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

Leandro F Moreno,Veronika Mayer,Rumsaïs Blatrix,J Benjamin Stielow,Marcus M Teixeira,Vania A Vicente,Sybren De Hoog,Hermann Voglmayr

doi:10.1007/s11557-018-01467-x

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.

Highlights

Black yeast-like fungi in the order Chaetothyriales are known for their preference for toxic (Seyedmousavi et al 2014) or hostile climatic (Selbmann et al 2015) conditions—lifestyles that may have enhanced their ability to cause infection in human hosts (Moreno et al 2018d)
As hundreds of ant species are known to live in symbiosis with plants (Chomicki and Renner 2015), and as the ant species investigated far often live with black yeast-like fungi (Mayer et al 2014), many new ant-plant associated Chaetothyriales remain to be discovered
Genome sequences of four Chaetothyriales colonizing ant domatia were determined by Illumina high-throughput sequencing and de novo assembled

Summary

Introduction

Black yeast-like fungi in the order Chaetothyriales are known for their preference for toxic (Seyedmousavi et al 2014) or hostile climatic (Selbmann et al 2015) conditions—lifestyles that may have enhanced their ability to cause infection in human hosts (Moreno et al 2018d). Some of the black yeast-like fungi living in symbiotic association with ants, seem to occupy restricted ecological niches and might be specialists (Fig. 1) (Voglmayr et al 2011; Vasse et al 2017). Ant-associated Chaetothyriales can be classified in three ecological categories based on the nature of the fungal-ant interaction: (a) living in ant-occupied domatia in plants, (b) colonizing ant-made carton structures, and (c) living as parts of fungus-gardens of leaf-cutter ants (Vasse et al 2017). A recent phylogenetic classification revealed that many of the melanized ant-fungi cluster in a single clade, but some species are scattered across the phylogeny of the Chaetothyriales (Voglmayr et al 2011; Vasse et al 2017). Some of the generalist extremotolerant species, such as a fungus close to (99.4% ITS similarity) the hydrocarbon degrader Exophiala oligosperma, have been found colonizing ant-plant domatia (Vasse et al 2017), suggesting that hydrocarbon degradation may be an essential factor in symbiosis with ants

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