Daly et al. 2021 From lignocellulose to plastics: Knowledge transfer on the degradation approaches by fungi

Daly-et-al-2021-featured-image

Daly P, Cai F, Kubicek CP, Jiang S, Grujic M, Rahimi MJ, Sheteiwy MS, Giles R, Riaz A, de Vries RP, Bayram Akcapinar G, Wei L, Druzhinina IS (2021) From lignocellulose to plastics: Knowledge transfer on the degradation approaches by fungi, Biotechnology Advances, 50,
107770, https://doi.org/10.1016/j.biotechadv.2021.107770.

In this review, we argue that there is much to be learned by transferring knowledge from research on lignocellulose degradation to that on plastic. Plastic waste accumulates in the environment to hazardous levels, because it is inherently recalcitrant to biological degradation. Plants evolved lignocellulose to be resistant to degradation, but with time, fungi became capable of utilising it for their nutrition. Examples of how fungal strategies to degrade lignocellulose could be insightful for plastic degradation include how fungi overcome the hydrophobicity of lignin (e.g. production of hydrophobins) and crystallinity of cellulose (e.g. oxidative approaches). In parallel, knowledge of the methods for understanding lignocellulose degradation could be insightful such as advanced microscopy, genomic and post-genomic approaches (e.g. gene expression analysis). The known limitations of biological lignocellulose degradation, such as the necessity for physiochemical pretreatments for biofuel production, can be predictive of potential restrictions of biological plastic degradation. Taking lessons from lignocellulose degradation for plastic degradation is also important for biosafety as engineered plastic-degrading fungi could also have increased plant biomass degrading capabilities. Even though plastics are significantly different from lignocellulose because they lack hydrolysable C-C or C-O bonds and therefore have higher recalcitrance, there are apparent similarities, e.g. both types of compounds are mixtures of hydrophobic polymers with amorphous and crystalline regions, and both require hydrolases and oxidoreductases for their degradation. Thus, many lessons could be learned from fungal lignocellulose degradation.

Cai & Druzhinina, 2021 In honor of John Bissett: authoritative guidelines on molecular identification of Trichoderma, Fungal Diversity

Cai & Druzhinina 2021 DNA Barcoding of fungi and labor

Cai, F., Druzhinina, I.S. In honor of John Bissett: authoritative guidelines on molecular identification of Trichoderma. Fungal Diversity 107, 1–69 (2021). https://doi.org/10.1007/s13225-020-00464-4

Modern taxonomy has developed towards the establishment of global authoritative lists of species that assume the standardized principles of species recognition, at least in a given taxonomic group. However, in fungi, species delimitation is frequently subjective because it depends on the choice of a species concept and the criteria selected by a taxonomist. Contrary to it, identification of fungal species is expected to be accurate and precise because it should predict the properties that are required for applications or that are relevant in pathology. The industrial and plant-beneficial fungi from the genus Trichoderma (Hypocreales) offer a suitable model to address this collision between species delimitation and species identification. A few decades ago, Trichoderma diversity was limited to a few dozen species. The introduction of molecular evolutionary methods resulted in the exponential expansion of Trichoderma taxonomy, with up to 50 new species recognized per year. Here, we have reviewed the genus-wide taxonomy of Trichoderma and compiled a complete inventory of all Trichoderma species and DNA barcoding material deposited in public databases (the inventory is available at the website of the International Subcommission on Taxonomy of Trichoderma www.trichoderma.info). Among the 375 species with valid names as of July 2020, 361 (96%) have been cultivated in vitro and DNA barcoded. Thus, we have developed a protocol for molecular identification of Trichoderma that requires analysis of the three DNA barcodes (ITS, tef1, and rpb2), and it is supported by online tools that are available on www.trichokey.info. We then used all the whole-genome sequenced (WGS) Trichoderma strains that are available in public databases to provide versatile practical examples of molecular identification, reveal shortcomings, and discuss possible ambiguities. Based on the Trichoderma example, this study shows why the identification of a fungal species is an intricate and laborious task that requires a background in mycology, molecular biological skills, training in molecular evolutionary analysis, and knowledge of taxonomic literature. We provide an in-depth discussion of species concepts that are applied in Trichoderma taxonomy, and conclude that these fungi are particularly suitable for the implementation of a polyphasic approach that was first introduced in Trichoderma taxonomy by John Bissett (1948–2020), whose work inspired the current study. We also propose a regulatory and unifying role of international commissions on the taxonomy of particular fungal groups. An important outcome of this work is the demonstration of an urgent need for cooperation between Trichoderma researchers to get prepared to the efficient use of the upcoming wave of Trichoderma genomic data.

Peer-reviewed articles of Irina S. Druzhinina

A complete list of publications may also be found at https://www.researchgate.net/profile/Irina_Druzhinina/contributions

Cai, F., Zhao, Z., Gao R., Ding, M., Jiang, S., Gao, Q., Chenthamara, K., Grujic, M., Bayram-Akcapinar, G., Shen, Q., and Druzhinina, I. S. Intracellular hydrophobin vesicles modulate the architecture and longevity of fungal colonies. (preprint) doi: 10.1101/2020.08.18.255406

Cai F, Druzhinina IS (2020) In honor of John Bissett: Authoritative guidelines on molecular identification of Trichoderma. Fungal Diversity. (in press) doi: 10.1007/s13225-020-00464-4

Cai F, Gao R, Zhao Z, Ding M, Jiang S, Yagtu C, Zhu H, Zhang J, Ebner T, Mayrhofer-Reinhartshuber M, Kainz P, Chenthamara K, Akcapinar GB, Shen Q, Druzhinina IS (2020) Evolutionary compromises in fungal fitness: hydrophobins can hinder the adverse dispersal of conidiospores and challenge their survival. The ISME Journal 14 (10):2610-2624. doi:10.1038/s41396-020-0709-0

Ding MY, Chen W, Ma XC, Lv BW, Jiang SQ, Yu YN, Rahimi MJ, Gao RW, Zhao Z, Cai F, Druzhinina IS (2020) Emerging salt marshes as a source of Trichoderma arenarium sp. nov. and other fungal bio effectors for bio saline agriculture. Journal of Applied Microbiology :jam.14751. doi:10.1111/jam.14751

Gao R, Ding M, Jiang S, Zhao Z, Chenthamara K, Shen Q, Cai F, Druzhinina IS (2020) The Evolutionary and Functional Paradox of Cerato-platanins in Fungi. Appl Environ Microb 86 (13):e00696-00620, /aem/00686/00613/AEM.00696-00620.atom. doi:10.1128/AEM.00696-20

Hoenigsberger M, Pretzer C, Rahimi MJ, Kopchinskiy AG, Parich A, Laciny A, Metscher B, Chan CM, Lim LBL, Salim KA, Zettel H, Druzhinina IS, Schuhmacher R (2020) Strong antimicrobial and low insecticidal activity of mandibular gland reservoir content in Bornean “exploding ants” Colobopsis explodens Laciny & Zettel, 2018 (Hymenoptera: Formicidae). doi:10.25849/ MYRMECOL.NEWS_030:201

