| Summary: | Mycoviruses widely exist in filamentous fungi and sometimes cause phenotypic changes in hosts. <i>Trichoderma harzianum</i> hypovirus 1 (ThHV1) and its defective RNA ThHV1-S were found in <i>T. harzianum</i> and exhibited high transmissibility. In our previous study, ThHV1 and ThHV1-S were transferred to an excellent biological control agent <i>T. koningiopsis</i> T-51 to form a derivative strain 51-13. In this study, we assessed the metabolic changes in strain 51-13 and antifungal activity of its culture filtrate (CF) and volatile organic compounds (VOCs). The antifungal activity of CF and VOCs of T-51 and 51-13 was different. Compared with the CF of T-51, that of 51-13 exhibited high inhibitory activity against <i>B. cinerea</i>, <i>Sclerotinia sclerotiorum</i>, and <i>Stagonosporopsis cucurbitacearum</i> but low inhibitory activity against <i>Leptosphaeria biglobosa</i> and <i>Villosiclava virens</i>. The VOCs of 51-13 exhibited high inhibitory activity against <i>F. oxysporum</i> but low inhibitory activity against <i>B. cinerea</i>. The transcriptomes of T-51 and 51-13 were compared; 5531 differentially expressed genes (DEGs) were identified in 51-13 with 2904 up- and 2627 downregulated genes. In KEGG enrichment analysis, 1127 DEGs related to metabolic pathways (57.53%) and 396 DEGs related to biosynthesis of secondary metabolites (20.21%) were clearly enriched. From the CF of T-51 and 51-13, 134 differential secondary metabolites (DSMs) were detected between T-51 and 51-13 with 39 up- and 95 downregulated metabolites. From these, 13 upregulated metabolites were selected to test their antifungal activity against <i>B. cinerea</i>. Among them, indole-3-lactic acid and p-coumaric acid methyl ester (MeCA) exhibited strong antifungal activity. The IC<sub>50</sub> of MeCA was 657.35 μM and four genes possibly related to the synthesis of MeCA exhibited higher expression in 51-13 than in T-51. This study revealed the mechanism underlying the increase in antifungal activity of T-51 because of the mycovirus and provided novel insights in fungal engineering to obtain bioactive metabolites via mycoviruses.
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