Abstract
Fungal cells are surrounded by a tight cell wall to protect them from harmful environmental conditions and to resist lysis. The synthesis and assembly determine the shape, structure, and integrity of the cell wall during the process of mycelial growth and development. High temperature is an important abiotic stress, which affects the synthesis and assembly of cell walls. In the present study, the chitin and β-1,3-glucan concentrations in the cell wall of Pleurotus ostreatus mycelia were changed after high-temperature treatment. Significantly higher chitin and β-1,3-glucan concentrations were detected at 36 °C than those incubated at 28 °C. With the increased temperature, many aberrant chitin deposition patches occurred, and the distribution of chitin in the cell wall was uneven. Moreover, high temperature disrupts the cell wall integrity, and P. ostreatus mycelia became hypersensitive to cell wall-perturbing agents at 36 °C. The cell wall structure tended to shrink or distorted after high temperature. The cell walls were observed to be thicker and looser by using transmission electron microscopy. High temperature can decrease the mannose content in the cell wall and increase the relative cell wall porosity. According to infrared absorption spectrum, high temperature broke or decreased the glycosidic linkages. Finally, P. ostreatus mycelial cell wall was easily degraded by lysing enzymes after high-temperature treatment. In other words, the cell wall destruction caused by high temperature may be a breakthrough for P. ostreatus to be easily infected by Trichoderma.
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References
Abidi N, Cabrales L, Haigler CH (2014) Changes in the cell wall and cellulose content of developing cotton fibers investigated by FTIR spectroscopy. Carbohydr Polym 100:9–16. https://doi.org/10.1016/j.carbpol.2013.01.074
Aguilar-Uscanga B, Francois JM (2003) A study of the yeast cell wall composition and structure in response to growth conditions and mode of cultivation. Lett Appl Microbiol 37(3):268–274. https://doi.org/10.1046/j.1472-765X.2003.01394.x
Akabane M, Yamamoto A, Aizawa S-i, Taga A, Kodama S (2014) Simultaneous enantioseparation of monosaccharides derivatized with L-tryptophan by reversed phase HPLC. Anal Sci 30(7):739–743. https://doi.org/10.2116/analsci.30.739
Bickle M, Delley PA, Schmidt A, Hall MN (1998) Cell wall integrity modulates RHO1 activity via the exchange factor ROM2. EMBO J 17(8):2235–2245. https://doi.org/10.1093/emboj/17.8.2235
Blaszczyk L, Siwulski M, Sobieralski K, Fruzynska-Jozwiak D (2013) Diversity of Trichoderma spp. causing Pleurotus green mould diseases in Central Europe. Folia Microbiol (Praha) 58(4):325–333. https://doi.org/10.1007/s12223-012-0214-6
Bulik DA, Olczak M, Lucero HA, Osmond BC, Robbins PW, Specht CA (2003) Chitin synthesis in Saccharomyces cerevisiae in response to supplementation of growth medium with glucosamine and cell wall stress. Eukaryot Cell 2(5):886–900. https://doi.org/10.1128/ec.2.5.886-900.2003
Cabib E, Roh DH, Schmidt M, Crotti LB, Varma A (2001) The yeast cell wall and septum as paradigms of cell growth and morphogenesis. J Biol Chem 276(23):19679–19682. https://doi.org/10.1074/jbc.R000031200
Cortes JC, Katoh-Fukui R, Moto K, Ribas JC, Ishiguro J (2004) Schizosaccharomyces pombe Pmr1p is essential for cell wall integrity and is required for polarized cell growth and cytokinesis. Eukaryot Cell 3(5):1124–1135. https://doi.org/10.1128/EC.3.5.1124-1135.2004
de Groot PW, Ruiz C, Vázquez de Aldana CR, Duenas E, Cid VJ, Del Rey F, Rodríquez-Peña JM, Pérez P, Andel A, Caubín J, Arroyo J, García JC, Gil C, Molina M, García LJ, Nombela C, Klis FM (2001) A genomic approach for the identification and classification of genes involved in cell wall formation and its regulation in Saccharomyces cerevisiae. Comp Funct Genomics 2(3):124–142. https://doi.org/10.1002/cfg.85
De Nobel JG, Klis FM, Munnik T, Priem J, Van Den Ende H (1990) An assay of relative cell wall porosity in Saccharomyces cerevisiae, Kluyveromyces lactis and Schizosaccharomyces pombe. Yeast 6(6):483–490. https://doi.org/10.1002/yea.320060605
Depree J, Emerson GW, Sullivan PA (1993) The cell wall of the oleaginous yeast Trichosporon cutaneum. J Gen Microbiol 139(9):2123–2133