Lücking R, Aime MC, Robbertse B, Miller AN, Ariyawansa HA, Aoki T, Cardinali G, Crous PW, Druzhinina IS, Geiser DM, Hawksworth DL, Hyde KD, Irinyi L, Jeewon R, Johnston PR, Kirk PM, Malosso E, May TW, Meyer W, Öpik M, Robert V, Stadler M, Thines M, Vu D, Yurkov AM, Zhang N, Schoch CL (2020) Unambiguous identification of fungi: where do we stand and how accurate and precise is fungal DNA barcoding? IMA Fungus 11 (1):14. doi:10.1186/s43008-020-00033-z

Pérez-Llano Y, Rodríguez-Pupo EC, Druzhinina IS, Chenthamara K, Cai F, Gunde-Cimerman N, Zalar P, Gostinčar C, Kostanjšek R, Folch-Mallol JL, Batista-García RA, Sánchez-Carbente MdR (2020) Stress Reshapes the Physiological Response of Halophile Fungi to Salinity. Cells 9 (3):525. doi:10.3390/cells9030525

Wijayawardene N, Hyde KD, Dai DQ, Tang LZ, Aptroot A, CastanedaRuiz RF, Druzhinina IS, Cai F, Ekanayaka AH, Erdogdu M (2020) A dynamic portal for a community-driven, continuously updated classification of Fungi and fungus-like organisms: outlineoffungi.org. Mycosphere 11 (1):1514-1526. doi:10.5943/mycosphere/11/1/11

Grujić M, Dojnov B, Potočnik I, Atanasova L, Duduk B, Srebotnik E, Druzhinina IS, Kubicek CP, Vujčić Z (2019) Superior cellulolytic activity of Trichoderma guizhouense on raw wheat straw. World Journal of Microbiology and Biotechnology 35 (12):194. doi:10.1007/s11274-019-2774-y

Hatvani L, Homa M, Chenthamara K, Cai F, Kocsubé S, Atanasova L, Mlinaric-Missoni E, Manikandan P, Revathi R, Dóczi I, Bogáts G, Narendran V, Büchner R, Vágvölgyi C, Druzhinina IS, Kredics L (2019) Agricultural systems as potential sources of emerging human mycoses caused by Trichoderma: a successful, common phylotype of Trichoderma longibrachiatum in the frontline. FEMS Microbiology Letters 366 (21):fnz246. doi:10.1093/femsle/fnz246

Hoenigsberger M, Kopchinskiy A, Bueschl C, Parich A, Laciny A, Zettel H, Salim K, Lim L, Druzhinina I, Schuhmacher R (2019) Volatiles from the Mandibular Gland Reservoir Content of Colobopsis explodens Laciny and Zettel, 2018, Worker Ants (Hymenoptera: Formicidae). Molecules 24 (19):3468. doi:10.3390/molecules24193468

Kubicek CP, Steindorff AS, Chenthamara K, Manganiello G, Henrissat B, Zhang J, Cai F, Kopchinskiy AG, Kubicek EM, Kuo A, Baroncelli R, Sarrocco S, Noronha EF, Vannacci G, Shen Q, Grigoriev IV, Druzhinina IS (2019) Evolution and comparative genomics of the most common Trichoderma species. BMC Genomics 20 (1):485. doi:10.1186/s12864-019-5680-7

Laciny A, Nemeschkal HL, Zettel H, Metscher B, Druzhinina IS (2019) Caste-specific morphological modularity in the ant tribe Camponotini (Hymenoptera, Formicidae). BMC Zoology 4 (1):9. doi:10.1186/s40850-019-0048-7

Marik T, Tyagi C, Balázs D, Urbán P, Szepesi Á, Bakacsy L, Endre G, Rakk D, Szekeres A, Andersson MA, Salonen H, Druzhinina IS, Vágvölgyi C, Kredics L (2019) Structural Diversity and Bioactivities of Peptaibol Compounds From the Longibrachiatum Clade of the Filamentous Fungal Genus Trichoderma. Front Microbiol 10:1434. doi:10.3389/fmicb.2019.01434

Zhang J, Miao Y, Rahimi MJ, Zhu H, Steindorff A, Schiessler S, Cai F, Pang G, Chenthamara K, Xu Y, Kubicek CP, Shen Q, Druzhinina IS (2019) Guttation capsules containing hydrogen peroxide: an evolutionarily conserved NADPH oxidase gains a role in wars between related fungi. Environmental Microbiology 21 (8):2644-2658. doi:10.1111/1462-2920.14575

Chadha S, Mehetre ST, Bansal R, Kuo A, Aerts A, Grigoriev IV, Druzhinina IS, Mukherjee PK (2018) Genome-wide analysis of cytochrome P450s of Trichoderma spp.: annotation and evolutionary relationships. Fungal Biology and Biotechnology 5 (1):12. doi:10.1186/s40694-018-0056-3

Druzhinina IS, Chenthamara K, Zhang J, Atanasova L, Yang D, Miao Y, Rahimi MJ, Grujic M, Cai F, Pourmehdi S, Salim KA, Pretzer C, Kopchinskiy AG, Henrissat B, Kuo A, Hundley H, Wang M, Aerts A, Salamov A, Lipzen A, LaButti K, Barry K, Grigoriev IV, Shen Q, Kubicek CP (2018) Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts. PLOS Genetics 14 (4):e1007322. doi:10.1371/journal.pgen.1007322

du Plessis IL, Druzhinina IS, Atanasova L, Yarden O, Jacobs K (2018) The diversity of Trichoderma species from soil in South Africa, with five new additions. Mycologia 110 (3):559-583. doi:10.1080/00275514.2018.1463059

Hoenigsberger M, Kopchinskiy AG, Parich A, Hiller K, Laciny A, Zettel H, Lim LBL, Salim KA, Druzhinina IS, Schuhmacher R (2018) Isolation of Mandibular Gland Reservoir Contents from Bornean ‘Exploding Ants’ (Formicidae) for Volatilome Analysis by GC-MS and Metabolite Detector. JoVE (138):57652. doi:10.3791/57652

Kamravamanesh D, Kovacs T, Pflügl S, Druzhinina I, Kroll P, Lackner M, Herwig C (2018) Increased poly-β-hydroxybutyrate production from carbon dioxide in randomly mutated cells of cyanobacterial strain Synechocystis sp. PCC 6714: Mutant generation and characterization. Bioresource Technology 266:34-44. doi:10.1016/j.biortech.2018.06.057

Laciny A, Zettel H, Kopchinskiy A, Pretzer C, Pal A, Abu Salim K, Javad Rahimi M, Hoenigsberger M, Lim L, Jaitrong W, Druzhinina IS (2018) Colobopsis explodens sp. n., model species for studies on “exploding ants” (Hymenoptera, Formicidae), with biological notes and first illustrations of males of the Colobopsis cylindrica group. Zookeys 751:1-40. doi:10.3897/zookeys.751.22661

Zettel H, Laciny A, Weeyawat J, Syaukani S, Kopchinskiy A, Druzhinina IS (2018) Evidence of predation in two species of the Colobopsis cylindrica group (Hymenoptera: Formicidae: Camponotini). Asian Myrmecology 10: e010011 (1-11) doi:10.20362/AM.010011

Druzhinina IS, Kubicek CP (2017) Genetic engineering of Trichoderma reesei cellulases and their production. Microb Biotechnol 10 (6):1485-1499. doi:10.1111/1751-7915.12726

