Abstract

Stress-tolerant fungi that can thrive under various environmental extremes are highly desirable for their application to biological control, as an alternative to chemicals for pest management. However, in fungi, the mechanisms of stress tolerance might also have roles in mammal opportunism. We tested five species with high biocontrol potential in agriculture (Aureobasidium pullulans, Debayomyces hansenii, Meyerozyma guilliermondii, Metschnikowia fructicola, Rhodotorula mucilaginosa) and two species recognized as emerging opportunistic human pathogens (Exophiala dermatitidis, Aureobasidium melanogenum) for growth under oligotrophic conditions and at 37 °C, and for tolerance to oxidative stress, formation of biofilms, production of hydrolytic enzymes and siderophores, and use of hydrocarbons as sole carbon source. The results show large overlap between traits desirable for biocontrol and traits linked to opportunism (growth under oligotrophic conditions, production of siderophores, high oxidative stress tolerance, and specific enzyme activities). Based on existing knowledge and these data, we suggest that oligotrophism and thermotolerance together with siderophore production at 37 °C, urease activity, melanization, and biofilm production are the main traits that increase the potential for fungi to cause opportunistic infections in mammals. These traits should be carefully considered when assessing safety of potential biocontrol agents.

Highlights

  • Biocontrol agents employ various and interlinking mechanisms to inhibit or outcompete growth of pathogenic microorganisms such as antibiosis by secretion of numerous compounds; direct parasitism by being armored with various lytic enzymes [1] and by efficient competition for nutrients and space

  • A. pullulans and A. melanogenum are a good example of how closely related species in the same genus can show very different behaviors, considering that these two species were known as varieties of A. pullulans until 2014 [5]

  • A. pullulans is considered to be safe and is used in the biocontrol of plant pathogens, while A. melanogenum is associated with human opportunistic infections

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Summary

Introduction

Biocontrol agents employ various and interlinking mechanisms to inhibit or outcompete growth of pathogenic microorganisms such as antibiosis by secretion of numerous compounds (e.g., siderophores, antibiotics, toxins, etc.); direct parasitism by being armored with various lytic enzymes [1] and by efficient competition for nutrients and space. Genes 2019, 10, 42 as potential biocontrol agents in agriculture (i.e., Aureobasidium pullulans, Debayomyces hansenii, Meyerozyma guilliermondii, Metchnikowia fructicola and Rhodotorula mucilaginosa) and two are well-known opportunistic pathogens (i.e., Exophiala dermatitidis and Aureobasidium melanogenum) Among these species, A. pullulans and A. melanogenum (order, Dothideales; class, Dothideomycetes; subphylum, Pezizomycotina; phylum, Ascomycota) are a good example of how closely related species in the same genus can show very different behaviors, considering that these two species were known as varieties of A. pullulans until 2014 [5]. A. melanogenum on the other hand is recognized as an emerging human opportunist [8] that is responsible for several infections in immunocompromised patients, ranging from cutaneous, ocular, catheter-related, pulmonary and peritonitis infections, to systemic (reviewed in [5]) Both species are polyextremotolerant–able to survive hypersaline

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