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Title: 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. weberimore » 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.« less

Authors:
ORCiD logo [1];  [1];  [2];  [3];  [4];  [4]; ORCiD logo [1];  [1]; ORCiD logo [5];  [1]; ORCiD logo [6];  [1];  [1]; ORCiD logo [7]; ORCiD logo [8];  [8];  [8];  [8];  [8];  [8] more »; ORCiD logo [8];  [8];  [9];  [4];  [1];  [10] « less
+ Show Author Affiliations
  1. TU Wien, Vienna (Austria)
  2. Nanjing Univ. (China)
  3. TU Wien, Vienna (Austria); Univ. of Natural Resources and Life Sciences–BOKU, Vienna (Austria)
  4. Nanjing Agricultural Univ., Nanjing (China)
  5. TU Wien, Vienna (Austria); Nanjing Agricultural Univ., Nanjing (China)
  6. Univ. Brunei Brunei (Darussalam)
  7. Aix-Marseille Univ., Marseille (France); INRA, USC, Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
  8. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  9. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
  10. (France)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, Oakland, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); Austrian Science Fund (FWF); National Natural Science Foundation of China (NSFC); Chinese Ministry of Science and Technology
OSTI Identifier:
1544030
Alternate Identifier(s):
OSTI ID: 1619097
Grant/Contract Number:  
AC02-05CH11231; P25613-B20; WWTF-LS13-048; 31330069; 2015CB150500
Resource Type:
Accepted Manuscript
Journal Name:
PLoS Genetics
Additional Journal Information:
Journal Volume: 14; Journal Issue: 4; Journal ID: ISSN 1553-7404
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Genetics & Heredity

Citation Formats

Druzhinina, Irina S., Chenthamara, Komal, Zhang, Jian, Atanasova, Lea, Yang, Dongqing, Miao, Youzhi, Rahimi, Mohammad J., Grujic, Marica, Cai, Feng, Pourmehdi, Shadi, Salim, Kamariah Abu, Pretzer, Carina, Kopchinskiy, Alexey G., Henrissat, Bernard, Kuo, Alan, Hundley, Hope, Wang, Mei, Aerts, Andrea, Salamov, Asaf, Lipzen, Anna, LaButti, Kurt, Barry, Kerrie, Grigoriev, Igor V., Shen, Qirong, Kubicek, Christian P., and Martin, Francis. Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts. United States: N. p., 2018. Web. doi:10.1371/journal.pgen.1007322.
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Druzhinina, Irina S., Chenthamara, Komal, Zhang, Jian, Atanasova, Lea, Yang, Dongqing, Miao, Youzhi, Rahimi, Mohammad J., Grujic, Marica, Cai, Feng, Pourmehdi, Shadi, Salim, Kamariah Abu, Pretzer, Carina, Kopchinskiy, Alexey G., Henrissat, Bernard, Kuo, Alan, Hundley, Hope, Wang, Mei, Aerts, Andrea, Salamov, Asaf, Lipzen, Anna, LaButti, Kurt, Barry, Kerrie, Grigoriev, Igor V., Shen, Qirong, Kubicek, Christian P., & Martin, Francis. Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts. United States. https://doi.org/10.1371/journal.pgen.1007322
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Druzhinina, Irina S., Chenthamara, Komal, Zhang, Jian, Atanasova, Lea, Yang, Dongqing, Miao, Youzhi, Rahimi, Mohammad J., Grujic, Marica, Cai, Feng, Pourmehdi, Shadi, Salim, Kamariah Abu, Pretzer, Carina, Kopchinskiy, Alexey G., Henrissat, Bernard, Kuo, Alan, Hundley, Hope, Wang, Mei, Aerts, Andrea, Salamov, Asaf, Lipzen, Anna, LaButti, Kurt, Barry, Kerrie, Grigoriev, Igor V., Shen, Qirong, Kubicek, Christian P., and Martin, Francis. Mon . "Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts". United States. https://doi.org/10.1371/journal.pgen.1007322. https://www.osti.gov/servlets/purl/1544030.
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@article{osti_1544030,
title = {Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts},
author = {Druzhinina, Irina S. and Chenthamara, Komal and Zhang, Jian and Atanasova, Lea and Yang, Dongqing and Miao, Youzhi and Rahimi, Mohammad J. and Grujic, Marica and Cai, Feng and Pourmehdi, Shadi and Salim, Kamariah Abu and Pretzer, Carina and Kopchinskiy, Alexey G. and Henrissat, Bernard and Kuo, Alan and Hundley, Hope and Wang, Mei and Aerts, Andrea and Salamov, Asaf and Lipzen, Anna and LaButti, Kurt and Barry, Kerrie and Grigoriev, Igor V. and Shen, Qirong and Kubicek, Christian P. and Martin, Francis},
abstractNote = {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.},
doi = {10.1371/journal.pgen.1007322},
journal = {PLoS Genetics},
number = 4,
volume = 14,
place = {United States},
year = {2018},
month = {4}
}
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https://doi.org/10.1371/journal.pgen.1007322
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Inferring duplications, losses, transfers and incomplete lineage sorting with nonbinary species trees.
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    Evolution and functional characterization of pectate lyase PEL12, a member of a highly expanded Clonostachys rosea polysaccharide lyase 1 family
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