Gaskell J, Kersten P, Larrondo LF, Canessa P, Martinez D, Hibbett D, Schmoll M, Kubicek CP, Martinez AT, Yadav J, Master E, Magnuson JK, Yaver D, Berka R, Lail K, Chen C, LaButti K, Nolan M, Lipzen A, Aerts A, Riley R, Barry K, Henrissat B, Blanchette R, Grigoriev IV, Cullen D (2017) Draft genome sequence of a monokaryotic model brown-rot fungus Postia (Rhodonia) placenta SB12. Genomics Data 14:21-23. doi:10.1016/j.gdata.2017.08.003

Laciny A, Zettel H, Metscher B, Kamariah AS, Kopchinskiy A, Druzhinina IS (2017) Morphological variation and mermithism in female castes of Colobopsis sp. nrSA, a Bornean “exploding ant” of the Colobopsis cylindrica group (Hymenoptera: Formicidae). Myrmecological News 24:91-106

Marik T, Urbán P, Tyagi C, Szekeres A, Leitgeb B, Vágvölgyi M, Manczinger L, Druzhinina IS, Vágvölgyi C, Kredics L (2017) Diversity Profile and Dynamics of Peptaibols Produced by Green Mould Trichoderma Species in Interactions with Their Hosts Agaricus bisporus and Pleurotus ostreatus. Chem Biodiversity 14 (6):e1700033. doi:10.1002/cbdv.201700033

Miao Y, Li P, Li G, Liu D, Druzhinina IS, Kubicek CP, Shen Q, Zhang R (2017) Two degradation strategies for overcoming the recalcitrance of natural lignocellulosic xylan by polysaccharides-binding GH10 and GH11 xylanases of filamentous fungi: Lignocellulosic xylan degradation strategies. Environmental Microbiology 19 (3):1054-1064. doi:10.1111/1462-2920.13614

Pretzer C, Druzhinina IS, Amaro C, Benediktsdóttir E, Hedenström I, Hervio‐Heath D, Huhulescu S, Schets FM, Farnleitner AH, Kirschner AKT (2017) High genetic diversity of Vibrio cholerae in the European lake Neusiedler See is associated with intensive recombination in the reed habitat and the long‐distance transfer of strains. Environmental Microbiology 19 (1):328-344. doi:10.1111/1462-2920.13612

Przylucka A, Akcapinar GB, Bonazza K, Mello-de-Sousa TM, Mach-Aigner AR, Lobanov V, Grothe H, Kubicek CP, Reimhult E, Druzhinina IS (2017) Comparative physiochemical analysis of hydrophobins produced in Escherichia coli and Pichia pastoris. Colloids and Surfaces B: Biointerfaces 159:913-923. doi:10.1016/j.colsurfb.2017.08.058

Przylucka A, Akcapinar GB, Chenthamara K, Cai F, Grujic M, Karpenko J, Livoi M, Shen Q, Kubicek CP, Druzhinina IS (2017) HFB7 – A novel orphan hydrophobin of the Harzianum and Virens clades of Trichoderma, is involved in response to biotic and abiotic stresses. Fungal Genetics and Biology 102:63-76. doi:10.1016/j.fgb.2017.01.002

Qin Y, Pan X, Kubicek C, Druzhinina I, Chenthamara K, Labbé J, Yuan Z (2017) Diverse Plant-Associated Pleosporalean Fungi from Saline Areas: Ecological Tolerance and Nitrogen-Status Dependent Effects on Plant Growth. Front Microbiol 8. doi:10.3389/fmicb.2017.00158

Davidson DW, Kopchinskiy A, Salim KA, Grujic M, Lim L, Mei CC, Jones TH, Casamatta D, Atanasova L, Druzhinina IS (2016) Nutrition of Borneo’s ‘exploding’ ants (Hymenoptera: Formicidae: Colobopsis ): a preliminary assessment. Biotropica 48 (4):518-527. doi:10.1111/btp.12323

de Man TJB, Stajich JE, Kubicek CP, Teiling C, Chenthamara K, Atanasova L, Druzhinina IS, Levenkova N, Birnbaum SSL, Barribeau SM, Bozick BA, Suen G, Currie CR, Gerardo NM (2016) Small genome of the fungus Escovopsis weberi, a specialized disease agent of ant agriculture. Proceedings of the National Academy of Sciences 113 (13):3567-3572. doi:10.1073/pnas.1518501113

Druzhinina IS, Kopchinskiy AG, Kubicek EM, Kubicek CP (2016) A complete annotation of the chromosomes of the cellulase producer Trichoderma reesei provides insights in gene clusters, their expression and reveals genes required for fitness. Biotechnology for Biofuels 9 (1):75. doi:10.1186/s13068-016-0488-z

Druzhinina IS, Kubicek CP (2016) Familiar Stranger. Ecological Genomics of the Model Saprotroph and Industrial Enzyme Producer Trichoderma reesei Breaks the Stereotypes In: Advances in Applied Microbiology, Adv Appl Microbiol. 2016;95:69-147.doi: 10.1016/bs.aambs.2016.02.001.

Druzhinina IS, Kubicek EM, Kubicek CP (2016) Several steps of lateral gene transfer followed by events of ‘birth-and-death’ evolution shaped a fungal sorbicillinoid biosynthetic gene cluster. BMC Evolutionary Biology 16 (1):269. doi:10.1186/s12862-016-0834-6

Laciny A, Zettel H, Druzhinina I (2016) Workers, soldiers, and gynes – morphometric characterization and description of the female castes of Camponotus singularis (Smith, 1858) (Hymenoptera, Formicidae). DEZ 63 (2):183-193. doi:10.3897/dez.63.9435

Qin Y, Druzhinina IS, Pan X, Yuan Z (2016) Microbially Mediated Plant Salt Tolerance and Microbiome-based Solutions for Saline Agriculture. Biotechnology Advances 34 (7):1245-1259. doi:10.1016/j.biotechadv.2016.08.005

Yuan Z, Druzhinina IS, Labbé J, Redman R, Qin Y, Rodriguez R, Zhang C, Tuskan GA, Lin F (2016) Specialized Microbiome of a Halophyte and its Role in Helping Non-Host Plants to Withstand Salinity. Scientific Reports: 2016 Aug 30;6:32467. doi: 10.1038/srep32467.

Zhang N, Yang D, Kendall JRA, Borriss R, Druzhinina IS, Kubicek CP, Shen Q, Zhang R (2016) Comparative Genomic Analysis of Bacillus amyloliquefaciens and Bacillus subtilis Reveals Evolutional Traits for Adaptation to Plant-Associated Habitats. Front Microbiol 7. doi:10.3389/fmicb.2016.02039

Bonazza K, Gaderer R, Neudl S, Przylucka A, Allmaier G, Druzhinina IS, Grothe H, Friedbacher G, Seidl-Seiboth V (2015) The fungal cerato-platanin protein EPL1 forms highly ordered layers at hydrophobic/hydrophilic interfaces. Soft Matter 11 (9):1723-1732. doi:10.1039/C4SM02389G

Ribitsch D, Herrero Acero E, Przylucka A, Zitzenbacher S, Marold A, Gamerith C, Tscheließnig R, Jungbauer A, Rennhofer H, Lichtenegger H, Amenitsch H, Bonazza K, Kubicek CP, Druzhinina IS, Guebitz GM (2015) Enhanced Cutinase-Catalyzed Hydrolysis of Polyethylene Terephthalate by Covalent Fusion to Hydrophobins. Appl Environ Microb 81 (11):3586-3592. doi:10.1128/AEM.04111-14

