Enlightening Gliotoxin Biological System in Agriculturally Relevant Trichoderma spp.

Abstract

Gliotoxin (GT) is a dual fungal secondary metabolite (SM). It displays pleiotropic activities and possesses medicinal properties and biocontrol abilities but, unfortunately, has toxic properties in humans. Various <i>Trichoderma</i> species are used as fungal biological control agents (BCAs), as a sustainable alternative for crop protection worldwide. Among them is <i>Trichoderma virens</i>, a GT-producing fungus. Since no information was available on the genetically coded prerequisites for the production of GT in other <i>Trichoderma</i> spp., genome analyses were carried out in 10 <i>Trichoderma</i> spp. genomes. Moreover, a real-time PCR assay setup <i>ad hoc</i> and high-performance liquid chromatography (HPLC) analyses were employed to understand the GT-producing biological systems in <i>T. virens</i> GV29-8 (TvGv29-8) and <i>Trichoderma afroharzianum</i> T6776 (TaT6776), two relevant biocontrol fungi. The structure of the GT biosynthesis genes (GT-BG) is polymorphic, with two distinct types associated with the ability to produce GT. GliH, a key protein for GT synthesis, is absent in most of the <i>Trichoderma</i> GT biosynthetic pathways, which may be the reason for their inability to produce GT. The GT-BG are expressed in TvGv29-8 as expected, while they are silent in TaT6776. Interestingly, in the GT-non-producing TaT6776, only <i>gliA</i> (putative GT transporter) and <i>gtmA</i> (putative GT <i>S</i>-methyltransferase) were induced by exogenous GT, underlining the ability of this strain to reduce the deleterious effect of the toxin. This ability is confirmed by growth assays and by the detection of the bis-thiomethylated form of GT catalyzed by GtmA in the culture medium supplemented with GT. To the best of our knowledge, this is the first general description of the GT biological system in different <i>Trichoderma</i> spp. as far as the GT-BG content and organization is concerned and a preliminary insight into their functionality.