Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts

Abstract

Unlike most other fungi, molds of the genus Trichoderma (Hypocreales, Ascomycota) are aggressive parasites of other fungi and efficient decomposers of plant biomass. Although nutritional shifts are common among hypocrealean fungi, there are no examples of such broad substrate versatility as that observed in Trichoderma. A phylogenomic analysis of 23 hypocrealean fungi (including nine Trichoderma spp. and the related Escovopsis weberi) revealed that the genus Trichoderma has evolved from an ancestor with limited cellulolytic capability that fed on either fungi or arthropods. The evolutionary analysis of Trichoderma genes encoding plant cell wall-degrading carbohydrate-active enzymes and auxiliary proteins (pcwdCAZome, 122 gene families) based on a gene tree / species tree reconciliation demonstrated that the formation of the genus was accompanied by an unprecedented extent of lateral gene transfer (LGT). Nearly one-half of the genes in Trichoderma pcwdCAZome (41%) were obtained via LGT from plant-associated filamentous fungi belonging to different classes of Ascomycota, while no LGT was observed from other potential donors. In addition to the ability to feed on unrelated fungi (such as Basidiomycota), we also showed that Trichoderma is capable of endoparasitism on a broad range of Ascomycota, including extant LGT donors. This phenomenon was not observed in E. weberi and rarely in other mycoparasitic hypocrealean fungi. Thus, our study suggests that LGT is linked to the ability of Trichoderma to parasitize taxonomically related fungi (up to adelphoparasitism in strict sense). This may have allowed primarily mycotrophic Trichoderma fungi to evolve into decomposers of plant biomass.

A comparative genomics study of 23 Aspergillus species from section Flavi

“…This could be similar to the case of T. reesei, which also has a reduced CAZyme gene set, but produces the corresponding enzymes at very high levels 56 . However, the origin of this approach is likely very different as its CAZyme content was shaped by loss and then massive HGT gain of plant cell wall degrading enzymes 57 , while no indications for this are present for A. coremiiformis.…”

Guttation capsules containing hydrogen peroxide: an evolutionarily conserved NADPH oxidase gains a role in wars between related fungi

“…While investigating the interactions between Trichoderma spp. and other hypocrealean fungi (Chenthamara and Druzhinina, 2016;Druzhinina et al, 2018), we noticed that a strain of Fusarium oxysporum f. sp. cubense 4 TUCIM 4848 (Foc4), was highly resistant to antagonism by various Trichoderma species, and only Trichoderma guizhouense NJAU 4742 (Tgui) repeatedly overgrew it in dual confrontation assays (Supporting Information S1).…”

“…The genome of Tgui harbours 11 255 genes (Druzhinina et al, 2018). When the fungus was in contact with Foc4, •− is stained dark blue by nitro blue tetrazolium, H 2 O 2 is visualized as the reddish brown colour that developed due to the presence of diaminobenzidine and horseradish peroxidase.…”

“…The other sector of interest in fungus-fungus opposition is the interaction between so-called plant-beneficial fungi and plant pathogens. For example, if conditions are appropriate, practically any species of Trichoderma (Hypocreales, Ascomycota) can directly attack a given plant pathogenic fungus, inhibit its growth by chemicals or beat it in a competition for the resources (Komon-Zelazowska et al, 2007;Jaklitsch, 2009;Seidl et al, 2009;Jaklitsch, 2011;Atanasova et al, 2013;Steindorff et al, 2014;Zhang et al, 2016;Druzhinina et al, 2018). The multitude of these Trichoderma interactions is used in the biological control of fungal pests (biocontrol) (Druzhinina et al, 2011).…”

Chitin and chitosan remodeling defines vegetative development and Trichoderma biocontrol

“…All cda knockout lines demonstrated severe defects in overgrowth of S. sclerotiorum ( Fig 7A) and B. cinerea and less pronounced with R. solani (S7A Fig). This behavior of T. atroviride to parasitize closely related phytopathogenic Ascomycota [96,97] is considered to be the major trait that sets Trichoderma apart from the other mycoparasitic Hypocreaceae that mainly attack Basidiomycota. Interestingly, while the parental strain was able to entirely overgrow S. sclerotiorum within 5 days (overgrowth is marked with a dotted line), the Δcda mutants completely stalled growth already during the early phase of interaction, i.e.…”