The carbon starvation response of the ectomycorrhizal fungus Paxillus involutus

Ellstrom, Magnus; Shah, Firoz; Johansson, Tomas; Ahren, Dag; Persson, Per; Tunlid, Anders

doi:10.1093/femsec/fiv027

The carbon starvation response of the ectomycorrhizal fungus Paxillus involutus

Journal Article · Mon Mar 16 00:00:00 EDT 2015 · FEMS Microbiology Ecology (Online)

DOI:https://doi.org/10.1093/femsec/fiv027· OSTI ID:1343065

Ellstrom, Magnus ^[1]; Shah, Firoz ^[2]; Johansson, Tomas ^[2]; Ahren, Dag ^[3]; Persson, Per ^[4]; Tunlid, Anders ^[2]

Lund Univ. (Sweden). Dept. of Biology. Microbial Ecology. Centre for Environmental and Climate Research (CEC); DOE Office of Scientific and Technical Information (OSTI)
Lund Univ. (Sweden). Dept. of Biology. Microbial Ecology
Lund Univ. (Sweden). Dept. of Biology. Microbial Ecology. Bioinformatics Infrastructure for Life Sciences (BILS)
Lund Univ. (Sweden). Dept. of Biology. Microbial Ecology. Centre for Environmental and Climate Research (CEC)

The amounts of carbon allocated to the fungal partner in ectomycorrhizal associations can vary substantially depending on the plant growth and the soil nutrient conditions, and the fungus may frequently be confronted with limitations in carbon. We used chemical analysis and transcriptome profiling to examine the physiological response of the ectomycorrhizal fungus Paxillus involutus to carbon starvation during axenic cultivation. Carbon starvation induced a decrease in the biomass. Concomitantly, ammonium, cell wall material (chitin) and proteolytic enzymes were released into the medium, which suggest autolysis. Compared with the transcriptome of actively growing hyphae, about 45% of the transcripts analyzed were differentially regulated during C-starvation. Induced during starvation were transcripts encoding extracellular enzymes such as peptidases, chitinases and laccases. In parallel, transcripts of N-transporters were upregulated, which suggest that some of the released nitrogen compounds were re-assimilated by the mycelium. The observed changes suggest that the carbon starvation response in P. involutus is associated with complex cellular changes that involves autolysis, recycling of intracellular compounds by autophagy and reabsorption of the extracellular released material. The study provides molecular markers that can be used to examine the role of autolysis for the turnover and survival of the ectomycorrhizal mycelium in soils.

View Accepted Manuscript (DOE)

Research Organization:: Lund Univ. (Sweden); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); Swedish Research Council (VR)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1343065

Journal Information:: FEMS Microbiology Ecology (Online), Journal Name: FEMS Microbiology Ecology (Online) Journal Issue: 4 Vol. 91; ISSN 1574-6941

Publisher:: Federation of European Microbiological SocietiesCopyright Statement

Country of Publication:: United States

Language:: English

References (52)

