Cai et al. 2020 Evolutionary compromises in fungal fitness: hydrophobins hinder the adverse dispersal of spores and challenge their survival, The ISME J

The role of HFB4 in Trichoderma fitness

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., Bayram-Akcapinar, G., Shen, Q., and Druzhinina, I. S. 2020 Evolutionary compromises in fungal fitness: hydrophobins hinder the adverse dispersal of spores and challenge their survival, The ISME J 14, 2610–2624 (2020). https://doi.org/10.1038/s41396-020-0709-0

Fungal evolutionary biology is impeded by the scarcity of fossils, irregular life cycles, immortality, and frequent asexual reproduction. Simple and diminutive bodies of fungi develop inside a substrate and have exceptional metabolic and ecological plasticity, which hinders species delimitation. However, the unique fungal traits can shed light on evolutionary forces that shape the environmental adaptations of these taxa. Higher filamentous fungi that disperse through aerial spores produce amphiphilic and highly surface-active proteins called hydrophobins (HFBs), which coat spores and mediate environmental interactions. We exploited a library of HFB-deficient mutants for two cryptic species of mycoparasitic and saprotrophic fungi from the genus Trichoderma (Hypocreales) and estimated fungal development, reproductive potential, and stress resistance. HFB4 and HFB10 were found to be relevant for Trichoderma fitness because they could impact the spore-mediated dispersal processes and control other fitness traits. An analysis in silico revealed purifying selection for all cases except for HFB4 from T. harzianum, which evolved under strong positive selection pressure. Interestingly, the deletion of the hfb4 gene in T. harzianum considerably increased its fitness-related traits. Conversely, the deletion of hfb4 in T. guizhouense led to the characteristic phenotypes associated with relatively low fitness. The net contribution of the hfb4 gene to fitness was found to result from evolutionary tradeoffs between individual traits. Our analysis of HFB-dependent fitness traits has provided an evolutionary snapshot of the selective pressures and speciation process in closely related fungal species.

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.

Zhao et al. 2021 At least three families of hyphosphere small secreted cysteine-rich proteins can optimize surface properties to a moderately hydrophilic state suitable for fungal attachment

Zhao et al., 2021 Hyphosphere concept

Zhao, Z., Cai, F., Gao, R., Ding, M., Jiang, S., Chen, P., Pang, G., Chenthamara, K., Shen, Q., Bayram Akcapinar, G. and Druzhinina, I.S. (2021), At least three families of hyphosphere small secreted cysteine-rich proteins can optimize surface properties to a moderately hydrophilic state suitable for fungal attachment. Environ Microbiol. https://doi.org/10.1111/1462-2920.15413

The secretomes of filamentous fungi contain a diversity of small secreted cysteine-rich proteins (SSCPs) that have a variety of properties ranging from toxicity to surface activity. Some SSCPs are recognized by other organisms as indicators of fungal presence, but their function in fungi is not fully understood. We detected a new family of fungal surface-active SSCPs (saSSCPs), here named hyphosphere proteins (HFSs). An evolutionary analysis of the HFSs in Pezizomycotina revealed a unique pattern of eight single cysteine residues (C-CXXXC-C-C-C-C-C) and a long evolutionary history of multiple gene duplications and ancient interfungal lateral gene transfers, suggesting their functional significance for fungi with different lifestyles. Interestingly, recombinantly produced saSSCPs from three families (HFSs, hydrophobins and cerato-platanins) showed convergent surface-modulating activity on glass and on poly(ethylene-terephthalate), transforming their surfaces to a moderately hydrophilic state, which significantly favoured subsequent hyphal attachment. The addition of purified saSSCPs to the tomato rhizosphere had mixed effects on hyphal attachment to roots, while all tested saSSCPs had an adverse effect on plant growth in vitro. We propose that the exceptionally high diversity of saSSCPs in Trichoderma and other fungi evolved to efficiently condition various surfaces in the hyphosphere to a fungal-beneficial state.

