Genomic analysis of ant domatia-associated melanized fungi (Chaetothyriales, Ascomycota)

Author(s)
Leandro F. Moreno, Veronika Mayer, Hermann Voglmayr, Rumsais Blatrix, J. B. Stielow, Marcus M. Teixeira, Vania A. Vicente, Sybren de Hoog
Abstract

Several species of melanized (“black yeast-like”) fungi in the order Chaetothyriales live in symbiotic association with ants inhabiting plant cavities (domatia) or with ants that use carton-like material for the construction of nests and tunnels. To investigate the genetic basis and evolution of this lifestyle, genomes of a lineage of four chaetothyrialean strains were sequenced and the genes annotated. While many members of Chaetothyriales have a large ensemble of enzymes enhancing tolerance of extreme or toxic environmental conditions, such as soil polluted with benzene, toluene, ethylbenzene, and xylene (BTEX), members of the domatia symbiont clade experienced significant gene family contractions. This includes enzymes involved in detoxification processes such as cytochrome P450s, transporters, and alcohol dehydrogenases. Overall, the genomes of domatia-associated species are relatively small compared to other Chaetothyriales, with low numbers of protein-coding genes and with a high content of repetitive elements. Biosynthetic clusters involved in the production of secondary metabolites and with potential antimicrobial activities are overrepresented in the genomes of these fungi. We speculate that, despite the reduction of several protein families, members of the domatia-associated clade might tolerate, and perhaps even metabolize, toxic compounds produced from exocrine glands of the ants as defense against microbes. In addition, in this symbiotic association, the plant and the ants could benefit from the production of secondary metabolites by the Chaetothyriales that participate in this tripartite association. We consider a new ecological classification for Chaetothyriales based on genomic features: (i) derived species with high abundance of paralogs colonizing habitats rich in polyaromatic and (ii) potential producers of secondary metabolites with antimicrobial activities, beneficial for symbiotic interactions, occupying specific micro-habitats such as ant domatia.

Organisation(s)
Department of Botany and Biodiversity Research
External organisation(s)
Royal Netherlands Academy of Arts and Sciences, Federal University of Parana, Northern Arizona University, Université Paul-Valéry Montpellier 3, University of Amsterdam (UvA), Radboud University
Journal
Mycological Progress
Volume
18
Pages
541-552
No. of pages
12
ISSN
1861-8952
DOI
https://doi.org/10.1007/s11557-018-01467-x
Publication date
03-2019
Peer reviewed
Yes
Austrian Fields of Science 2012
106008 Botany, 106012 Evolutionary research, 106042 Systematic botany
Keywords
ASJC Scopus subject areas
Ecology, Evolution, Behavior and Systematics, Agricultural and Biological Sciences (miscellaneous)
Portal url
https://ucrisportal.univie.ac.at/en/publications/d10e2efa-1e59-4556-81b9-917b6803198c