Paxillus Wallander, H.; Söderström, B. Ectomycorrhizal Fungi Key Genera in Profile https://doi.org/10.1007/978-3-662-06827-4_9	book	January 1999
The production and turnover of extramatrical mycelium of ectomycorrhizal fungi in forest soils: role in carbon cycling Ekblad, A.; Wallander, H.; Godbold, D. L. Plant and Soil, Vol. 366, Issue 1-2 https://doi.org/10.1007/s11104-013-1630-3	journal	February 2013
Fluorescein isothiocyanate-labeled casein assay for proteolytic enzymes Twining, Sally S. Analytical Biochemistry, Vol. 143, Issue 1 https://doi.org/10.1016/0003-2697(84)90553-0	journal	November 1984
Autophagy in filamentous fungi Pollack, J.; Harris, S.; Marten, M. Fungal Genetics and Biology, Vol. 46, Issue 1 https://doi.org/10.1016/j.fgb.2008.10.010	journal	January 2009
Ammonia: a candidate for nitrogen transfer at the mycorrhizal interface Chalot, Michel; Blaudez, Damien; Brun, Annick Trends in Plant Science, Vol. 11, Issue 6 https://doi.org/10.1016/j.tplants.2006.04.005	journal	June 2006
Estimation of mycelial growth of basidiomycetes by means of chitin determination Plassard, Claude S.; Mousain, Daniel G.; Salsac, Louis E. Phytochemistry, Vol. 21, Issue 2 https://doi.org/10.1016/s0031-9422(00)95263-4	journal	January 1982
The machinery of macroautophagy Feng, Yuchen; He, Ding; Yao, Zhiyuan Cell Research, Vol. 24, Issue 1 https://doi.org/10.1038/cr.2013.168	journal	December 2013
Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus Rineau, F.; Shah, F.; Smits, M. M. The ISME Journal, Vol. 7, Issue 10 https://doi.org/10.1038/ismej.2013.91	journal	June 2013
SignalP 4.0: discriminating signal peptides from transmembrane regions Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar Nature Methods, Vol. 8, Issue 10 https://doi.org/10.1038/nmeth.1701	journal	September 2011
Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil Högberg, Mona N.; Högberg, Peter New Phytologist, Vol. 154, Issue 3 https://doi.org/10.1046/j.1469-8137.2002.00417.x	journal	June 2002
ATO3 Encoding a Putative Outward Ammonium Transporter Is an RTG- independent Retrograde Responsive Gene Regulated by GCN4 and the Ssy1-Ptr3-Ssy5 Amino Acid Sensor System Guaragnella, Nicoletta; Butow, Ronald A. Journal of Biological Chemistry, Vol. 278, Issue 46 https://doi.org/10.1074/jbc.m309301200	journal	September 2003
The Autolysis of Industrial Filamentous Fungi White, Stewart; McIntyre, Mhairi; Berry, David R. Critical Reviews in Biotechnology, Vol. 22, Issue 1 https://doi.org/10.1080/07388550290789432	journal	January 2002
A comparison of normalization methods for high density oligonucleotide array data based on variance and bias Bolstad, B. M.; Irizarry, R. A.; Astrand, M. Bioinformatics, Vol. 19, Issue 2 https://doi.org/10.1093/bioinformatics/19.2.185	journal	January 2003
Gene Expression Omnibus: NCBI gene expression and hybridization array data repository Edgar, R. Nucleic Acids Research, Vol. 30, Issue 1 https://doi.org/10.1093/nar/30.1.207	journal	January 2002
UniProt: the Universal Protein knowledgebase Apweiler, R. Nucleic Acids Research, Vol. 32, Issue 90001 https://doi.org/10.1093/nar/gkh131	journal	January 2004
The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics Cantarel, B. L.; Coutinho, P. M.; Rancurel, C. Nucleic Acids Research, Vol. 37, Issue Database https://doi.org/10.1093/nar/gkn663	journal	January 2009
MEROPS: the database of proteolytic enzymes, their substrates and inhibitors Rawlings, N. D.; Barrett, A. J.; Bateman, A. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr987	journal	November 2011
Pfam: the protein families database Finn, Robert D.; Bateman, Alex; Clements, Jody Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1223	journal	November 2013
Summaries of Affymetrix GeneChip probe level data Irizarry, R. A. Nucleic Acids Research, Vol. 31, Issue 4 https://doi.org/10.1093/nar/gng015	journal	February 2003
Rates and quantities of carbon flux to ectomycorrhizal mycelium following 14C pulse labeling of Pinus sylvestris seedlings: effects of litter patches and interaction with a wood-decomposer fungus Leake, J. R.; Donnelly, D. P.; Saunders, E. M. Tree Physiology, Vol. 21, Issue 2-3 https://doi.org/10.1093/treephys/21.2-3.71	journal	February 2001
