Abstract
Agaricus bisporus is the most widely cultivated edible mushroom in the world. Strain quality has an important influence on the yield of A. bisporus, with strains that exhibit aging being a common problem during cultivation. However, little is known about the aging mechanisms of A. bisporus strain. In this study, the normal A. bisporus As2796 strain was compared to the aging A. bisporus As2796Y strain (which was previously discovered during cultivation). In the aging As2796Y mycelia, the mycelial growth rate and fruiting body yield were decreased and the chitin level and cell wall thickness were increased. Additionally, intracellular vacuoles increased, there was cytoplasmic shrinkage, and the sterol level which stabilizes the cell membrane decreased, which led to cytoplasmic outflow and the exudation of a large amount of yellow water from the mycelia. Additionally, there was increased electrolyte leakage. Furthermore, gas chromatography-mass spectrometry (GC/MS) was used to profile the metabolic changes in the aging As2796Y mycelia compared to the normal As2796 mycelia. A total of 52 differential metabolites were identified (75% were downregulated and 25% were upregulated in As2796Y). The reduction of many metabolites decreased the mycelial viability and the ability to maintain cell stability. Overall, this study is the first to report on the morphologic and metabolic changes in aged A. bisporus mycelia, which will aid future research on the mechanisms underlying A. bisporus mycelial aging.
Key points
• Aging of Agaricus bisporus strains will greatly reduce the fruiting body yield.
• Aging of Agaricus bisporus strains can significantly change the cell structure of mycelia.
• Many metabolites in the mycelium of aging spawn As2796Y significantly changed.
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Data availability
All data generated or analyzed during this study are available from the corresponding author on reasonable request.
References
Abu-Seidah AA (2007) Effect of salt stress on amino acids, organic acids and ultra-structure of Aspergillus flavus and Penicillium roquefortii. Int J Agric Biol 9:419–425
Aguilar-Uscanga B, Francois JM (2010) A study of the yeast cell wall composition and structure in response to growth conditions and mode of cultivation. Lett Appl Microbiol 37:268–274. https://doi.org/10.1046/j.1472-765x.2003.01394.x
Bischof O, Martínez-Zamudio RI (2015) MicroRNAs and lncRNAs in senescence: a re-view. IUBMB Life 67:255–267. https://doi.org/10.1002/iub.1373
Bok JW, Ishida KI, Griffiths AJF (2003) Ultrastructural changes in Neurospora cells undergoing senescence induced by kalilo plasmids. Mycologia 95:500–505. https://doi.org/10.1080/15572536.2004.11833095
Brilhante RSN, Caetano EP, Lima RAC, Castelo Branco DSCM, Serpa R, Oliveira JS, Monteiro AJ, Rocha MFG, Cordeiro RA, Sidrim JJC (2015) In vitro antifungal activity of miltefosine and levamisole: their impact on ergosterol biosynthesis and cell permeability of dimorphic fungi. J Appl Microbiol 119:962–969. https://doi.org/10.1111/jam.12891
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 2:886–900. https://doi.org/10.1128/ec.2.5.886-900.2003
Chander SS (2006) Implications of sterol structure for membrane lipid composition, fluidity and phospholipid asymmetry in Saccharomyces cerevisiae. FEMS Yeast Res 6:1047–1051. https://doi.org/10.1111/j.1567-1364.2006.00149.x
Chen MY, Liao JH, Li HR, Cai ZX, Guo ZJ, Wang ZS (2015) Developmental proteomics analysis of the button mushroom Agaricus bisporus. Mycosystema 34:1153–1164. https://doi.org/10.13346/j.mycosystema.140188
Davies FL, Lin FK, Gottieb D (1974) Synthesis of RNA with relation to aging in Rhizoctonia solani. Arch Microbiol 95:145–122. https://doi.org/10.1007/BF02451756
D’souza AD, Maheshwari R (2002) Senescence in fungi. Resonance 7:51–55. https://doi.org/10.1007/BF02896308
Davis DJ, Burlak C, Money NP (2000) Osmotic pressure of fungal compatible osmolytes. Mycol Res 104:800–804. https://doi.org/10.1017/s0953756299002087
Donker HCW, As HV (1999) Cell water balance of white button mushrooms (Agaricus bisporus) during its post-harvest lifetime studied by quantitative magnetic resonance imaging. Biochim Biophys Acta 1427:287–297. https://doi.org/10.1016/s0304-4165(99)00027-6