Yang D, Pomraning K, Kopchinskiy A, Karimi Aghcheh R, Atanasova L, Chenthamara K, Baker SE, Zhang R, Shen Q, Freitag M, Kubicek CP, Druzhinina IS (2015) Genome Sequence and Annotation of Trichoderma parareesei, the Ancestor of the Cellulase Producer Trichoderma reesei. Genome Announcements 3 (4):e00885-00815. doi:10.1128/genomeA.00885-15

Zhang J, Akcapinar GB, Atanasova L, Rahimi MJ, Przylucka A, Yang D, Kubicek CP, Zhang R, Shen Q, Druzhinina IS (2015) The neutral metallopeptidase NMP1 of Trichoderma guizhouense is required for mycotrophy and selfdefence. Environmental Microbiology: https://doi.org/10.1111/1462-2920.12966

Hori C, Ishida T, Igarashi K, Samejima M, Suzuki H, Master E, Ferreira P, Ruiz-Dueñas FJ, Held B, Canessa P, Larrondo LF, Schmoll M, Druzhinina IS, Kubicek CP, Gaskell JA, Kersten P, St. John F, Glasner J, Sabat G, Splinter BonDurant S, Syed K, Yadav J, Mgbeahuruike AC, Kovalchuk A, Asiegbu FO, Lackner G, Hoffmeister D, Rencoret J, Gutiérrez A, Sun H, Lindquist E, Barry K, Riley R, Grigoriev IV, Henrissat B, Kües U, Berka RM, Martínez AT, Covert SF, Blanchette RA, Cullen D (2014) Analysis of the Phlebiopsis gigantea Genome, Transcriptome and Secretome Provides Insight into Its Pioneer Colonization Strategies of Wood. PLoS Genetics 10 (12):e1004759. doi:10.1371/journal.pgen.1004759

Karimi Aghcheh R, Németh Z, Atanasova L, Fekete E, Paholcsek M, Sándor E, Aquino B, Druzhinina IS, Karaffa L, Kubicek CP (2014) The VELVET A Orthologue VEL1 of Trichoderma reesei Regulates Fungal Development and Is Essential for Cellulase Gene Expression. PLoS ONE 9 (11):e112799. doi:10.1371/journal.pone.0112799

Pfliegler WP, Atanasova L, Karanyicz E, Sipiczki M, Bond U, Druzhinina IS, Sterflinger K, Lopandic K (2014) Generation of New Genotypic and Phenotypic Features in Artificial and Natural Yeast Hybrids.12

Agneheh RK, Druzhinina IS, Kubicek CP (2013) The Putative Protein Methyltransferase LAE1 of Trichoderma atroviride Is a Key Regulator of Asexual Development and Mycoparasitism. PLoS ONE 8 (6):e67144. doi:10.1371/journal.pone.0067144

Atanasova L, Crom SL, Gruber S, Coulpier F, Seidl-Seiboth V, Kubicek CP, Druzhinina IS (2013) Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism. BMC Genomics 14 (1):121. doi:10.1186/1471-2164-14-121

Atanasova L, Knox BP, Kubicek CP, Druzhinina IS, Baker SE (2013) The Polyketide Synthase Gene pks4 of Trichoderma reesei Provides Pigmentation and Stress Resistance. Eukaryotic Cell 12 (11):1499-1508. doi:10.1128/EC.00103-13

Erper I, Turkkan M, Atanasova L, Druzhinina IS, Karaca GH, CebI-KilIcoglu M (2013) Integrated assessment of the mycoparasitic and phytostimulating properties of Trichoderma strains against Rhizoctonia solani. Bulgarian Journal of Agricultural Science 19(4):737-743

Espino-Rammer L, Ribitsch D, Przylucka A, Marold A, Greimel KJ, Herrero Acero E, Guebitz GM, Kubicek CP, Druzhinina IS (2013) Two Novel Class II Hydrophobins from Trichoderma spp. Stimulate Enzymatic Hydrolysis of Poly(Ethylene Terephthalate) when Expressed as Fusion Proteins. Appl Environ Microb 79 (14):4230-4238. doi:10.1128/AEM.01132-13

Karaffa L, Coulier L, Fekete E, Overkamp KM, Druzhinina IS, Mikus M, Seiboth B, Novák L, Punt PJ, Kubicek CP (2013) The intracellular galactoglycome in Trichoderma reesei during growth on lactose. Applied Microbiology and Biotechnology 97 (12):5447-5456. doi:10.1007/s00253-012-4667-y

Lehner SM, Atanasova L, Neumann NKN, Krska R, Lemmens M, Druzhinina IS, Schuhmacher R (2013) Isotope-Assisted Screening for Iron-Containing Metabolites Reveals a High Degree of Diversity among Known and Unknown Siderophores Produced by Trichoderma spp. Appl Environ Microb 79 (1):18-31. doi:10.1128/AEM.02339-12

López-Quintero CA, Atanasova L, Franco-Molano AE, Gams W, Komon-Zelazowska M, Theelen B, Müller WH, Boekhout T, Druzhinina I (2013) DNA barcoding survey of Trichoderma diversity in soil and litter of the Colombian lowland Amazonian rainforest reveals Trichoderma strigosellum sp. nov. and other species. Antonie van Leeuwenhoek 104 (5):657-674. doi:10.1007/s10482-013-9975-4

Mulaw T, Druzhinina I, Kubicek C, Atanasova L (2013) Novel Endophytic Trichoderma spp. Isolated from Healthy Coffea arabica Roots are Capable of Controlling Coffee Tracheomycosis. Diversity 5 (4):750-766. doi:10.3390/d5040750

Pummer BG, Atanasova L, Bauer H, Bernardi J, Druzhinina IS, Fröhlich-Nowoisky J, Grothe H (2013) Spores of many common airborne fungi reveal no ice nucleation activity in oil immersion freezing experiments. Biogeosciences 10 (12):8083-8091. doi:10.5194/bg-10-8083-2013

Degenkolb T, Karimi Aghcheh R, Dieckmann R, Neuhof T, Baker SE, Druzhinina IS, Kubicek CP, Brückner H, von Döhren H (2012) The Production of Multiple Small Peptaibol Families by Single 14-Module Peptide Synthetases in Trichoderma/Hypocrea. Chem Biodiversity 9 (3):499-535. doi:10.1002/cbdv.201100212

Druzhinina IS, Komoń-Zelazowska M, Ismaiel A, Jaklitsch W, Mullaw T, Samuels GJ, Kubicek CP (2012) Molecular phylogeny and species delimitation in the section Longibrachiatum of Trichoderma. Fungal Genetics and Biology 49 (5):358-368. doi:10.1016/j.fgb.2012.02.004

Druzhinina IS, Shelest E, Kubicek CP (2012) Novel traits of Trichoderma predicted through the analysis of its secretome. FEMS Microbiology Letters 337 (1):1-9. doi:10.1111/j.1574-6968.2012.02665.x

Friedl MA, Druzhinina IS (2012) Taxon-specific metagenomics of Trichoderma reveals a narrow community of opportunistic species that regulate each other’s development. Microbiology 158 (1):69-83. doi:10.1099/mic.0.052555-0