Growth and product formation in chemostat and recycling cultures by Aspergillus niger N402 and a glucoamylase overproducing transformant, provided with multiple copies of the glaA gene Schrickx, J. M.; Krave, A. S.; Verdoes, J. C. Journal of General Microbiology, Vol. 139, Issue 11 https://doi.org/10.1099/00221287-139-11-2801	journal	November 1993
Changes in Constituents and Ultrastructure of Hyphal Compartments during Autolysis of Glucose-starved Penicillium chrysogenum Trinci, A. P. J.; Righelato, R. C. Journal of General Microbiology, Vol. 60, Issue 2 https://doi.org/10.1099/00221287-60-2-239	journal	February 1970
Transcriptome changes initiated by carbon starvation in Aspergillus nidulans Szilágyi, Melinda; Miskei, Márton; Karányi, Zsolt Microbiology, Vol. 159, Issue Pt_1 https://doi.org/10.1099/mic.0.062935-0	journal	January 2013
The ectomycorrhizal fungus Paxillus involutus converts organic matter in plant litter using a trimmed brown-rot mechanism involving Fenton chemistry: Organic matter degradation by ectomycorrhizal fungi Rineau, Francois; Roth, Doris; Shah, Firoz Environmental Microbiology, Vol. 14, Issue 6 https://doi.org/10.1111/j.1462-2920.2012.02736.x	journal	March 2012
A gene repertoire for nitrogen transporters in Laccaria bicolor Lucic, Eva; Fourrey, Claire; Kohler, Annegret New Phytologist, Vol. 180, Issue 2 https://doi.org/10.1111/j.1469-8137.2008.02580.x	journal	October 2008
Aquaporins: for more than water at the plant–fungus interface? Maurel, Christophe; Plassard, Claude New Phytologist, Vol. 190, Issue 4 https://doi.org/10.1111/j.1469-8137.2011.03731.x	journal	May 2011
Fungal apoptosis: function, genes and gene function Sharon, Amir; Finkelstein, Alin; Shlezinger, Neta FEMS Microbiology Reviews, Vol. 33, Issue 5 https://doi.org/10.1111/j.1574-6976.2009.00180.x	journal	September 2009
Ectomycorrhizal fungi - potential organic matter decomposers, yet not saprotrophs Lindahl, Björn D.; Tunlid, Anders New Phytologist, Vol. 205, Issue 4 https://doi.org/10.1111/nph.13201	journal	December 2014
The Plant Cell Wall-Decomposing Machinery Underlies the Functional Diversity of Forest Fungi Eastwood, D. C.; Floudas, D.; Binder, M. Science, Vol. 333, Issue 6043, p. 762-765 https://doi.org/10.1126/science.1205411	journal	July 2011
The carbon starvation response of Aspergillus niger during submerged cultivation: Insights from the transcriptome and secretome Nitsche, Benjamin M.; Jørgensen, Thomas R.; Akeroyd, Michiel BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-380	journal	January 2012
Characterization and genomic analysis of kraft lignin biodegradation by the beta-proteobacterium Cupriavidus basilensis B-8 Shi, Yan; Chai, Liyuan; Tang, Chongjian Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-1	journal	January 2013
Analytical Chemical Studies on Amino Sugars. II. Deterimation of Hexosamines using 3-Methyl-2-benzothiazolone Hydrazone Hydrochloride Tsuji, Akio; Kinoshita, Toshio; Hoshino, Masanori CHEMICAL & PHARMACEUTICAL BULLETIN, Vol. 17, Issue 7 https://doi.org/10.1248/cpb.17.1505	journal	January 1969
Autolysis and ageing of Penicillium chrysogenum under carbon starvation: respiration and glucose oxidase production Sámi, L.; Karaffa, L.; Emri, T. Acta Microbiologica et Immunologica Hungarica, Vol. 50, Issue 1 https://doi.org/10.1556/amicr.50.2003.1.7	journal	April 2003
Nitrogen amendments reduce the growth of extramatrical ectomycorrhizal mycelium Arnebrant, K. Mycorrhiza, Vol. 5, Issue 1 https://doi.org/10.1007/BF00204014	journal	November 1994
Autophagy promotes survival in aging submerged cultures of the filamentous fungus Aspergillus niger Nitsche, Benjamin M.; Burggraaf-van Welzen, Anne-Marie; Lamers, Gerda Applied Microbiology and Biotechnology, Vol. 97, Issue 18 https://doi.org/10.1007/s00253-013-4971-1	journal	May 2013
Self-eating to grow and kill: autophagy in filamentous ascomycetes Voigt, Oliver; Pöggeler, Stefanie Applied Microbiology and Biotechnology, Vol. 97, Issue 21 https://doi.org/10.1007/s00253-013-5221-2	journal	September 2013
