Chitin and chitosan remodeling defines vegetative development and Trichoderma biocontrol

Fungal parasitism depends on the ability to invade host organisms and mandates adaptive cell wall remodeling to avoid detection and defense reactions by the host. All plant and human pathogens share invasive strategies, which aid to escape the chitin-triggered and chitin-targeted host immune system. Here we describe the full spectrum of the chitin/chitosan-modifying enzymes in the mycoparasite Trichoderma atroviride with a central role in cell wall remodeling. Rapid adaption to a variety of growth conditions, environmental stresses and host defense mechanisms such as oxidative stress depend on the concerted interplay of these enzymes and, ultimately, are necessary for the success of the mycoparasitic attack. To our knowledge, we provide the first in class description of chitin and associated glycopolymer synthesis in a mycoparasite and demonstrate that they are essential for biocontrol. Eight chitin synthases, six chitin deacetylases, additional chitinolytic enzymes, including six chitosanases, transglycosylases as well as accessory proteins are involved in this intricately regulated process. Systematic and biochemical classification, phenotypic characterization and mycoparasitic confrontation assays emphasize the importance of chitin and chitosan assembly in vegetative development and biocontrol in T. atroviride. Our findings critically contribute to understanding the molecular mechanism of chitin synthesis in filamentous fungi and mycoparasites with the overarching goal to selectively exploit the discovered biocontrol strategies. Author summary Fungal pathogens pose an emerging threat in crop production and thus human health. Trichoderma atroviride is considered a potential biocontrol agent against a broad spectrum of phytopathogens. Cell wall chitin was identified as promising target to combat fungal diseases. Here we uncovered the regulation of chitin and chitosan synthesis and their contribution to dynamic cell wall remodeling as protective components in self-defense reactions during the mycoparasitic attack of Trichoderma. The systematic evaluation of the newly identified chitin-modifying enzymes confirmed their concerted interplay and their essential contribution to a successful mycoparasitic invasion. These findings provide further valuable, more specific information on targeting critical factors in the fungal cell wall adaptation process for therapeutic purposes as well as improved biocontrol applications.