Galinski E, Trüper H (1994) Microbial behaviour in salt-stressed ecosystems. FEMS Microbiol Rev 15:95–108. https://doi.org/10.1111/j.1574-6976.1994.tb00128.x
García R, Botet J, Manuel J, 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
Goldberg I, Rokem JS, Pines O (2010) Organic acids: old metabolites, new themes. J Chem Technol Biotech 81:1601–1611. https://doi.org/10.1002/jctb.1590
Gull K, Trinci APJ (1974) Detection of areas of wall differentiation in fungi using fluorescent staining. Arch Microbiol 96:53–57. https://doi.org/10.1007/BF00590162
Hu L, Wang Z, Du H, Huang B (2010) Differential accumulation of dehydrins in response to water stress for hybrid and common bermudagrass genotypes differing in drought tolerance. J Plant Physiol 167:103–109. https://doi.org/10.1016/j.jplph.2009.07.008
Jazwinski SM (2007) Models of aging: invertebrates, filamentous fungi, and yeasts. Encyclopedia of Gerontology Louisiana State University Health Sciences Center, New Orleans, LA, USA
Klamer M, Bååth E (2004) Estimation of conversion factors for fungal biomass determination in compost using ergosterol and PLFA 18:2ω6,9. Soil Biol Biochem 36:57–65. https://doi.org/10.1016/j.soilbio.2003.08.019
Klionsky DJ, Herman PK, Emr SD (1990) The fungal vacuole: composition, function, and biogenesis. Microbiol Rev 54:266–292
Lei M, Wu X, Huang C, Qiu Z, Zhang J (2019) Trehalose induced by reactive oxygen species relieved the radial growth defects of Pleurotus ostreatus under heat stress. Appl Microbiol Biotechnol 103:5379–5390. https://doi.org/10.1007/s00253-019-09834-8
Levin DE (2011) Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189:1145–1175. https://doi.org/10.1534/genetics.111.128264
Lu S, Chen C, Wang Z, Guo Z, Li H (2009) Physiological responses of somaclonal variants of triploid bermudagrass (Cynodon transvaalensis x Cynodon dactylon) to drought stress. Plant Cell Rep 28:517–526. https://doi.org/10.1007/s00299-008-0649-z
Mager WH, Varela JC (2010) Osmostress response of the yeast Saccharomyces. Mol Microbiol 10:253–258. https://doi.org/10.1111/j.1365-2958.1993.tb01951.x
Mamiro DP, Royse DJ (2008) The influence of spawn type and strain on yield, size and mushroom solids content of Agaricus bisporus produced on non-composted and spent mushroom compost. Bioresour Technol 99:3205–3212. https://doi.org/10.1016/j.biortech.2007.05.073
Marchant R, Smith DG (1968) A serological investigation of hyphal growth in Fusarium culmorum. Archiv Microbiol 63:85–94. https://doi.org/10.1007/BF00407067
Mendoza CG (1992) Cell wall structure and protoplast reversion in basidiomycetes. World J Microbiol Biotechnol 1:36–38. https://doi.org/10.1007/BF02421486
Moros G, Chatziioannou AC, Gika HG, Raikos N, Theodoridis G (2017) Investigation of the derivatization conditions for GC-MS metabolomics of biological samples. Bioanalysis 9:53–65. https://doi.org/10.4155/bio-2016-0224
Niederpruem DJ (1965) Carbohydrate metabolism. 2. Tricarboxylic acid cycle. In The Fungi, eds. G. C. Ainsworth, A. S. Sussman (New York-London: Academic Press), pp 269-300
Osiewacz HD (2002) Genes, mitochondria and aging in filamentous fungi. Ageing Res Rev 1:425–442. https://doi.org/10.1016/s1568-1637(02)00010-7
Osiewacz HD, Stumpferl SW (2001) Metabolism and aging in the filamentous fungus Podospora anserina. Arch Gerontol Geriatr 32:185–197. https://doi.org/10.1016/s0167-4943(01)00096-6
Pallavi RMV, Ramana D, Sashidhar RB (1997) Synthesis of the antigen bovine serum albumin-ergosterol and its immunocharacterization. Food Agr Immunol 9:85–95. https://doi.org/10.1080/09540109709354939
Papagianni M (2004) Fungal morphology and metabolite production in submerged mycelial processes. Biotechnol Adv 22:189–259. https://doi.org/10.1016/j.biotechadv.2003.09.005
Paul GC, Kent CA, Thomas CR (2010) Hyphal vacuolation and fragmentation in Penicillium chrysogenum. Biotechnol Bioeng 44:655–660. https://doi.org/10.1002/bit.260440513
Qiu ZH, Wu XL, Zhang JX, Huang CY (2018) High-temperature induced changes of extracellular metabolites in Pleurotus ostreatus and their positive effects on the growth of Trichoderma asperellum. Front Microbiol 9:10. https://doi.org/10.3389/fmicb.2018.00010