Publications of Komal Chenthamara

Peer-reviewed scientific articles

CAI Feng, GAO Renwai, ZHAO Zheng, DING Mingyue, JIANG Siqi, YAGTU Civan, ZHU Hong, ZHANG Jian, EBNER Thomas, MAYRHOFER-REINHARTSHUBER Michael, KAINZ Philipp, CHENTHAMARA Komal, AKCAPINAR Gunseli Bayram, SHEN Qirong, DRUZHININA Irina. Evolutionary compromises in fungal fitness: hydrophobins can hinder the adverse dispersal of conidiospores and challenge their survival. ISME Journal 14(10):1-15, July 2020

GAO Renwai, DING Mingyue, JIANG Siqi, ZHAO Zheng, CHENTHAMARA Komal, SHEN Qirong, CAI Feng, DRUZHININA Irina. The evolutionary and functional paradox of cerato- platanins in the mycoparasitic fungus Trichoderma: high diversity, stabilizing selection, and a minor role in biotic interactions. Applied Environmental Microbiology, April 2020

PÉREZ-LLANO Yordanis, RODRÍGUEZ-PUPO Eya Caridad, DRUZHININA Irina, CHENTHAMARA Komal, CAI Feng, GUNDE-CIMERMAN Nina, ZALAR Polona, GOSTINČAR Cene, KOSTANJŠEK Rok, FOLCH-MALLOL Jorge Luis, BATISTA-GARCÍA Ramón Alberto and SÁNCHEZ-CARBENTE María del Rayo. Stress Reshapes the Physiological Response of Halophile Fungi to Salinity. Cells, February 2020

HATVANI Lóránt, HOMA Mónika, CHENTHAMARA Komal, KOCSUBÉ Sándor, ATANASOVA Lea, MLINARIC-MISSONI Emilija, MANIKANDAN Palanisamy, REVATHI Rajaraman, DÓCZI Ilona, IVÁNYI Béla, BOGÁTS Gábor, NARENDRAN Venkatapathy, BÜCHNER Rita, VÁGVÖLGYI Csaba, DRUZHININA Irina, KREDICS László. Agricultural systems as potential sources of emerging human mycoses caused by Trichoderma. FEMS Microbiology letters, December 2019

KUBICEK Christian§, STEINDORFF Andrei§, CHENTHAMARA Komal, MANGANIELLO Gelsomina, BERNARD Henrissat, ZHANG Jian, CAI Feng, KOPCHINSKIY Alexey, KUBICEK Eva M, KUO Alan, BARONCELLI Riccardo, SARROCCO Sabrina, NORONHA Eliane Ferreira, VANNACCI Giovanni, SHEN Qirong, GRIGORIEV Igor and DRUZHININA Irina. Evolution and comparative genomics of the most common Trichoderma species. BMC Genomics, June 2019

ZHANG Jian, MIAO Youzhi, RAHIMI Mohammad Javad, ZHU Hong, STEINDORFF Andrei, SCHIESSLER Sabine, CAI Feng, PANG Guan, CHENTHAMARA Komal, XU Yu, KUBICEK Christian, SHEN Qirong, and DRUZHININA Irina. Guttation capsules containing hydrogen peroxide: an evolutionarily conserved NADPH oxidase gains a role in wars between related fungi. Environmental Microbiology, February 2019

DRUZHININA Irina, CHENTHAMARA Komal, ZHANG Jian, ATANASOVA Lea, YANG Dongqing, MIAO Youzhi, RAHIMI Mohammad, GRUJIC Marica, CAI Feng, POURMEHDI Shadi, ABU SALIM Kamariah, PRETZER Carina, KOPCHINSKIY Alexey, HENRISSAT Bernard, KUO Alan, HUNDLEY Hope, WANG Mei, AERTS Andrea, SALAMOV Asaf, LIPZEN Anna, LABUTTI Kurt, BARRY Kerrie, GRIGORIEV Igor, SHEN Qirong, and KUBICEK Christian. Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts. PLOS Genetics, April 2018

QIN Yuan, PAN Xueyu, KUBICEK Christian, DRUZHININA Irina, CHENTHAMARA Komal, LABBÉ Jessy and YUAN Zhilin. Diverse Plant-Associated Pleosporalean Fungi from Saline Areas: Ecological Tolerance and Nitrogen-Status Dependent Effects on Plant Growth. Frontiers in Microbiology, February 2017

PRZYLUCKA Agnes, AKCAPINAR Gunseli Bayram, CHENTHAMARA Komal, CAI Feng, GRUJIC Marica, KARPENKO Juriy, LIVOI Miriam, SHEN Qirong, KUBICEK Christian, DRUZHININA Irina. 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, May 2017

DE MAN Tom, STAJICH Jason, KUBICEK Christian, TEILING Clotilde, CHENTHAMARA Komal, ATANASOVA Lea, DRUZHININA Irina, LEVENKOVA Natasha, BIRNBAUM Stephanie, BARRIBEAU Seth, BOZICK Brooke, SUEN Garret, CURRIE Cameron, and GERARDO Nicole. Small genome of the fungus Escovopsis weberi, a specialized disease agent of ant agriculture. PNAS, Proceedings of the National Academy of Sciences, March 2016

