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The Secretome of Agaricus bisporus: Temporal Dynamics of Plant Polysaccharides and Lignin Degradation

Summary

This research investigated how white button mushrooms break down plant material during commercial mushroom production. The study revealed that mushrooms secrete different enzymes over time that work together to break down complex plant materials like cellulose and lignin. Understanding this process could help improve mushroom production and develop better ways to convert plant waste into useful products. Impacts on everyday life: • More efficient mushroom farming techniques could lead to lower production costs and more affordable mushrooms • Better understanding of natural biomass degradation could help develop greener industrial processes • Knowledge gained could help create new ways to recycle plant waste into valuable products • Improved understanding of fungal enzymes could lead to new industrial applications • Could contribute to more sustainable agriculture and waste management practices

Background

Plant biomass degradation is ubiquitous in nature, particularly in biodiverse systems inhabited by fungi and bacteria. The commercial substrate production process for the white button mushroom Agaricus bisporus represents an effective system for converting low-value lignocellulose to food products. While A. bisporus is known to encode many carbohydrate-active enzymes and oxidoreductases, its role in lignin degradation is not fully understood compared to typical white-rot fungi.

Objective

To investigate the relationship between oxidoreductases and delignification, determine if lignocellulose-degrading CAZymes are actively secreted, examine temporal dynamics of secretomes throughout A. bisporus mycelial growth in industrial substrate production compared to axenic lab cultures, and test the secretomes’ ability to degrade plant polysaccharides and modify dimeric lignin model compounds.

Results

Secretomes from day 6-15 contained A. bisporus endo-acting and substituent-removing glycoside hydrolases, while β-xylosidase and glucosidase activities gradually decreased. Laccases appeared from day 6 onwards. From day 10 onwards, many oxidoreductases were found, including multicopper oxidases, aryl alcohol oxidases, glyoxal oxidases, manganese peroxidase, and unspecific peroxygenases. The secretomes modified dimeric lignin models by catalyzing syringylglycerol-β-guaiacyl ether cleavage, guaiacylglycerol-β-guaiacyl ether polymerization, and non-phenolic veratrylglycerol-β-guaiacyl ether oxidation.

Conclusion

A. bisporus secretomes contain a diverse mix of lignocellulose-active enzymes that show temporal dynamic changes during substrate colonization. The protein composition of later stage industrial secretomes largely matched secretomes from axenic cultures. Multiple oxidoreductases were detected that can modify lignin compounds through various mechanisms. Understanding this enzymatic machinery could help optimize substrate utilization efficiency and inform future biorefinery applications.
  • Published in:iScience,
  • Study Type:Laboratory Research,
  • Source: 10.1016/j.isci.2023.107087
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