth medium. A transcript index based on these markers correlated significantly with differences in CUE between the fungal isolates. Our study paves the way for the use of these markers to assess differences in growth, respiration and CUE in natural fungal communities, using metatranscriptomic or the RT-qPCR approach.

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Allison SD, Wallenstein MD, Bradford MA. Soil-carbon response to warming dependent on microbial physiology. Nat Geosci. 2010;3:336–40.

Allison SD. A trait-based approach for modelling microbial litter decomposition. Ecol Lett. 2012;15:1058–70. PubMed

Andrews S. FASTQC: A quality control tool for high throughput sequence data. 2010. https://www.bioinformatics.babraham.ac.uk/projects/fastqc/.

Barbi F, Kohler A, Barry Ket al. . Fungal ecological strategies reflected in gene transcription - a case study of two litter decomposers. Environ Microbiol. 2020;22:1089–103. PubMed

Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20. PubMed PMC

Bowman SM, Free SJ. The structure and synthesis of the fungal cell wall. Bioessays. 2006;28:799–808. PubMed

Camenzind T, Philipp Grenz, Ket al. . Soil fungal mycelia have unexpectedly flexible stoichiometric C:n and C:p ratios. Ecology Letters. 2021;24:208–18. PubMed

Cotrufo MF, Wallenstein MD, Boot CMet al. . The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter?. Glob Change Biol. 2013;19:988–95. PubMed

Druzhinina IS, Chenthamara K, Zhang Jet al. . Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts. PLos Genet. 2018;14:e1007322. PubMed PMC

Eastwood DC, Floudas D, Binder Met al. . The plant cell wall-decomposing machinery underlies the functional diversity of forest fungi. Science. 2011;333:762–5. PubMed

Gálvez S, Gadal P. On the function of the NADP-dependent isocitrate dehydrogenase isoenzymes in living organisms. Plant Sci. 1995;105:1–14.

Geyer KM, Dijkstra P, Sinsabaugh Ret al. . Clarifying the interpretation of carbon use efficiency in soil through methods comparison. Soil Biol Biochem. 2019;128:79–88.

Geyer KM, Kyker-Snowman E, Grandy ASet al. . Microbial carbon use efficiency: accounting for population, community, and ecosystem-scale controls over the fate of metabolized organic matter. Biogeochemistry. 2016;127:173–88.

Haselbeck RJ, McAlister-Henn L. Function and expression of yeast mitochondrial NAD- and NADP-specific isocitrate dehydrogenases. J Biol Chem. 1993;268:12116–22. PubMed

Kanehisa M. Enzyme annotation and metabolic reconstruction using KEGG. Methods Mol Biol. 2017;1611:135–45. PubMed

Kauserud H, Svegården IB, Sætre GPet al. . Asian origin and rapid global spread of the destructive dry rot fungus Serpula lacrymans. Mol Ecol. 2007;16:3350–60. PubMed

Kelly R, Register E, Hsu MJet al. . Isolation of a gene involved in 1,3-beta-glucan synthesis in Aspergillus nidulans and purification of the corresponding protein. J Bacteriol. 1996;178:4381 LP–4391. PubMed PMC

Kershaw JL, Stewart GR. The role of glutamine synthetase, glutamate synthase and glutamate dehydrogenase in ammonia assimilation by the mycorrhizal fungus Pisolithus tinctorius. Annales des Sciences Forestières. 1989;46:706s–10s.

Koukol O. New species of Chalara occupying coniferous needles. Fung Diver. 2011;49:75.

Kuske CR, Hesse CN, Challacombe JFet al. . Prospects and challenges for fungal metatranscriptomics of complex communities. Fung Ecol. 2015;14:133–7.

Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–9. PubMed PMC

Li H, Handsaker B, Wysoker Aet al. . The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078–9. PubMed PMC

Li H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics. 2011;27:2987–93. PubMed PMC

Lindahl BD, Kuske CR. Metagenomics for study of fungal ecology. Ecol Genomics Fungi. 2013:279–303. DOI: 10.1002/9781118735893.ch13.

Lipson DA. The complex relationship between microbial growth rate and yield and its implications for ecosystem processes. Front Microbiol. 2015;6:1–5. PubMed PMC

Lombard V, Golaconda Ramulu, Het al. . The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014;42:490–5. PubMed PMC

Manzoni S, Čapek P, Mooshammer Met al. . Optimal metabolic regulation along resource stoichiometry gradients. Ecol Lett. 2017;20:1182–91. PubMed

Manzoni S, Čapek P, Porada Pet al. . Reviews and syntheses: carbon use efficiency from organisms to ecosystems - Definitions, theories, and empirical evidence. Biogeosciences. 2018;15:5929–49.

Martin F, Aerts A, Ahrén Det al. . The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature. 2008;452:88–92. PubMed

Marx DH. Influence of ectotrophic mycorrhizal fungi on resistance of pine roots to pathogenic infections .II. production identification and biological activity of antibiotics produced by Leucopaxillus cerealis var piceina. Phytopathology. 1969;59:411–7. PubMed

Montanini B, Betti M, Márquez AJet al. . Distinctive properties and expression profiles of glutamine synthetase from a plant symbiotic fungus. Biochem J. 2003;373:357–68. PubMed PMC

Mortazavi A, Williams BA, McCue Ket al. . Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008;5:621–8. PubMed

Nilsson RH, Anslan S, Bahram Met al. . Mycobiome diversity: high-throughput sequencing and identification of fungi. Nat Rev Microbiol. 2019;17:95–109. PubMed

R Core Team . R: A Language and Environment for Statistical Computing. 2019.

Repetto B, Tzagoloff A. Structure and regulation of KGD1, the structural gene for yeast alpha-ketoglutarate dehydrogenase. Mol Cell Biol. 1989;9:2695 LP–2705. PubMed PMC

Riggs CE, Hobbie SE, Bach EMet al. . Nitrogen addition changes grassland soil organic matter decomposition. Biogeochemistry. 2015;125:203–19.

Spohn M, Pötsch EM, Eichorst SAet al. . Soil microbial carbon use efficiency and biomass turnover in a long-term fertilization experiment in a temperate grassland. Soil Biol Biochem. 2016;97:168–75.

Spohn M. Microbial respiration per unit microbial biomass depends on litter layer carbon-to-nitrogen ratio. Biogeosciences. 2015;12:817–23.

Sreenivasaprasad S, Burton KS, Wood DA. Cloning and characterisation of a chitin synthase gene cDNA from the cultivated mushroom Agaricus bisporus and its expression during morphogenesis1. FEMS Microbiol Lett. 2000;189:73–7. PubMed

Treseder KK, Lennon JT. Fungal traits that drive ecosystem dynamics on land. Microbiol Mol Biol Rev. 2015;79:243–62. PubMed PMC

Wang C, Qu L, Yang Let al. . Large-scale importance of microbial carbon use efficiency and necromass to soil organic carbon. Glob Change Biol. 2021;27:2039–48. PubMed

Weindling R. Trichoderma lignorum as a parasite of other soil fungiNo title. Phytopathology. 1932;22:837–45.

Zhang H, Goll DS, Manzoni Set al. . Modeling the effects of litter stoichiometry and soil mineral N availability on soil organic matter formation using CENTURY-CUE (v1.0). Geosci Model Dev. 2018;11:4779–96.

Zhang J, Elser JJ. Carbon: nitrogen: phosphorus stoichiometry in fungi: a meta-analysis. Front Microbiol. 2017;8:1–9. PubMed PMC

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