Ecological generalism drives hyperdiversity of secondary metabolite gene clusters in xylarialean endophytes

Abstract

Although secondary metabolites are typically associated with competitive or pathogenic interactions, the high bioactivity of endophytic fungi in the Xylariales, coupled with their abundance and broad host ranges spanning all lineages of land plants and lichens, suggests that enhanced secondary metabolism might facilitate symbioses with phylogenetically diverse hosts.Here, we examined secondary metabolite gene clusters (SMGCs) across 96 Xylariales genomes in two clades (Xylariaceae s.l. and Hypoxylaceae), including 88 newly sequenced genomes of endophytes and closely related saprotrophs and pathogens. We paired genomic data with extensive metadata on endophyte hosts and substrates, enabling us to examine genomic factors related to the breadth of symbiotic interactions and ecological roles.All genomes contain hyperabundant SMGCs; however, Xylariaceae have increased numbers of gene duplications, horizontal gene transfers (HGTs) and SMGCs. Enhanced metabolic diversity of endophytes is associated with a greater diversity of hosts and increased capacity for lignocellulose decomposition.Our results suggest that, as host and substrate generalists, Xylariaceae endophytes experience greater selection to diversify SMGCs compared with more ecologically specialised Hypoxylaceae species. Overall, our results provide new evidence that SMGCs may facilitate symbiosis with phylogenetically diverse hosts, highlighting the importance of microbial symbioses to drive fungal metabolic diversity.

Lifestyle Transitions in Fusarioid Fungi are Frequent and Lack Clear Genomic Signatures

“…This contrasts with other well-defined lifestyles such as that of mycorrhizal fungi, for which specific genetic features have been associated with lifestyle in both ascomycetes and basidiomycetes ( Martin et al 2010 ; Delaux et al 2013 ; Kohler et al 2015 ; Peter et al 2016 ; Miyauchi et al 2020 ; Rich et al 2021 ). One observed hallmark of the transition to mycorrhizal symbiosis is the loss of genes encoding PCWDEs ( Kohler et al 2015 ; Peter et al 2016 ; Miyauchi et al 2020 ), but, as we found here, these are retained in various endophytic taxa ( Zuccaro et al 2014 ; Lahrmann et al 2015 ; Hacquard et al 2016 ; Franco et al 2022 ; Mesny et al 2021 ). As PCWDEs have often been treated predominantly as features of saprotrophy, this has fed into the hypothesis that many endophytes are latent saprotrophs, but in a broad comparison of CAZymes across the Dikarya, Zhao et al (2013) demonstrated that plant pathogens have on average more CAZymes belonging to typical PCDWE families than saprotrophs.…”

“…Furthermore, treating lifestyles as categorical traits does not accurately reflect the range of outcomes we know can exist within even one lifestyle, such as different pathogenic strains within the same species varying in “aggressiveness” (e.g., Holtz et al 2011 ; Chen et al 2014 ; Šišić et al 2018 ). These both remain central issues with current approaches to fungal lifestyle comparison at large (e.g., Knapp et al 2018 ; Miyauchi et al 2020 ; Mesny et al 2021 ; Franco et al 2022 ). New methods that can effectively incorporate multiple lifestyle hypotheses, or treat lifestyles as points on a continuous spectrum, are sorely needed to encapsulate the nuance of these highly context-dependent interactions.…”

Lifestyles shape genome size and gene content in fungal pathogens

“…The second major predictor of genome size is gene content. Expansion and diversification of genes are usually linked to adaptation to a specific niche, for instance in mycorhizal (Miyauchi et al, 2020) or wood decomposing fungi (Franco et al, 2022). We find that an overall increase in gene repertoire is linked to a pathogenic lifestyle, and this pattern is visible in pathogens from different Sordariomycetes clades, except for vector-transmitted tree pathogens.…”

Traits along the leaf economics spectrum are associated with communities of foliar endophytic symbionts

“…The robust bioactivity of endophytic Xylariales, which included cellulase, chitinase, protease, and antipathogen activity, is consistent with a potentially defensive role in the softer, lower-C leaves with limited structural protection in which they most frequently occur. Recent work has highlighted the remarkable chemical diversity of Xylariales such that the traits observed in this study may be relevant beyond the specific strains studied here ( Franco et al, 2022 ). Notably, some strains of Botryosphaeriales also displayed bioactivity, but in general these traits were less common, consistent with their occurrence in leaves with robust structural defenses.…”