Mukherjee PK, Buensanteai N, Moran-Diez ME, Druzhinina IS, Kenerley CM (2012) Functional analysis of non-ribosomal peptide synthetases (NRPSs) in Trichoderma virens reveals a polyketide synthase (PKS)/NRPS hybrid enzyme involved in the induced systemic resistance response in maize. Microbiology 158 (1):155-165. doi:10.1099/mic.0.052159-0

Samuels GJ, Ismaiel A, Mulaw TB, Szakacs G, Druzhinina IS, Kubicek CP, Jaklitsch WM (2012) The Longibrachiatum Clade of Trichoderma: a revision with new species. Fungal Diversity 55 (1):77-108. doi:10.1007/s13225-012-0152-2

Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP (2011) Trichoderma: the genomics of opportunistic success. Nature Reviews Microbiology 9 (10):749-759. doi:10.1038/nrmicro2637

Gal-Hemed I, Atanasova L, Komon-Zelazowska M, Druzhinina IS, Viterbo A, Yarden O (2011) Marine Isolates of Trichoderma spp. as Potential Halotolerant Agents of Biological Control for Arid-Zone Agriculture. Appl Environ Microb 77 (15):5100-5109. doi:10.1128/AEM.00541-11

Kubicek CP, Herrera-Estrella A, Seidl-Seiboth V, Martinez DA, Druzhinina IS, Thon M, Zeilinger S, Casas-Flores S, Horwitz BA, Mukherjee PK, Mukherjee M, Kredics L, Alcaraz LD, Aerts A, Antal Z, Atanasova L, Cervantes-Badillo MG, Challacombe J, Chertkov O, McCluskey K, Coulpier F, Deshpande N, von Döhren H, Ebbole DJ, Esquivel-Naranjo EU, Fekete E, Flipphi M, Glaser F, Gómez-Rodríguez EY, Gruber S, Han C, Henrissat B, Hermosa R, Hernández-Oñate M, Karaffa L, Kosti I, Le Crom S, Lindquist E, Lucas S, Lübeck M, Lübeck PS, Margeot A, Metz B, Misra M, Nevalainen H, Omann M, Packer N, Perrone G, Uresti-Rivera EE, Salamov A, Schmoll M, Seiboth B, Shapiro H, Sukno S, Tamayo-Ramos JA, Tisch D, Wiest A, Wilkinson HH, Zhang M, Coutinho PM, Kenerley CM, Monte E, Baker SE, Grigoriev IV (2011) Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biology 12 (4):R40. doi:10.1186/gb-2011-12-4-r40

Atanasova L, Druzhinina IS (2010) Global nutrient profiling by Phenotype MicroArrays: a tool complementing genomic and proteomic studies in conidial fungi. J Zhejiang Univ Sci B 11 (3):151-168. doi:10.1631/jzus.B1000007

Atanasova L, Jaklitsch WM, Komoń-Zelazowska M, Kubicek CP, Druzhinina IS (2010) Clonal Species Trichoderma parareesei sp. nov. Likely Resembles the Ancestor of the Cellulase Producer Hypocrea jecorina/T. reesei. Appl Environ Microb 76 (21):7259-7267. doi:10.1128/AEM.01184-10

Druzhinina IS, Komoń-Zelazowska M, Atanasova L, Seidl V, Kubicek CP (2010) Evolution and Ecophysiology of the Industrial Producer Hypocrea jecorina (Anamorph Trichoderma reesei) and a New Sympatric Agamospecies Related to It. PLoS ONE 5 (2):e9191. doi:10.1371/journal.pone.0009191

Druzhinina IS, Kubicek CP, Komon-Zelazowska M, Belayneh Mulaw T, Bissett J (2010) The Trichoderma harzianum demon: complex speciation history resulting in coexistence of hypothetical biological species, recent agamospecies and numerous relict lineages. BMC Evolutionary Biology 10 (1):94. doi:10.1186/1471-2148-10-94

Mulaw TB, C.P. K, Druzhinina IS (2010) The Rhizosphere of Coffea Arabica in Its Native Highland Forests of Ethiopia Provides a Niche for a Distinguished Diversity of Trichoderma. Diversity 2(4)

Paz Z, Komon-Zelazowska M, Druzhinina IS, Aveskamp MM, Shnaiderman A, Aluma Y, Carmeli S, Ilan M, Yarden O (2010) Diversity and potential antifungal properties of fungi associated with a Mediterranean sponge. Fungal Diversity 42 (1):17-26. doi:10.1007/s13225-010-0020-x

Kemptner J, Marchetti-Deschmann M, Mach R, Druzhinina IS, Kubicek CP, Allmaier G (2009) Evaluation of matrix-assisted laser desorption/ionization (MALDI) preparation techniques for surface characterization of intact Fusarium spores by MALDI linear time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 23 (6):877-884. doi:10.1002/rcm.3949

Kredics Ls, Kocsubé Sn, Nagy Ls, Komoń-Zelazowska M, Manczinger Ls, Sajben E, Nagy A, Vágvölgyi C, Kubicek CP, Druzhinina IS, Hatvani Lrn (2009) Molecular identification of Trichoderma species associated with Pleurotus ostreatus and natural substrates of the oyster mushroom. FEMS Microbiology Letters 300 (1):58-67. doi:10.1111/j.1574-6968.2009.01765.x

Le Crom S, Schackwitz W, Pennacchio L, Magnuson JK, Culley DE, Collett JR, Martin J, Druzhinina IS, Mathis H, Monot F, Seiboth B, Cherry B, Rey M, Berka R, Kubicek CP, Baker SE, Margeot A (2009) Tracking the roots of cellulase hyperproduction by the fungus Trichoderma reesei using massively parallel DNA sequencing. Proceedings of the National Academy of Sciences 106 (38):16151-16156. doi:10.1073/pnas.0905848106

Migheli Q, Balmas V, Komoñ-Zelazowska M, Scherm B, Fiori S, Kopchinskiy AG, Kubicek CP, Druzhinina IS (2009) Soils of a Mediterranean hot spot of biodiversity and endemism (Sardinia, Tyrrhenian Islands) are inhabited by pan-European, invasive species of Hypocrea/Trichoderma. Environmental Microbiology 11 (1):35-46. doi:10.1111/j.1462-2920.2008.01736.x

Mikus M, Hatvani Lrn, Neuhof T, Komoń-Zelazowska M, Dieckmann R, Schwecke T, Druzhinina IS, von D�hren H, Kubicek CP (2009) Differential Regulation and Posttranslational Processing of the Class II Hydrophobin Genes from the Biocontrol Fungus Hypocrea atroviridis. Appl Environ Microb 75 (10):3222-3229. doi:10.1128/AEM.01764-08

Zachow C, Berg C, Müller H, Meincke R, Komon-Zelazowska M, Druzhinina IS, Kubicek CP, Berg G (2009) Fungal diversity in the rhizosphere of endemic plant species of Tenerife (Canary Islands): relationship to vegetation zones and environmental factors. The ISME Journal 3 (1):79-92. doi:10.1038/ismej.2008.87

Brunner K, Omann M, Pucher ME, Delic M, Lehner SM, Domnanich P, Kratochwill K, Druzhinina I, Denk D, Zeilinger S (2008) Trichoderma G protein-coupled receptors: functional characterisation of a cAMP receptor-like protein from Trichoderma atroviride. Current Genetics 54 (6):283-299. doi:10.1007/s00294-008-0217-7

