Fungal endophytes as priority colonizers initiating wood decomposition

Abstract

Summary Priority effects among wood decomposers have been demonstrated by manipulating fungal assembly history via inoculations in dead wood and then tracking community development using DNA sequencing. Individual wood‐degrading fungi have been shown, however, to initiate decay after having colonized living trees as endophytes. To track these ‘upstream’ colonizers across the endophyte–saprophyte transition, we coupled high‐throughput sequencing with wood physiochemical analyses in stem sections extracted from healthy birch trees (Betula papyrifera; 4–7 cm dia.). We incubated wood in microcosms, limiting communities as endophytes−only or challenging endophytes with Fomes fomentarius or Piptoporus betulinus at high exogenous inoculum potential. Initial fungal richness in birch stems averaged 143 OTUs and decreased nearly threefold after five months of decomposition. Although F. fomentarius successfully colonized some stem sections incubated at 25 °C, decayed wood was generally dominated by saprophytic fungi that were present originally in lower abundances as endophytes. Among saprophytes, fungi in the brown rot functional guild consistently dominated, matching wood residues bearing the chemical hallmarks of brown rot. Despite this functionally redundant outcome, the taxa that rose to dominate in individual sections varied. Surprisingly, the brown rot taxa dominating wood decomposition were better known for lumber degradation rather than log decay in ground contact. Given the isolation from colonizers in our design, this redundancy of brown rot as the outcome suggests that these taxa and more generally brown rot fungi could have adapted to decompose wood where there is lower competitive pressure. Competitive avoidance would complement the diffuse depolymerization mechanisms of brown rot fungi, which are likely more prone to sugar pilfering by other organisms than the processive depolymerization mechanisms of white rot fungi. Overall, this guild‐level predictability of fungal endophyte development and consequence is encouraging given the challenges of predicting wood decomposition, and it provides a base for testing these dynamics under increasing natural complexity.

Independent effects of host and environment on the diversity of wood‐inhabiting fungi

“…It is well known that species of host trees differ considerably in their physicochemical properties and hence in basic habitat conditions for fungi (Cornwell et al., ; Hoppe et al., ; Kahl et al., ). However, recent studies have also shown the importance of endophytic fungi of wood, which are prevalent even in living trees and are able to switch to a saprophytic lifestyle after the death of the tree (Parfitt, Hunt, Dockrell, Rogers, & Boddy, ; Promputtha et al., ; Song et al., ). Activity of this primary colonizer community also potentially influences micro‐habitat conditions of the host tree via modification of woody compounds (e.g.…”

“…Activity of this primary colonizer community also potentially influences micro‐habitat conditions of the host tree via modification of woody compounds (e.g. lignin, cellulose decay with cell wall density loss; Schilling, Kaffenberger, Liew, & Song, ; Song et al., ) and related metabolites plus the possible response (production of secondary metabolites) of the host (Hiscox et al., ). The endophytic community is most likely primarily driven by the identity of the host species, that is, angiosperm vs. gymnosperm, and secondarily by the vitality of the host (Schwarze, Engels, & Mattheck, ), which could also contribute in explaining differences in diversity patterns between hosts (Figure , Table ).…”

“…Hoppe et al., ) or non‐fungal saproxylic organisms (Saint‐Germain, Drapeau, & Buddle, ). Both groups of colonizers can affect the colonization success of species arriving later—the so‐called “priority effect” (Dickie, Fukami, Wilkie, Allen, & Buchanan, ; Fukami et al., ; Hiscox, Clarkson, et al., ; Hiscox, Savoury, et al., ; Song, Kennedy, Liew, & Schilling, ; Song, Vail, Sadowsky, & Schilling, ). With regard to the size of a dead‐wood object, a log provides more resources in space and time for fungi than a branch (Heilmann‐Clausen & Christensen, ; Juutilainen et al., ).…”

Fomitopsis betulina (formerly Piptoporus betulinus): the Iceman’s polypore fungus with modern biotechnological potential

“…As other fungi of this type, it degrades wood to yield brown, cubical cracks easily broken down. Many factors, including microflora or compounds present in wood, contribute to this complex process (Przybył and Żłobińska-Podejma 2000; Song et al 2016; Zarzyński 2009). Shang et al (2013) showed that wood samples decayed by F. betulina lost 57% of dry weight (dw) and 74% of holocellulose after 30 days, whereas the fungus growing on wheat straw causes 65% loss of dw within 98 days of culture (Valášková and Baldrian 2006a).…”

Potential links between wood‐inhabiting and soil fungal communities: Evidence from high‐throughput sequencing

“…Recent studies have demonstrated that diverse taxonomic and ecological functional groups of WIF colonize deadwood (Ottosson et al, ; Purahong et al, ; Song, Kennedy, Liew, & Schilling, ). The functional groups identified include saprotrophs, plant pathogens, endophytes, animal endosymbionts, mycoparasites, mycorrhizae, and lichenized fungi (Ottosson et al, ; Purahong et al, ; Song et al, ). Although several studies have investigated factors related to WIF community assembly (Fukami et al, ; Hoppe et al, ; Rajala et al, ; Song et al, ; van der Wal et al, ), connections between the WIF community and soil fungi, and dispersal mechanisms responsible for their colonization between these compartments, are still unclear.…”