No abstract

Systems of classification are important for guiding research activities and providing a common platform for discussion and investigation. One such system is assigning microbial taxa to the roles of mutualists and pathogens. Yet, there are often challenges and even inconsistencies in reports of research findings when microbial taxa display behaviors outside of these two static conditions (e.g. commensal). Over the last two decades, there has been some effort to highlight a continuum of symbiosis, wherein certain microbial taxa may exhibit mutualistic or pathogenic traits depending on environmental contexts, life stages, and plant host associations. However, gaps remain in understanding how to apply the continuum approach to host-microbe pairs across a range of environmental and ecological factors. This commentary presents an alternative framework for evaluating the continuum of symbiosis using dominant archetypes that define symbiotic ranges. We focus particularly on fungi and bacteria, though we recognize that archaea and other microeukaryotes play important roles in host-microbe interactions that may be described by this approach. This framework is centered in eco-evolutionary theory and aims to enhance communication among researchers, as well as prioritize holistic consideration of the factors shaping microbial life strategies. We discuss the influence of plant-mediated factors, habitat constraints, co-evolutionary forces, and the genetic contributions which shape different microbial lifestyles. Looking to the future, using a continuum of symbiosis paradigm will enable greater flexibility in defining the roles of target microbes and facilitate a more holistic view of the complex and dynamic relationship between microbes and plants.

Black yeasts are polyextremotolerant fungi that contain high amounts of melanin in their cell wall and maintain a primarily yeast form. These fungi grow in xeric, nutrient deplete environments which implies that they require highly flexible metabolisms and the ability to form lichen-like mutualisms with nearby algae and bacteria. However, the exact ecological niche and interactions between these fungi and their surrounding community is not well understood. We have isolated two novel black yeast fungi of the genus Exophiala: JF 03-3F “Goopy” E. viscosium and JF 03-4F “Slimy” E. limosus, which are from dryland biological soil crusts. A combination of whole genome sequencing and various phenotyping experiments have been performed on these isolates to determine their fundamental niches within the biological soil crust consortium. Our results reveal that these Exophiala spp. are capable of utilizing a wide variety of carbon and nitrogen sources potentially from symbiotic microbes, they can withstand many abiotic stresses, and can potentially provide UV resistance to the crust community in the form of secreted melanin. Besides the identification of two novel species within the genus Exophiala, our study also provides new insight into the production and regulation of melanin in extremotolerant fungi.

Black yeasts are polyextremotolerant fungi that contain high amounts of melanin in their cell wall and maintain a primar yeast form. These fungi grow in xeric, nutrient depletes environments which implies that they require highly flexible metabolisms and have been suggested to contain the ability to form lichen-like mutualisms with nearby algae and bacteria. However, the exact ecological niche and interactions between these fungi and their surrounding community are not well understood. We have isolated 2 novel black yeasts from the genus Exophiala that were recovered from dryland biological soil crusts. Despite notable differences in colony and cellular morphology, both fungi appear to be members of the same species, which has been named Exophiala viscosa (i.e. E. viscosa JF 03-3 Goopy and E. viscosa JF 03-4F Slimy). A combination of whole genome sequencing, phenotypic experiments, and melanin regulation experiments have been performed on these isolates to fully characterize these fungi and help decipher their fundamental niche within the biological soil crust consortium. Our results reveal that E. viscosa is capable of utilizing a wide variety of carbon and nitrogen sources potentially derived from symbiotic microbes, can withstand many forms of abiotic stresses, and excretes melanin which can potentially provide ultraviolet resistance to the biological soil crust community. Besides the identification of a novel species within the genus Exophiala, our study also provides new insight into the regulation of melanin production in polyextremotolerant fungi.