Druzhinina IS, Komoń-Zelazowska M, Kredics L, Hatvani L, Antal Z, Belayneh T, Kubicek CP (2008) Alternative reproductive strategies of Hypocrea orientalis and genetically close but clonal Trichoderma longibrachiatum, both capable of causing invasive mycoses of humans. Microbiology 154 (11):3447-3459. doi:10.1099/mic.0.2008/021196-0

Friedl MA, Kubicek CP, Druzhinina IS (2008) Carbon Source Dependence and Photostimulation of Conidiation in Hypocrea atroviridis. Appl Environ Microb 74 (1):245-250. doi:10.1128/AEM.02068-07

Friedl MA, Schmoll M, Kubicek CP, Druzhinina IS (2008) Photostimulation of Hypocrea atroviridis growth occurs due to a cross-talk of carbon metabolism, blue light receptors and response to oxidative stress. Microbiology 154(Pt 4):1229-41

Jaklitsch WM, Kubicek CP, Druzhinina IS (2008) Three European species of Hypocrea with reddish brown stromata and green ascospores. Mycologia 100 (5):796-815. doi:10.3852/08-039

Kubicek CP, Baker SE, Gamauf C, Kenerley CM, Druzhinina IS (2008) Purifying selection and birth-and-death evolution in the class II hydrophobin gene families of the ascomycete Trichoderma/Hypocrea. BMC Evolutionary Biology 8 (1):4. doi:10.1186/1471-2148-8-4

Kubicek CP, Komon-Zelazowska M, Druzhinina IS (2008) Fungal genus Hypocrea/Trichoderma: from barcodes to biodiversity. J Zhejiang Univ Sci B 9 (10):753-763. doi:10.1631/jzus.B0860015

Seidl V, Gamauf C, Druzhinina IS, Seiboth B, Hartl L, Kubicek CP (2008) The Hypocrea jecorina (Trichoderma reesei) hypercellulolytic mutant RUT C30 lacks a 85 kb (29 gene-encoding) region of the wild-type genome. BMC Genomics 9 (1):327. doi:10.1186/1471-2164-9-327

Váczy KZ, Sándor E, Karaffa L, Fekete E, Fekete É, Árnyasi M, Czeglédi L, Kövics GJ, Druzhinina IS, Kubicek CP (2008) Sexual Recombination in the Botrytis cinerea Populations in Hungarian Vineyards. Phytopathology 98 (12):1312-1319. doi:10.1094/PHYTO-98-12-1312

Druzhinina IS, LaFe K, Willinger B, Komoń-Zelazowska M, Ammirati J, Kubicek CP, Rogers JD (2007) An Unknown Hypocreaceae Species Isolated from Human Lung Tissue of a Patient with Non-Fatal Pulmonary Fibrosis. Clinical Microbiology Newsletter 29 (23):180-184. doi:10.1016/j.clinmicnews.2007.11.002

Hatvani L, Antal Z, Manczinger L, Szekeres A, Druzhinina IS, Kubicek CP, Nagy A, Nagy E, Vágvölgyi C, Kredics L (2007) Green Mold Diseases of Agaricus and Pleurotus spp. Are Caused by Related but Phylogenetically Different Trichoderma Species. Phytopathology 97 (4):532-537. doi:10.1094/PHYTO-97-4-0532

Komoń-Zelazowska M, Bissett J, Zafari D, Hatvani L, Manczinger L, Woo S, Lorito M, Kredics L, Kubicek CP, Druzhinina IS (2007) Genetically Closely Related but Phenotypically Divergent Trichoderma Species Cause Green Mold Disease in Oyster Mushroom Farms Worldwide. Appl Environ Microb 73 (22):7415-7426. doi:10.1128/AEM.01059-07

Komon-Zelazowska M, Neuhof T, Dieckmann R, von Döhren H, Herrera-Estrella A, Kubicek CP, Druzhinina IS (2007) Formation of Atroviridin by Hypocrea atroviridis Is Conidiation Associated and Positively Regulated by Blue Light and the G Protein GNA3. Eukaryotic Cell 6 (12):2332-2342. doi:10.1128/EC.00143-07

Kubicek CP, Komoń-Zelazowska M, Sándor E, Druzhinina IS (2007) Facts and Challenges in the Understanding of the Biosynthesis of Peptaibols by Trichoderma. Chem Biodiversity 4 (6):1068-1082. doi:10.1002/cbdv.200790097

Nagy V, Seidl V, Szakacs G, Komoń-Zelazowska M, Kubicek CP, Druzhinina IS (2007) Application of DNA Bar Codes for Screening of Industrially Important Fungi: the Haplotype of Trichoderma harzianum Sensu Stricto Indicates Superior Chitinase Formation. Appl Environ Microb 73 (21):7048-7058. doi:10.1128/AEM.00995-07

Neuhof T, Dieckmann R, Druzhinina IS, Kubicek CP, Nakari-Setälä T, Penttilä M, von Döhren H (2007) Direct identification of hydrophobins and their processing in Trichoderma using intact-cell MALDI-TOF MS: Trichoderma hydrophobins. FEBS Journal 274 (3):841-852. doi:10.1111/j.1742-4658.2007.05636.x

Neuhof T, Dieckmann R, Druzhinina IS, Kubicek CP, von Döhren H (2007) Intact-cell MALDI-TOF mass spectrometry analysis of peptaibol formation by the genus Trichoderma/Hypocrea: can molecular phylogeny of species predict peptaibol structures? Microbiology 153 (10):3417-3437. doi:10.1099/mic.0.2007/006692-0

Schuster A, Kubicek CP, Friedl MA, Druzhinina IS, Schmoll M (2007) Impact of light on Hypocrea jecorina and the multiple cellular roles of ENVOY in this process. BMC Genomics 8 (1):449. doi:10.1186/1471-2164-8-449

Zhang C-l, Liu S-p, Lin F-c, Kubicek CP, Druzhinina IS (2007) Trichoderma taxi sp. nov., an endophytic fungus from Chinese yew Taxus mairei. FEMS Microbiology Letters 270 (1):90-96. doi:10.1111/j.1574-6968.2007.00659.x

Dela Cruz TEE, Schulz BE, Kubicek CP, Druzhinina IS (2006) Carbon source utilization by the marine Dendryphiella species D. arenaria and D. salina. FEMS Microbiology Ecology 58 (3):343-353. doi:10.1111/j.1574-6941.2006.00184.x

Druzhinina IS, Kopchinskiy AG, Kubicek CP (2006) The first 100 Trichoderma species characterized by molecular data. Mycoscience 47 (2):55-64. doi:10.1007/S10267-006-0279-7

Druzhinina IS, Schmoll M, Seiboth B, Kubicek CP (2006) Global Carbon Utilization Profiles of Wild-Type, Mutant, and Transformant Strains of Hypocrea jecorina. Appl Environ Microb 72 (3):2126-2133. doi:10.1128/AEM.72.3.2126-2133.2006

Jaklitsch WM, Komon M, Kubicek CP, Druzhinina IS (2006) Hypocrea crystalligena sp. nov., a common European species with a white-spored Trichoderma anamorph. Mycologia 98(3):499-513

Jaklitsch WM, Komon M, Kubicek CP, Druzhinina IS (2006) Hypocrea voglmayrii sp. nov. from the Austrian Alps represents a new phylogenetic clade in Hypocrea/Trichoderma. Mycologia 97(6):1365-78