Sahin E, Akata I (2018) Viruses Infecting Macrofungi Virus Dis 29:1–18. https://doi.org/10.1007/s13337-018-0434-8
Shi H, Wang Y, Cheng Z, Ye T, Chan Z (2012) Analysis of natural variation in bermudagrass (Cynodon dactylon) reveals physiological responses underlying drought tolerance. PLoS ONE 7:e53422. https://doi.org/10.1371/journal.pone.0053422
Sonnenberg AS, Baars JJ, Gao W, Visser RG (2017) Developments in breeding of Agaricus bisporus var. bisporus: progress made and technical and legal hurdles to take. Appl Microbiol Biotechnol 101:1819–1829. https://doi.org/10.1007/s00253-017-8102-2
Todd RB, Lockington RA, Kelly JM (2000) The Aspergillus nidulans creC gene involved in carbon catabolite repression encodes a WD40 repeat protein. Mol Gen Genet 263:561–570. https://doi.org/10.1007/s004380051202
Umar M, Van Griensven L (1997) Morphological studies on the life span, developmental stages, senescence and death of fruit bodies of Agaricus bisporus. Mycol Res 101:1409–1422. https://doi.org/10.1017/S0953756297005212
Verstichel A (1971) Hyphal wall synthesis in Aspergillus nidulans: effect of protein synthesis inhibition and osmotic shock on chitin insertion and morphogenesis. J Bacteriol 108:184–190. https://doi.org/10.1128/JB.108.1.184-190.1971
Wang B, Xu XH, Yuan L (2011) Morphological studies on senescence of vegetative mycelium of Agaricus bisporus. J Northeast Agr Univ 42:99–103. https://doi.org/10.19720/j.cnki.issn.1005-9369.2011.05.019
Wang HX, Wang ZS (2005) A brief review of the breeding and cultivation of button mushroom Agaricus bisporus (J. Lge) Imbach in China with the promotion of professor Shu-ting Chang. Int J Med Mushrooms 7:15–22. https://doi.org/10.1615/IntJMedMushr.v7.i12.30
Worley B, Powers R (2016) PCA as a practical indicator of OPLS-DA model reliability. Curr Metabolomic 4:97–103. https://doi.org/10.2174/2213235X04666160613122429
Xu XH, Sheng SY, Zhu HF, Li DT (2019) Effect of additives on aging of liquid spawn of Auricularia auricula. J Northeast Agr Univ 50:19–27. https://doi.org/10.19720/j.cnki.issn.1005-9369.2019.09.003
Yang GL (2004) Mushroom Production Book. China Agricultural Press, Beijing
You FQ (2015) Sustainability of products, processes and supply chains: theory and applications. Northwestern University, Evanston, IL, USA. pp 311–329. https://doi.org/10.1016/B978-0-444-63472-6.00012-4.
Zhang HL, Wei JK, Wang QH, Yang R, Gao XJ, Sang YX, Cai PP, Zhang GQ, Chen QJ (2018) Lignocellulose utilization and bacterial communities of millet straw based mushroom (Agaricus bisporus) production. Sci Rep 9:1151. https://doi.org/10.1038/s41598-018-37681-6
Zhang S, Xia Y, Keyhani NO (2011) Contribution of the gas1 gene of the entomopathogenic fungus Beauveria bassiana, encoding a putative glycosylphosphatidylinositol-anchored beta-1,3-glucanosyltransferase, to conidial thermotolerance and virulence. Appl Environ Microbiol 77:2676–2684. https://doi.org/10.1128/AEM.02747-10
Funding
This study was supported by the Fundamental Research Project for Public Welfare Scientific Research Institutes in Fujian (2015R1020-2), China Agriculture Research System (CARS20), Breeding Project for NNSF in FAAS (AGP2018-5), Fujian Regional Development Project (2020N3009), Special Fund for Agro-scientific Research in the Public Interest (201503137), National Natural Science Foundation of China (31701977), International Agro-biological Resources and the Collection of Information about Agro-technic Demands and Agricultural Strategies (2016-X07).
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ZH and CM: conceived, designed, and analyzed the data. SL wrote and performed the experiments. ZZ checked the final version. DJ, CY, and LY contributed new reagents or analytical tools. XW and CH: revised the manuscript. All authors have read and approved the manuscript.
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Lili Shu and Zhiheng Zeng are co-first authors.
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Shu, L., Zeng, Z., Dai, J. et al. Morphological and metabolic changes in an aged strain of Agaricus bisporus As2796. Appl Microbiol Biotechnol 105, 7997–8007 (2021). https://doi.org/10.1007/s00253-021-11526-1
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DOI: https://doi.org/10.1007/s00253-021-11526-1