Significance: Wood-decomposing fungi are key players in the carbon cycle and are models for making energy from lignocellulose, sustainably. Our study focuses on brown rot fungi that selectively remove carbohydrates, leaving most lignin behind. These fungi often decompose wood faster than their lignin-degrading white rot ancestors, despite losses in genes involved in plant cell wall hydrolysis. To explain brown rot, many have implicated reactive oxygen species (ROS) in facilitating hydrolysis, with microenvironmental gradients partitioning ROS from enzymes. By spatially colocalizing gene expression and enzyme activities as Postia placenta colonizes wood, we provide evidence of an oxidative-hydrolytic two-step mechanism controlled by differential expression, not microenvironments, and we highlight 549 genes (∼4% of the genome) that are upregulated during this unique pretreatment.

Summary: Priority effects among wood decomposers have been demonstrated by manipulating fungal assembly history via inoculations in dead wood and then tracking community development usingDNAsequencing. 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 withFomes fomentariusorPiptoporus betulinusat high exogenous inoculum potential. Initial fungal richness in birch stems averaged 143OTUs and decreased nearly threefold after five months of decomposition. AlthoughF. fomentariussuccessfully 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.

Fungi dominate the turnover of wood, Earth’s largest pool of aboveground terrestrial carbon. Fungi first evolved this capacity by degrading lignin to access and hydrolyze embedded carbohydrates (white rot). Multiple lineages, however, adapted faster reactive oxygen species (ROS) pretreatments to loosen lignocellulose and selectively extract sugars (brown rot). This brown rot “shortcut” often coincided with losses (>60%) of conventional lignocellulolytic genes, implying that ROS adaptations supplanted conventional pathways. We used comparative transcriptomics to further pursue brown rot adaptations, which illuminated the clear temporal expression shift of ROS genes, as well as the shift toward synthesizing more GHs in brown rot relative to white rot. These imply that gene regulatory shifts, not simply ROS innovations, were key to brown rot fungal evolution. These results not only reveal an important biological shift among these unique fungi, but they may also illuminate a trait that restricts brown rot fungi to certain ecological niches.

Wood-decomposing fungi use distinct strategies to deconstruct wood that can significantly vary carbon release rates and fates. White and brown rot-type fungi attack lignin as a prerequisite to access carbohydrates (white rot) or selectively remove carbohydrates (brown rot). Soft rot fungi use less well-studied mechanisms to deconstruct wood (e.g., cavitation and erosion). These fungi often co-exist in nature, creating a balance in carbon turnover that could presumably “tip” in a changing climate. There is no simple genetic marker, however, to distinguish fungi by rot types, and traditional black and white distinctions (brown and white, in this case) cannot explain a spectrum of “gray” carbon loss possibilities. In this study, we tested 39 wood-degrading fungal strains along this spectrum of rot types. We tracked wood mass loss and chemical changes in aspen blocks in early- to mid-decay stages, including three signatures of fungal nutritional mode measured from wood rather than from fungus: dilute alkali solubility, water-soluble monosaccharides, and lignin loss (%) relative to density loss (%) (L/D). Results were then plotted relative to rot types and correlated with gene counts, combining new data with past results in some cases. Results yielded a novel distinction in soluble monosaccharide patterns for brown rot fungi, and reliable distinctions between white and brown rot fungi, although soft rot fungi were not as clearly distinguished as suggested in past studies. Gene contents (carbohydrate-active enzymes and peroxidases) also clearly distinguished brown and white rot fungi, but did not offer reliable correlation with lignin vs. carbohydrate selectivity. These results support the use of wood residue chemistry to link fungal genes (with known or unknown function) with emergent patterns of decomposition. Wood signatures, particularly L/D, not only confirm the rot type of dominant fungi, but they offer a more nuanced, continuous variable to which we can correlate genomic, transcriptomic, and secretomic evidence rather than limit it to functional categories as distinct “bins.”