Jaklitsch WM, Samuels GJ, Dodd SL, Lu B-S, Druzhinina IS (2006) Hypocrea rufa/Trichoderma viride: a reassessment, and description of five closely related species with and without warted conidia. Studies in Mycology 56:135-177. doi:10.3114/sim.2006.56.04

Samuels GJ, Dodd SL, Lu B-S, Petrini O, Schroers H-J, Druzhinina IS (2006) The Trichoderma koningii aggregate species. Studies in Mycology 56:67-133. doi:10.3114/sim.2006.56.03

Seidl V, Druzhinina IS, Kubicek CP (2006) A screening system for carbon sources enhancing β-N-acetylglucosaminidase formation in Hypocrea atroviridis (Trichoderma atroviride). Microbiology 152 (7):2003-2012. doi:10.1099/mic.0.28897-0

Druzhinina I, Kubicek CP (2005) Species concepts and biodiversity in Trichoderma and Hypocrea: from aggregate species to species clusters? J Zhejiang Univ Sci B (2):100-112. doi:10.1631/jzus.2005.B0100

Druzhinina IS, Kopchinskiy AG, Komoń M, Bissett J, Szakacs G, Kubicek CP (2005) An oligonucleotide barcode for species identification in Trichoderma and Hypocrea. Fungal Genetics and Biology 42 (10):813-828. doi:10.1016/j.fgb.2005.06.007

Kopchinskiy A, Komoń M, Kubicek CP, Druzhinina IS (2005) TrichoBlast: A Multilocus Database for Trichoderma and Hypocrea Identifications. Mycol Res 109 (6):658-660. doi:10.1017/S0953756205233397

Zhang C-l, Druzhinina IS, Kubicek CP, Xu T (2005) Trichoderma biodiversity in China: Evidence for a North to South distribution of species in East Asia. FEMS Microbiology Letters 251 (2):251-257. doi:10.1016/j.femsle.2005.08.034

Druzhinina I, Palma-Oliveira JM (2004) Radioactive contamination of wild mushrooms: a cross-cultural risk perception study. Journal of Environmental Radioactivity 74 (1-3):83-90. doi:10.1016/j.jenvrad.2004.01.025

Druzhinina IS, Chaverri P, Fallah P, Kubicek CP, Samuels GJ (2004) Hypocrea flaviconidia, a new species from Costa Rica with yellow conidia. Studies in Mycology, 50:401–407.

Gherbawy Y, Druzhinina I, Shaban GM, Wuczkowsky M, Yaser M, El-Naghy MA, Prillinger H-J, Kubicek CP (2004) Trichoderma populations from alkaline agricultural soil in the Nile valley, Egypt, consist of only two species. Mycol Prog 3 (3):211-218. doi:10.1007/s11557-006-0091-y

Kraus GF, Druzhinina I, Gams W, Bissett J, Zafari D, Szakacs G, Koptchinski A, Prillinger H, Zare R, Kubicek CP (2004) Trichoderma brevicompactum sp. nov. Mycologia 96 (5):1059-1073. doi:10.1080/15572536.2005.11832905

Lu B, Druzhinina IS, Fallah P, Chaverri P, Gradinger C, Kubicek CP, Samuels GJ (2004) Hypocrea/Trichoderma species with pachybasium-like conidiophores: teleomorphs for T. minutisporum and T. polysporum and their newly discovered relatives. Mycologia 96(2):310-42

Pail M, Peterbauer T, Seiboth B, Hametner C, Druzhinina I, Kubicek CP (2004) The metabolic role and evolution of l-arabinitol 4-dehydrogenase of Hypocrea jecorina. Eur J Biochem 271 (10):1864-1872. doi:10.1111/j.1432-1033.2004.04088.x

Bissett J, Szakacs G, Nolan CA, Druzhinina I, Gradinger C, Kubicek CP (2003) New species of Trichoderma from Asia. Can J Bot 81 (6):570-586. doi:10.1139/b03-051

Kubicek CP, Bissett J, Druzhinina I, Kullnig-Gradinger C, Szakacs G (2003) Genetic and metabolic diversity of Trichoderma: a case study on South-East Asian isolates. Fungal Genetics and Biology 38 (3):310-319. doi:10.1016/S1087-1845(02)00583-2

Wuczkowski M, Druzhinina I, Gherbawy Y, Klug B, Prillinger H, Kubicek CP (2003) Species pattern and genetic diversity of Trichoderma in a mid-European, primeval floodplain-forest. Microbiological Research 158 (2):125-133. doi:10.1078/0944-5013-00193

Druzhinina IS, Insarova ID, Shnyreva AV, D’Yakov YT, Altukhov YP (1997) Homokaryotic mycelial pellets of basidiomycetes: Application to genetic analysis. Russian Journal of Genetics 33 (5):521-526

Pang et al. 2020 Azaphilones biosynthesis complements the defence mechanism of Trichoderma guizhouense against oxidative stress, Environmental Microbiology

Guan et al., 2020 EM

Pang, G., Sun, T., Yu, Z., Yuan, T., Liu, W., Zhu, H., Gao, Q., Yang, D., Kubicek, C.P., Zhang, J., Shen, Q. (2020) Azaphilones biosynthesis complements the defence mechanism of Trichoderma guizhouense against oxidative stress, https://doi.org/10.1111/1462-2920.15246

Filamentous fungi are known as producers of a large array of diverse secondary metabolites (SMs) that aid in securing their environmental niche. Here, we demonstrated that the SMs have an additional role in fungal defense against other fungi: Trichoderma guizhouense, a mycoparasite, is able to antagonize Fusarium oxysporum f. sp. cubense race 4 (Foc4) by forming aerial hyphae that kill the host with hydrogen peroxide. At the same time, a gene cluster comprising two polyketide synthases is strongly expressed. Using functional genetics, we characterized this cluster and identified its products as azaphilones (termed as trigazaphilones). The trigazaphilones were found lacking in antifungal toxicity but exhibited high radical scavenging activities. The antioxidant property of trigazaphilones was in vivo functional under various tested conditions of oxidative stress. Thus, we conclude that the biosynthesis of trigazaphilones serves as a complementary antioxidant mechanism and defends T. guizhouense against the hydrogen peroxide that it produces to combat other fungi like Foc4.

Druzhinina et al. 2018 Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts

Druzhinina et al 2018 PLoS Genetics

Druzhinina IS, Chenthamara K, Zhang J, Atanasova L, Yang D, Miao Y, et al. (2018) Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts. PLoS Genet 14(4): e1007322. https://doi.org/10.1371/journal.pgen.1007322

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.

Zhang et al. 2019. Guttation capsules containing hydrogen peroxide: an evolutionarily conserved NADPH oxidase gains a role in wars between related fungi: The role of hydrogen peroxide in fungal wars. Environmental Microbiology.

Trichoderma - Fusarium interaction

Zhang, J., Miao, Y., Rahimi, M.J., Zhu, H., Steindorff, A., Schiessler, S., Cai, F., Pang, G., Chenthamara, K., Xu, Y., Kubicek, C.P., Shen, Q.*, Druzhinina, I.S.*, 2019. Guttation capsules containing hydrogen peroxide: an evolutionarily conserved NADPH oxidase gains a role in wars between related fungi: The role of hydrogen peroxide in fungal wars. Environmental Microbiology.