YANG Dongqing, POMRANING Kyle, KOPCHINSKIY Alexey, AGHCHEH Razieh Karimi, ATANASOVA Lea, CHENTHAMARA Komal, BAKER Scott E., ZHANG Ruifu, SHEN Qirong, FREITAG Michael, KUBICEK Christian, and DRUZHININA Irina. Genome Sequence and Annotation of Trichoderma parareesei, the Ancestor of the Cellulase Producer Trichoderma reesei. American Society for Microbiology – Genome Announcements August 2015

Book chapters

CHENTHAMARA Komal, DRUZHININA Irina, RAHIMI Mohammad, GRUJIC Marica, and CAI Feng. “Ecological genomics and evolution of Trichoderma reesei”. Springer – Trichoderma reesei ‐ Methods and Protocols, January 2021

RAHIMI Mohammad, CAI Feng, GRUJIC Marica, CHENTHAMARA Komal, and DRUZHININA Irina. Molecular Identification of Trichoderma reesei”. Springer – Trichoderma reesei ‐ Methods and Protocols, January 2021

CHENTHAMARA Komal, DRUZHININA Irina. “Ecological Genomics of Mycotrophic Fungi”. Springer – THE MYCOTA, Environmental and Microbial Relationships, Volume IV, Third Edition, March 2016

List of first author conference papers (Scientific posters)

CHENTHAMARA Komal, STEINDORFF Andrei, GOJIC Vladimir, SHELEST Ekaterina, GRIGORIEV Igor, KUBICEK Christian, DRUZHININA Irina. “The comparative genomics of the most common Trichoderma species reveals the unique pattern of the ankyrin domain-containing proteins in orphomes of individual Trichoderma species”; Poster: Joint Genome Institute User Meeting, Walnut Creek, San Francisco, USA, April 2019

CHENTHAMARA Komal, CAI Feng, VON ROTZ Sebastian, CERVENKA Isabella, SHEN Qirong, DRUZHININA Irina. “The enrichment in hydrophobin-encoding genes constitutes the main genomic hallmark of Trichoderma: the pattern search revealed a plethora of unknown genes absent in other hypocrealean fungi”; Poster: Joint Genome Institute User Meeting, Walnut Creek, San Francisco, USA, April 2019

CHENTHAMARA Komal, GOJIC Vladimir, BAJTELA Robert, DRUZHININA Irina. “Decoding the expanded Ankyrin-Repeat gene family in Trichoderma”; Joint Genome Institute User Meeting, Walnut Creek, San Francisco, USA, March 2018

CHENTHAMARA Komal, CAI Feng, PRZYLUCKA Agnieszka, SHEN Qirong, BAYRAM AKCAPINAR Günseli, DRUZHININA Irina.: “The origin and architecture of Trichoderma hydrophobome”; Poster: Joint Genome Institute User Meeting, Walnut Creek, San Francisco, USA, March 22, 2017, in “Abstract Book”, (2016), S.24

CHENTHAMARA Komal, CAI Feng, PRZYLUCKA Agnieszka, SHEN Qirong, BAYRAM AKCAPINAR Günseli, DRUZHININA Irina. “The origin and architecture of Trichoderma hydrophobome”; Short-talk and poster: Vienna young Scientists Symposium, TU WIEN, June 6, 2017; in “Abstract Book”, (2016), S90-91

DRUZHININA Irina, ATANASOVA Lea, CHENTHAMARA Komal, GRUJIC Marica, HENRISSAT Bernard, ZHANG Jian, SHEN Qirong, GRIGORIEV Igor, KUBICEK Christian. Horizontal gene transfers drove the mycoparasite Trichoderma to adapt to saprotrophy and cellulase production. Talk: 13th European Conference on Fungal Genetics, 3-6, April 2016, Paris, France; in “Abstract Book”, (2016), S.70.