Effects of different fertilizer treatments on ectomycorrhizal colonization potential in two Scots pine forests in Sweden Arnebrant, Kristina; Söderström, Bengt Forest Ecology and Management, Vol. 53, Issue 1-4 https://doi.org/10.1016/0378-1127(92)90035-8	journal	October 1992
Estimation of mycelial growth of basidiomycetes by means of chitin determination Plassard, Claude S.; Mousain, Daniel G.; Salsac, Louis E. Phytochemistry, Vol. 21, Issue 2 https://doi.org/10.1016/S0031-9422(00)95263-4	journal	January 1982
An infrared investigation in relation with chitin and chitosan characterization Brugnerotto, J.; Lizardi, J.; Goycoolea, F. M. Polymer, Vol. 42, Issue 8 https://doi.org/10.1016/S0032-3861(00)00713-8	journal	April 2001
Chemical characterization of protein-like fluorophores in DOM in relation to aromatic amino acids Yamashita, Youhei; Tanoue, Eiichiro Marine Chemistry, Vol. 82, Issue 3-4 https://doi.org/10.1016/S0304-4203(03)00073-2	journal	August 2003
Infrared spectroscopy of proteins Barth, Andreas Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1767, Issue 9 https://doi.org/10.1016/j.bbabio.2007.06.004	journal	September 2007
Growth of ectomycorrhizal fungal mycelium along a Norway spruce forest nitrogen deposition gradient and its effect on nitrogen leakage Bahr, Adam; Ellström, Magnus; Akselsson, Cecilia Soil Biology and Biochemistry, Vol. 59 https://doi.org/10.1016/j.soilbio.2013.01.004	journal	April 2013
Isolation and characterization of a general amino acid permease from the ectomycorrhizal fungus Amanita muscaria Nehls, Uwe; Kleber, Regine; Wiese, Joachim New Phytologist, Vol. 144, Issue 2 https://doi.org/10.1046/j.1469-8137.1999.00513.x	journal	November 1999
ATO3 Encoding a Putative Outward Ammonium Transporter Is an RTG- independent Retrograde Responsive Gene Regulated by GCN4 and the Ssy1-Ptr3-Ssy5 Amino Acid Sensor System Guaragnella, Nicoletta; Butow, Ronald A. Journal of Biological Chemistry, Vol. 278, Issue 46 https://doi.org/10.1074/jbc.M309301200	journal	September 2003
Effects of excess nitrogen and phosphorus starvation on the extramatrical mycelium of ectomycorrhizas of Pinus sylvestris L. Wallander, H.; Nylund, J. -E. New Phytologist, Vol. 120, Issue 4 https://doi.org/10.1111/j.1469-8137.1992.tb01798.x	journal	April 1992
Quantification of effects of season and nitrogen supply on tree below-ground carbon transfer to ectomycorrhizal fungi and other soil organisms in a boreal pine forest Högberg, Mona N.; Briones, Maria J. I.; Keel, Sonja G. New Phytologist, Vol. 187, Issue 2 https://doi.org/10.1111/j.1469-8137.2010.03274.x	journal	April 2010
The aquaporin gene family of the ectomycorrhizal fungus Laccaria bicolor: lessons for symbiotic functions Dietz, Sandra; von Bülow, Julia; Beitz, Eric New Phytologist, Vol. 190, Issue 4 https://doi.org/10.1111/j.1469-8137.2011.03651.x	journal	February 2011
Dramatic changes in ectomycorrhizal community composition, root tip abundance and mycelial production along a stand-scale nitrogen deposition gradient Kjøller, Rasmus; Nilsson, Lars-Ola; Hansen, Karin New Phytologist, Vol. 194, Issue 1 https://doi.org/10.1111/j.1469-8137.2011.04041.x	journal	February 2012
The molecular components of the extracellular protein-degradation pathways of the ectomycorrhizal fungus Paxillus involutus Shah, Firoz; Rineau, Francois; Canbäck, Björn New Phytologist, Vol. 200, Issue 3 https://doi.org/10.1111/nph.12425	journal	July 2013
Differential Roles of the ChiB Chitinase in Autolysis and Cell Death of Aspergillus nidulans Shin, Kwang-Soo; Kwon, Nak-Jung; Kim, Young Hwan Eukaryotic Cell, Vol. 8, Issue 5 https://doi.org/10.1128/EC.00368-08	journal	March 2009
A Functional-Phylogenetic Classification System for Transmembrane Solute Transporters Saier, M. H. Microbiology and Molecular Biology Reviews, Vol. 64, Issue 2 https://doi.org/10.1128/MMBR.64.2.354-411.2000	journal	June 2000
Autolysis and ageing of Penicillium chrysogenum under carbon starvation: respiration and glucose oxidase production Sámi, L.; Karaffa, L.; Emri, T. Acta Microbiologica et Immunologica Hungarica, Vol. 50, Issue 1 https://doi.org/10.1556/AMicr.50.2003.1.7	journal	April 2003

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