When resources are limited, the hypocrealean fungus Trichoderma guizhouense can overgrow another hypocrealean fungus Fusarium oxysporum, cause sporadic cell death and arrest growth. A transcriptomic analysis of this interaction shows that T. guizhouense undergoes a succession of metabolic stresses while F. oxysporum responded relatively neutrally but used the constitutive expression of several toxin-encoding genes as a protective strategy. Because of these toxins, T. guizhouense cannot approach it is potential host on the substrate surface and attacks F. oxysporum from above. The success of T. guizhouense is secured by the excessive production of hydrogen peroxide (H2 O2 ), which is stored in microscopic bag-like guttation droplets hanging on the contacting hyphae. The deletion of NADPH oxidase nox1 and its regulator, nor1 in T. guizhouense led to a substantial decrease in H2 O2 formation with concomitant loss of antagonistic activity. We envision the role of NOX proteins in the antagonism of T. guizhouense as an example of metabolic exaptation evolved in this fungus because the primary function of these ancient proteins was probably not linked to interfungal relationships. In support of this, F. oxysporum showed almost no transcriptional response to T. guizhouense Δnox1 strain indicating the role of NOX/H2 O2 in signalling and fungal communication.

Kubicek et al. 2019. Evolution and comparative genomics of the most common Trichoderma species. BMC Genomics 20.

Kubicek et al 2019 Trichoderma genomics

Kubicek, C.P., Steindorff, A.S., Chenthamara, K., Manganiello, G., Henrissat, B., Zhang, J., Cai, F., Kopchinskiy, A.G., Kubicek, E.M., Kuo, A., Baroncelli, R., Sarrocco, S., Noronha, E.F., Vannacci, G., Shen, Q.*, Grigoriev, I.V., Druzhinina, I.S.*, 2019. Evolution and comparative genomics of the most common Trichoderma specieshttps://pubmed.ncbi.nlm.nih.gov/31189469/. BMC Genomics 20.

Background

The growing importance of the ubiquitous fungal genus Trichoderma (Hypocreales, Ascomycota) requires understanding of its biology and evolution. Many Trichoderma species are used as biofertilizers and biofungicides and T. reesei is the model organism for industrial production of cellulolytic enzymes. In addition, some highly opportunistic species devastate mushroom farms and can become pathogens of humans. A comparative analysis of the first three whole genomes revealed mycoparasitism as the innate feature of Trichoderma. However, the evolution of these traits is not yet understood.

Results

We selected 12 most commonly occurring Trichoderma species and studied the evolution of their genome sequences. Trichoderma evolved in the time of the Cretaceous-Palaeogene extinction event 66 (±15) mya, but the formation of extant sections (Longibrachiatum, Trichoderma) or clades (Harzianum/Virens) happened in Oligocene. The evolution of the Harzianum clade and section Trichoderma was accompanied by significant gene gain, but the ancestor of section Longibrachiatum experienced rapid gene loss. The highest number of genes gained encoded ankyrins, HET domain proteins and transcription factors. We also identified the Trichoderma core genome, completely curated its annotation, investigated several gene families in detail and compared the results to those of other fungi. Eighty percent of those genes for which a function could be predicted were also found in other fungi, but only 67% of those without a predictable function.

Conclusions

Our study presents a time scaled pattern of genome evolution in 12 Trichoderma species from three phylogenetically distant clades/sections and a comprehensive analysis of their genes. The data offer insights in the evolution of a mycoparasite towards a generalist.

Jiang et al. 2019 High-throughput absolute quantification sequencing reveals the effect of different fertilizer applications on bacterial community in a tomato cultivated coastal saline soil. Science of The Total Environment

Jiang S-Q, Yu Y-N, Gao R-W, Wang H, Zhang J, Li R, Long X-H, Shen Q-R, Chen W, Cai F: High-throughput absolute quantification sequencing reveals the effect of different fertilizer applications on bacterial community in a tomato cultivated coastal saline soil. Science of The Total Environment 2019, 687:601-609.

Coastal saline soil is an important reserve land resource that has high potential for agricultural utilization. The present study adopted a high-throughput absolute quantification 16S rRNA sequencing method to investigate the effect of four different fertilization regimes (namely 100% of bio-organic fertilizer, 70% of bio-organic fertilizer +30% of chemical fertilizer, 30% of bio-organic fertilizer +70% of chemical fertilizer, and 100% of chemical fertilizer) on bacterial community assembly in a tomato cultivated saline soil. The results from the field experiment showed that a combination of 70% bio-organic fertilizer plus 30% of chemical fertilizer was the optimal dose to develop tomato cultivation (for improving yield and fruit quality) in this coastal tidal zone. The pot experiment gave the similar results on tomato growth and indicated the application of 70% bio-organic fertilizer plus 30% of chemical fertilizer as the best treatment to active the soil microbiome. The input of nutrients by fertilizers increased the total abundance of bacteria (to >3 fold compared to the initial soil) and simultaneously led to a significant loss of bacterial diversity in soil. The predominant phyla including Proteobacteria, Bacteroidetes and Firmicutes were the main contributors in the microbiome shift especially shown by their remarkable enrichment in the soil that treated by 70% of bio-organic fertilizer and those by the 100% chemical fertilizer. The RDA and Pearson correlation analyses indicated that the soil nutrient availability, especially available P and K, and soil salinity were the key environmental factors that shaped the bacterial community in this ecosystem, though the organic matter content and soil pH also played important roles in microbiome assembly.

Keywords: Absolute quantification 16S-seq; Bio-organic fertilizer; Coastal mud flat; Microbiome; Tomato cultivation.

Ding et al. 2020 Emerging salt marshes as a source of Trichoderma arenerea sp. nov. and other fungal bioeffectors for biosaline agriculture, Journal of Applied Microbiology

Trichoderma arenarium

Ding, M., Chen, W., Gao, R., Jiang, S., Zhao, Z., Cai, F., and Druzhinina, I. S. Emerging salt marshes as a source of Trichoderma arenerea sp. nov. and other fungal bioeffectors for biosaline agriculture, Journal of Applied Microbiology, doi: 10.1111/jam.14751.

Aims: Sustainable agriculture requires effective and safe biofertilizers and biofungicides with low environmental impact. Natural ecosystems that closely resemble the conditions of biosaline agriculture may present a reservoir for fungal strains that can be used as novel bioeffectors.

Methods and results: We isolated a library of fungi from the rhizosphere of three natural halotolerant plants grown in the emerging tidal salt marshes on the southeast coast of China. DNA barcoding of 116 isolates based on the rRNA ITS1 and 2 and other markers (tef1 or rpb2) revealed 38 fungal species, including plant pathogenic (41%), saprotrophic (24%), and mycoparasitic (28%) taxa. The mycoparasitic fungi were mainly species from the hypocrealean genus Trichoderma, including at least four novel phylotypes. Two of them, representing the taxa Trichoderma arenarium sp. nov. (described here) and T. asperelloides, showed effective antagonistic activity against five phytopathogenic fungi, and significant growth promotion on tomato seedlings under the conditions of saline agriculture.

Conclusions: Trichoderma spp. of salt marshes play the role of natural biological control in young soil ecosystems with a putatively premature microbiome.

Significance and impact: The saline soil microbiome is a rich source of halotolerant bioeffectors that can be used in biosaline agriculture.

Keywords: Trichoderma arenarium; Biosaline agriculture; Halotolerant fungi; Plant growth promotion; Rhizosphere; Salt marsh.