CHENTHAMARA Komal, ATANASOVA Lea, YANG Dongqing, ZHANG Jian, KOPCHINSKIY Alexey, GRIGORIEV Igor, KUBICEK Christian, SHEN Qirong, DRUZHININA Irina. Phylogenomics of Trichoderma. Poster: ECFG12- 12th European conference on fungal genetics, Seville, Spain; 23.3.-27.3. 2014. S: 184

Dipl. Ing. Dr. Tech. Komal Chenthamara

Professional Experience

2020 – currentExternal lab member at FungiG – research group of Irina S. Druzhinina and Feng Cai in China
2019 – 2020In statutory maternal protection and then maternity leave
2015 – 2018Project Assistant (FWF) (PhD student)
 E166-05-2 – Research Group for Microbiology and Applied Genomics, Research Area Biochemical Technology, Institute of Chemical, Environmental and Bioscience Engineering, Technische Universität Wien, Gumpendorfer Str. 1a, 1060 Vienna, Austria

Education

2018Doctoral programme, TU Wien (mit auszeichnung bestanden), Ph.D. Thesis (November 16, 2018): “Using comparative genomics to link phenotypes to genotypes of the mycotrophic fungus Trichoderma
2015Masters in Biotechnology and Bioanalytics, TU Wien, Vienna, Austria. Master Thesis: “Evolution of mycoparasitism in Hypocreales through phylogenomic approach
2011 – 2012B2 level -German, Österreichische Orient Gesellschaft, Vienna, Austria
2006 – 2010Bachelor of Technology (B-Tech) in Biotechnology, SRM University, Chennai, Tamil Nadu, India

Special Trainings

2018Trainee at the Bioinformatics unit (BIU), German Centre for Integrative Biodiversity Research (iDiv), Halle-Jena-Leipzig, Germany
2018Fungal Genomics Workshop, The DOE JGI Genomics of Energy and Environment Meeting, San Francisco, California, USA
2017Fungal Genomics Workshop, The DOE JGI Genomics of Energy and Environment Meeting, Walnut Creek, California, USA
KBase Workshop, The DOE JGI Genomics of Energy and Environment Meeting, Walnut Creek, California, USA
2013Intern in Research Group for Microbiology and Applied Genomics, TU Wien, TU Wien, Vienna, Austria
2013Training in Communication, BEST, Board of European Students of Technology, Vienna, Austria
2013Training in Time Management, BEST, Board of European Students of Technology, Vienna, Austria
2012Intern in Research Group for Bioprocess Technology, TU Wien, Vienna, Austria
2009IELTS (International English Language Testing System), Chennai, Tamil Nadu, India

Prizes and Awards

2017TU Wien Christiana HÖRBIGER Preis – Preis zur Förderung der internationalen Mobilität von Nachwuchswissenschaftler_innen
2016TU Wien Short-term grants for participation in conferences for PhD-students

Skills

Microbiological techniques and microscopy: axenic cultures, microbial diagnostics by DNA barcoding, fungal morphology, microbial cultivations, and phenotype microarrays. Basic molecular biological techniques for fungi and bacteria.

Molecular evolutionary analyses such as multiloci phylogenetics, phylogenomics, lateral gene transfer tests (T-Rex, Notung), natural selection pressure analyses, DNA barcoding, and protein modeling.

Basic skills in genomics (sequence similarity search, manual gene annotation), basic skills in the analyses of NGS data

Descriptive and multivariate exploratory statistical techniques(Statistica, Tableau, UpSet)

Bitmap and vector graphic skills for illustrations (CorelDraw, Affinity Designer)

Experience with citation tools like Zotero and EndNote

Experience with WorkFlow softwares like Geneious, CLC Bio

Experience with GitHub

Experience with Microsoft 365 and Acrobat

Curator of TUCIM (TU Wien Collection of Industrial Microorganisms)- A collection of over 7350 species and their respective DNAs.

Responsible for the introduction of lab techniques to new group members

Responsible for safety-training of all group members

Organized regular group meetings

Member of Journal club, – an initiative of young PostDoc researchers and Ph.D. students. A gathering dedicated to the discussion of the most paradigm-changing scientific discoveries in biotechnology and applied microbiology

Teaching Experience

2016 – 2018Lecturer for the course 166.648 “Biology and genetics of industrial microorganisms”, master Program Technical Chemistry (Biotechnology and Bioanalytics), TU Wien 
2016 – 2018Teaching Assistant for the mandatory course 166.231 “Applied Bioinformatics Lab”, master Program Technical Chemistry Biotechnology and Bioanalytics, TU Wien
2015 – 2018Tutor for mandatory laboratory course 166.222 “Biochemistry and Biotechnology”, bachelor program Technical Chemistry, TU Wien
2014Assistant for the mandatory laboratory course 166.193 “Microbiology”, master Program Technical Chemistry Biotechnology and Bioanalytics, TU Wien

Language Skills

English                                                         Fluent

German                                                       Basic

Hindi and Malayalam                           Mother-tongues

Interests / Hobbies

Reading comics

DIY skin and hair care

Baking

List of Publications

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.