Igor V. Grigoriev, Youzhi Miao, Alexey G. Kopchinskiy, Irina S. Druzhinina, Kurt LaButti, Shadi Pourmehdi, Asaf Salamov, Kamariah Abu Salim, Kerrie Barry, Jian Zhang, Lea Atanasova, Mohammad Javad Rahimi, Bernard Henrissat, Hope Hundley, Qirong Shen, Alan Kuo, Anna Lipzen, Komal Chenthamara, Feng Cai, Christian P. Kubicek, Marica Grujic, Andrea Aerts, Carina Pretzer, Dongqing Yang, Mei Wang, Research Area Biotechnology and Microbiology, Technical University of Vienna [Vienna] (TU WIEN)-Institute of Chemical Engineering, Technische Universität Wien (TU Wien), Laboratoire de Linguistique Formelle (LLF UMR7110), Centre National de la Recherche Scientifique (CNRS)-Université Paris Diderot - Paris 7 (UPD7), Nanjing Agricultural University, Fac Sci, Environm & Life Sci, University of Brunei Darussalam (Biology Department), Universiti Brunei Darussalam, Architecture et fonction des macromolécules biologiques (AFMB), Institut National de la Recherche Agronomique (INRA)-Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), US Department of Energy Joint Genome Institute, U.S Department of Energy, U.S. Department of Energy (DOE)-U.S. Department of Energy (DOE), Dept Energy Great Lakes Bioenergy Res Ctr, Joint Genome institute, United States Department of Energy, Joint Genome Institute, Department of Energy / Joint Genome Institute (DOE), Los Alamos National Laboratory (LANL), ANR-17-CE34-0002,EMBRASE,Environnement MicroBiologique et Risque Allergique, Suivi des Enfants à 5 ans(2017), Vienna University of Technology (TU Wien)-Institute of Chemical Engineering, Vienna University of Technology (TU Wien), Université Paris Diderot - Paris 7 (UPD7)-Centre National de la Recherche Scientifique (CNRS), Nanjing Agricultural University (NAU), U.S. Department of Energy [Washington] (DOE)-U.S. Department of Energy [Washington] (DOE), Austrian Science Fund (FWF) [P 25613 B20], Office of Science of the U.S. Department of Energy [DE-AC02-05CH11231], National Natural Science Foundation of China [31330069], Chinese Ministry of Science and Technology (973 Program) [2015CB150500], IDEX Aix-Marseille (Grant Microbio-E), Kuala Belalong Field Studies Centre [WWTF-LS13-048], Martin, Francis, Centre National de la Recherche Scientifique (CNRS)-Aix Marseille Université (AMU)-Institut National de la Recherche Agronomique (INRA), Druzhinina, Irina S., and Shen, Qirong
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., Author summary Individual fungi rely on particular host organisms or substrates for their nutrition. Therefore, the genomes of fungi feeding on plant biomass necessarily contain genes encoding plant cell wall-degrading enzymes, while animal parasites may depend on proteolytic activity. Molds in the genus Trichoderma (Ascomycota) display a unique nutritional versatility. They can feed on other fungi, attack animals, and degrade plant debris. The later property is so efficient that one species (T. reesei) is commercially used for the production of cellulolytic enzymes required for making biofuels and other industry. In this work, we have investigated the evolution of proteins required for plant cell wall degradation in nine Trichoderma genomes and found an unprecedented number of lateral gene transfer (LGT) events for genes encoding these enzymes. Interestingly, the transfers specifically occurred from Ascomycota molds that feed on plants. We detected no cases of LGT from other fungi (e.g., mushrooms or wood-rotting fungi from Basidiomycota) that are frequent hosts of Trichoderma. Therefore, we propose that LGT may be linked to the ability of Trichoderma to parasitize on related organisms. This is a characteristic ecological trait that distinguishes Trichoderma from other mycoparasitic fungi. In this report, we demonstrate that the lateral transfer of genes may result in a profound nutritional expansion and contribute to the emergence of a generalist capable of feeding on organic matter of any origin.