Fortwendel JR, Juvvadi PR, Pinchai N, Perfect BZ, Alspaugh JA, Perfect JR, Steinbach WJ (2009) Differential effects of inhibiting chitin and 1,3-β-D-glucan synthesis in ras and calcineurin mutants of Aspergillus fumigatus. Antimicrob Agents Chemother 53(2):476–482. https://doi.org/10.1128/AAC.01154-08
Ganeva V, Galutzov B, Teissie J (2013) Evidence that pulsed electric field treatment enhances the cell wall porosity of yeast cells. Appl Biochem Biotech 172(3):1540–1552. https://doi.org/10.1007/s12010-013-0628-x
Garcia R, Botet J, Rodriguez-Pena JM, Bermejo C, Ribas JC, Revuelta JL, Nombela C, Arroyo J (2015) Genomic profiling of fungal cell wall-interfering compounds: identification of a common gene signature. BMC Genomics 16:683. https://doi.org/10.1186/s12864-015-1879-4
Geraldine AM, Lopes FAC, Carvalho DDC, Barbosa ET, Rodrigues AR, Brandão RS, Ulhoa CJ, Lobo Junior M (2013) Cell wall-degrading enzymes and parasitism of sclerotia are key factors on field biocontrol of white mold by Trichoderma spp. Biol Control 67(3):308–316. https://doi.org/10.1016/j.biocontrol.2013.09.013
Gopal PK, Shepherd MG, Sullivan PA (1984) Analysis of wall glucans from yeast, hyphal and germ-tube forming cells of Candida albicans. J Gen Microbiol 130(12):3295–3301. https://doi.org/10.1099/00221287-130-12-3295
Henry C, Fontaine T, Heddergott C, Robinet P, Aimanianda V, Beau R, Beauvais A, Mouyna I, Prevost M-C, Fekkar A, Zhao Y, Perlin D, Latgé J-P (2016) Biosynthesis of cell wall mannan in the conidium and the mycelium of Aspergillus fumigatus. Cell Microbiol 18(12):1881–1891. https://doi.org/10.1111/cmi.12665
Huang X, Chen L, Ran W, Shen Q, Yang X (2011) Trichoderma harzianum strain SQR-T37 and its bio-organic fertilizer could control Rhizoctonia solani damping-off disease in cucumber seedlings mainly by the mycoparasitism. Appl Microbiol Biotechnol 91(3):741–755. https://doi.org/10.1007/s00253-011-3259-6
Jigami Y, Odani T (1999) Mannosylphosphate transfer to yeast mannan. Biochim Biophys Acta-Gen Subjects 1426(2):335–345. https://doi.org/10.1016/S0304-4165(98)00134-2
Jung US, Levin DE (1999) Genome-wide analysis of gene expression regulated by the yeast cell wall integrity signalling pathway. Mol Microbiol 34(5):1049–1057. https://doi.org/10.1046/j.1365-2958.1999.01667.x
Kanetsuna F, Carbonell LM (1970) Cell wall glucans of the yeast and mycelial forms of Paracoccidioides brasiliensis. J Bacteriol 101(3):675–680
Klis FM, Mol P, Hellingwerf K, Brul S (2002) Dynamics of cell wall structure in Saccharomyces cerevisiae. FEMS Microbiol Rev 26(3):239–256. https://doi.org/10.1016/s0168-6445(02)00087-6
Klis FM, Boorsma A, De Groot PW (2006) Cell wall construction in Saccharomyces cerevisiae. Yeast 23(3):185–202. https://doi.org/10.1002/yea.1349
Komon-Zelazowska M, Bissett J, Zafari D, Hatvani L, Manczinger L, Woo S, Lorito M, Kredics L, Kubicek CP, Druzhinina IS (2007) Genetically closely related but phenotypically divergent Trichoderma species cause green mold disease in oyster mushroom farms worldwide. Appl Environ Microbiol 73(22):7415–7426. https://doi.org/10.1128/AEM.01059-07
Kredics L, Kocsube S, Nagy L, Komon-Zelazowska M, Manczinger L, Sajben E, Nagy A, Vagvolgyi C, Kubicek CP, Druzhinina IS, Hatvani L (2009) Molecular identification of Trichoderma species associated with Pleurotus ostreatus and natural substrates of the oyster mushroom. FEMS Microbiol Lett 300(1):58–67. https://doi.org/10.1111/j.1574-6968.2009.01765.x
Lagorce A, Le Berre-Anton V, Aguilar-Uscanga B, Martin-Yken H, Dagkessamanskaia A, François J (2002) Involvement of GFA1, which encodes glutamine-fructose-6-phosphate amidotransferase, in the activation of the chitin synthesis pathway in response to cell-wall defects in Saccharomyces cerevisiae. Eur J Biochem 269(6):1697–1707. https://doi.org/10.1046/j.1432-1327.2002.02814.x
Lesage G, Bussey H (2006) Cell wall assembly in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70(2):317–343. https://doi.org/10.1128/MMBR.00038-05
Levin DE (2005) Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 69(2):262–291. https://doi.org/10.1128/MMBR.69.2.262-291.2005
Levin DE (2011) Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189(4):1145–1175. https://doi.org/10.1534/genetics.111.128264
Liu Y, Flanagan JJ, Barlowe C (2004) Sec22p export from the endoplasmic reticulum is independent of SNARE pairing. J Biol Chem 279(26):27225–27232. https://doi.org/10.1074/jbc.M312122200
Mendoza CG (1992) Cell wall structure and protoplast reversion in basidiomycetes. World J Microbiol Biotechnol 8(1):36–38. https://doi.org/10.1007/BF02421486
