Dual Regulatory Role of Chromatin Remodeler ISW1 in Coordinating Cellulase and Secondary Metabolite Biosynthesis in Trichoderma reesei

Abstract

The saprophytic filamentous fungus Trichoderma reesei represents one of the most prolific cellulase producers isolated from nature. <i>T. reesei</i> also produces a typical yellow pigment identified as sorbicillinoids during cultivation. Here, we identified an evolutionarily conserved histone remodeling factor, ISW1, in <i>T. reesei</i> that simultaneously participates in regulating cellulase and the yellow pigment biosynthesis. <i>Trisw1</i> deletion almost abolished vegetable growth, asexual spore formation, and cellulase gene expression. However, its absence significantly enhanced the production of the yellow pigment. The observed dual regulatory role of TrISW1 was dependent on its ATPase activity. We demonstrated that <i>Trisw1</i> disruption elevated the transcription of <i>ypr1</i> coding for the transcriptional activator of <i>sor</i> genes encoding the polyketide synthases catalyzing the biosynthesis of sorbicillinoids but compromised that of <i>xyr1</i> encoding the key transcriptional activator of cellulase genes. Discrete <i>T. reesei</i> homologous ISW1 accessory factors were also found to exert differential effects on the expression of these two types of genes. Further analyses showed that TrISW1 was recruited to cellulase gene promoters, and its absence interfered with loss of histone H4 at the <i>cbh1</i> and <i>eg1</i> promoters upon cellulose induction. To the contrary, <i>Trisw1</i> deletion facilitated loss of H4 at the <i>sor</i> locus. These data indicate that TrISW1 represents an important chromatin remodeler with a dual role in coordinating the cellulolytic response and biosynthesis of the major secondary metabolite in <i>T</i>. <i>reesei</i>. <b>IMPORTANCE</b> Microorganisms, including Trichoderma reesei, constantly face the challenge to outcompete other species to ensure efficient colonization in their natural habitat. They achieve this usually by adopting two alternative strategies by either maintaining fast growth on limited nutrient resources or producing a versatile array of secondary metabolites to fight against competitors. These two strategies, however, have to be subtly controlled to balance the assignment of and thus make the best use of cellular resources. Here, we identified a chromatin remodeling factor, TrISW1, with a dual role in coordinating the cellulolytic response and biosynthesis of the major secondary metabolite in <i>T. reesei</i>. The data also provide a novel insight into how <i>T. reesei</i> takes advantage of a chromatin remodeler to exquisitely balance two different adaptive strategies to ensure an efficient allocation of cellular resources to achieve efficient colonization in a specific environment.