Abstract

Wood-degrading fungi vary in their strategies for deconstructing wood, and their competitive successes shape the rate and fate of carbon released from wood, Earth’s largest pool of aboveground terrestrial carbon. In this study, one-on-one interspecific interactions between two model brown rot (carbohydrate-selective) fungi, Gloeophyllum trabeum and Rhodonia (Postia) placenta, were studied on wood wafers where a clearly resolved interaction zone (IZ) could be generated, reproducibly. Comparative RNAseq and proteomics between the IZ and non-interacting hyphae of each species identified combative strategies for each fungus. Glycoside hydrolases were a relatively smaller portion of the interaction secretome compared to non-interacting hyphae. The interaction zone showed higher pectinase specific activity than all other sampling locations, and higher laminarinase specific activity (branched β-glucan proxy) was seen in the IZ secretome relative to equivalent hyphae in single-species cultures. Our efforts also identified two distinct competitive strategies in these two fungi with a shared nutritional mode (brown rot) but polyphyletic ancestral lineages. Gloeophyllum trabeum (Gloeophyllum clade) upregulated more secondary metabolite (SM) synthesis genes in response to a competitor than did R. placenta. R. placenta (Antrodia clade) upregulated a larger variety of uncharacterized oxidoreductases in interacting hyphae, suggesting that these may play a role in mediating competitor response in this fungus. Both species produced several hypothetical proteins exclusively in the interaction zone, leaving questions as to the function of these proteins. This work supports the existence of multiple interaction strategies among brown rot fungi and highlights the functional diversity among wood decay fungi.

Highlights

  • Wood-degrading basidiomycetes live in complex microbial communities, sometimes with thousands of other fungal species in a single piece of degrading wood (Rajala et al, 2012)

  • Rhodonia placenta and Gloeophyllum trabeum are two model brown rot fungi commonly found on softwood lumber and while this interaction may not be likely without human intervention, it is presumed to occur in lumber

  • The single species cultures used here were used in a different orientation than the interaction microcosms, which may have caused some differences in gene expression and protein secretion and must be considered when interpreting the results

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Summary

Introduction

Wood-degrading basidiomycetes live in complex microbial communities, sometimes with thousands of other fungal species in a single piece of degrading wood (Rajala et al, 2012). Elevated GH 18 chitinase expression levels have been shown in secondary colonization of dead fungal hyphae of Heterobasidion irregulare by the white rot basidiomycete Phaneorchaete chrysosporium, a pattern which may appear in response to the hyphae of living fungal competitors (Karlsson et al, 2016) This type of response is likely widespread among wood-degrading saprophytes, as hyphal displacement is a common process in natural successional cycles among decay fungi (O’Leary et al, 2018). Expression levels of other classes of GHs involved in plant cell wall degradation have been shown to remain constant during interspecific interactions, as seen in the white rot fungus Pycnoporus coccineus paired against Coniophora puteana or Botrytis cinerea (Arfi et al, 2013) This pattern, albeit produced from a combination of model species, suggests a diversion of resources away from plant cell wall metabolism and toward fungal cell wall metabolism during interspecific combat

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