Nishikawa A, Mendez B, Jigami Y, Dean N (2002) Identification of a Candida glabrata homologue of the S. cerevisiae VRG4 gene, encoding the Golgi GDP-mannose transporter. Yeast 19(8):691–698. https://doi.org/10.1002/yea.854
Oka T, Futagami T, Goto M (2015) Cell wall biosynthesis in filamentous fungi. In: Takagi H, Kitagaki H (eds) Stress biology of yeasts and fungi: applications for industrial brewing and fermentation. Springer Japan, Tokyo, pp 151–168
Orlean P (1997) Biogenesis of yeast wall and surface components. In: Pringle JR, Broach JR, Jones EW (eds) The molecular biology of the yeast Saccharomyces, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 229–362
Osumi M (1998) The ultrastructure of yeast: cell wall structure and formation. Micron 29(2–3):207–233. https://doi.org/10.1016/s0968-4328(97)00072-3
Qiu Z, Wu X, Zhang J, Huang C (2017) High temperature enhances the ability of Trichoderma asperellum to infect Pleurotus ostreatus mycelia. PLoS One 12(10):e0187055. https://doi.org/10.1371/journal.pone.0187055
Rees DA, Morris E, Thom D, Madden JK (1982) Shapes and interactions of carbohydrate chains. In: Aspinall GO (ed) The polysaccharides I. Academic Press, New York, pp 195–290
Shimma Y, Nishikawa A, bin Kassim B, Eto A, Jigami Y (1997) A defect in GTP synthesis affects mannose outer chain elongation in Saccharomyces cerevisiae. Mol Gen Genet 256(5):469–480. https://doi.org/10.1007/s004380050591
Smits GJ, Kapteyn JC, van den Ende H, Klis FM (1999) Cell wall dynamics in yeast. Curr Opin Microbiol 2(4):348–352. https://doi.org/10.1016/s1369-5274(99)80061-7
Sobering AK, Watanabe R, Romeo MJ, Yan BC, Specht CA, Orlean P, Riezman H, Levin DE (2004) Yeast Ras regulates the complex that catalyzes the first step in GPI-anchor biosynthesis at the ER. Cell 117(5):637–648. https://doi.org/10.1016/j.cell.2004.05.003
Song W, Dou X, Qi Z, Wang Q, Zhang X, Zhang H, Guo M, Dong S, Zhang Z, Wang P, Zheng X (2010) R-SNARE homolog MoSec22 is required for conidiogenesis, cell wall integrity, and pathogenesis of Magnaporthe oryzae. PLoS One 5(10):e13193. https://doi.org/10.1371/journal.pone.0013193
Staniszewska M, Bondaryk M, Swoboda-Kopec E, Siennicka K, Sygitowicz G, Kurzatkowski W (2013) Candida albicans morphologies revealed by scanning electron microscopy analysis. Braz J Microbiol 44:813–821
Ufano S, del Rey F, Vazquez de Aldana CR (2004) Swm1p, a subunit of the APC/cyclosome, is required to maintain cell wall integrity during growth at high temperature in Saccharomyces cerevisiae. FEMS Microbiol Lett 234(2):371–378. https://doi.org/10.1016/j.femsle.2004.04.006
Verna J, Lodder A, Lee K, Vagts A, Ballester R (1997) A family of genes required for maintenance of cell wall integrity and for the stress response in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 94(25):13804–13809. https://doi.org/10.1073/pnas.94.25.13804
Zhang S, Xia Y, Keyhani NO (2011) Contribution of the gas1 gene of the entomopathogenic fungus Beauveria bassiana, encoding a putative glycosylphosphatidylinositol-anchored β-1,3-glucanosyltransferase, to conidial thermotolerance and virulence. Appl Environ Microbiol 77(8):2676–2684. https://doi.org/10.1128/AEM.02747-10
Zhao C, Jung US, Garrett-Engele P, Roe T, Cyert MS, Levin DE (1998) Temperature-induced expression of yeast FKS2 is under the dual control of protein kinase C and calcineurin. Mol Cell Biol 18(2):1013–1022
Zhou H, Hu H, Zhang L, Li R, Ouyang H, Ming J, Jin C (2007) O-Mannosyltransferase 1 in Aspergillus fumigatus (AfPmt1p) is crucial for cell wall integrity and conidium morphology, especially at an elevated temperature. Eukaryot Cell 6(12):2260–2268. https://doi.org/10.1128/ec.00261-07
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This research was financially supported by the National Basic Research Program of China (2014CB138303), the China Agriculture Research System (CARS20), and the Beijing Municipal Science and Technology Project (D151100004315003).
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Qiu, Z., Wu, X., Gao, W. et al. High temperature induced disruption of the cell wall integrity and structure in Pleurotus ostreatus mycelia. Appl Microbiol Biotechnol 102, 6627–6636 (2018). https://doi.org/10.1007/s00253-018-9090-6
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DOI: https://doi.org/10.1007/s00253-018-9090-6