Fungus wars: basidiomycete battles in wood decay

Understanding the mechanisms underlying wood decay basidiomycete community dynamics is crucial for fully understanding decomposition processes, and for modelling ecosystem function and resilience to environmental change. Competition drives community development in decaying woody resources, with interactions occurring at a distance, following physical contact, and through specialised relationships such as mycoparasitism. Outcomes of combative interactions range from replacement, where one mycelium displaces another, to deadlock, where neither combatant captures territory from the other; and a spectrum of intermediate outcomes (i.e. partial or mutual replacement) lie between these extremes. Many wood decay basidiomycetes coexist within a resource, in a complex and dynamic community, and new research techniques are focussing on spatial orientation of interactions in 3 dimensions, as opposed to historical two-dimensional research. Not only do interactions drive changes in species composition and thus wood decomposition rate, they also may have industrial applications in biocontrol of pathogenic or nuisance fungi, enzyme production, and in the production of novel antifungals and antibiotics. Altogether, fungal interactions are a fascinating and important field of study

Interspecific interactions between saprotrophic basidiomycetes: effects on ligninolytic enzyme activity, gene expression and metabolite production

Interspecific antagonism leads to morphological, biochemical and transcriptional changes in the competing mycelia. Several approaches were used to study interactions: enzyme assays, staining, expression of ligninolytic genes, and analysis of volatile organic compounds (VOCs). Laccase and manganese peroxidase (MnP) activities were assayed, and transcript levels of laccase, Mn-repressed peroxidase (MRP), LiP and catalase measured by RT-PCR during interactions between Trametes versicolor and other wood decay fungi on agar plates. Increased laccase activity occurred in all interactions, irrespective of outcome, with expression of a variety of laccase isozymes during growth alone and interactions. The highest laccase and MnP activities were detected in the interaction zone, with minor changes occurring in other regions of interacting mycelia. MnP activity was detected but not expression of MnP genes instead, activity of MRP could explain the observed activity. Whilst no LiP activity was detected in any pairing, low level expression of LiP genes was detected. Any increases in gene expression were probably transient, or missed at the time of sampling. No differences in combative ability or enzyme production were detected between homo- and heterokaryotic isolates of T. versicolor. VOC production was not linked to combative ability, although several constitutive and interaction-specific VOCs were potentially antagonistic. Other VOCs may be involved in the stimulation of laccase activity, or supporting peroxidase activity by the generation of H2O2

Armed and dangerous - chemical warfare in wood decay communities

Fungal community structure and development in decaying woody resources are largely dependent on interspecific antagonistic interactions that determine the distribution of territory – and hence the nutrients within – between different individuals occupying that resource. Interactions are mediated by antagonistic mechanisms, which determine the combative outcome: either deadlock, where neither mycelium loses any territory, or replacement, where one mycelium displaces the other. These mechanisms function aggressively and/or defensively, and include changes in primary metabolism and growth, as well as secondary metabolite production and stress mitigation responses. This chemical warfare may occur as a constitutive defence through modification of the territory occupied by an individual, and the deposition of antimicrobial compounds within. Following detection of a competitor, the metabolite and enzymic profile of a mycelium alters both qualitatively and quantitatively, and different mechanisms may be stimulated when confronted with different competitors. Biotic and abiotic factors, even small alterations, can affect the deployment of these antagonistic mechanisms, altering the general hierarchy of combative ability between species and making it impossible to predict outcomes with certainty. Here we explore recent advances in our understanding of combative interactions between wood decayers, and explain why future research priorities involving the application of emerging biochemical and molecular technologies must focus on interactions in more ecologically realistic and meaningful scenarios

Threesomes destabilise certain relationships: multispecies interactions between wood decay fungi in natural resources

Understanding interspecific interactions is key to explaining and modelling community development and associated ecosystem function. Most interactions research has focused on pairwise combinations, overlooking the complexity of multispecies communities. This study investigated three-way interactions between saprotrophic fungi in wood and across soil, and indicated that pairwise combinations are often inaccurate predictors of the outcomes of multispecies competition in wood block interactions. This inconsistency was especially true of intransitive combinations, resulting in increased species coexistence within the resource. Further, the addition of a third competitor frequently destabilised the otherwise consistent outcomes of pairwise combinations in wood blocks, which occasionally resulted in altered resource decomposition rates, depending on the relative decay abilities of the species involved. Conversely, interaction outcomes in soil microcosms were unaffected by the presence of a third combatant. Multispecies interactions promoted species diversity within natural resources, and made community dynamics less consistent than could be predicted from pairwise interaction studies

Highly competitive fungi manipulate bacterial communities in decomposing beech wood (Fagus sylvativa)

The bacterial communities in decomposing wood are receiving increased attention, but their interactions with wood-decay fungi are poorly understood. This is the first field study to test the hypothesis that fungi are responsible for driving bacterial communities in beech wood (Fagus sylvatica). A meta-genetic approach was used to characterise bacterial and fungal communities in wood that had been laboratory-colonised with known wood-decay fungi, and left for a year at six woodland sites. Alpha-, Beta- and Gammaproteobacteria and Acidobacteria were the proportionally dominant bacterial taxa, as in previous studies. Pre-colonising wood with decay fungi had a clear effect on the bacterial community, apparently via direct fungal influence; the bacterial and fungal communities present at the time of collection explained nearly 60% of their mutual covariance. Site was less important than fungal influence in determining bacterial communities, but the effects of pre-colonisation were more pronounced at some sites than at others. Wood pH was also a strong bacterial predictor, but was itself under considerable fungal influence. Burkholderiaceae and Acidobacteriaceae showed directional responses against the trend of the bacterial community as a whole

Antagonistic fungal interactions influence carbon dioxide evolution from decomposing wood

Fungal species vary in the rate and way in which they decay wood. Thus, understanding fungal community dynamics within dead wood is crucial to understanding decomposition and carbon cycling. Mycelia compete for wood territory, by employing antagonistic mechanisms involving changes in morphology, and production of volatile and diffusible chemicals. This is metabolically costly, and may affect the rate of use of the resource. The metabolic rate during pairwise interactions between wood decay ascomycetes and basidiomycetes was determined by measuring CO2 production. CO2 evolution altered over time, but changes were combination-specific. In only two combinations e when the dominant competitor overgrew the opponent’s territory as mycelia cords e did CO2 evolution increase over the course of the whole interaction. In most interactions, CO2 evolution increased only after complete replacement of one competitor, suggesting utilisation of the predecessor mycelium or differences in decay ability due to alteration of the resource by the predecessor. There was no relationship between rate of CO2 evolution and combative ability nor outcome of interaction

Effects of pre-colonisation and temperature on interspecific fungal interactions in wood

Understanding the effects of changing abiotic conditions on assembly history in wood decay communities is especially important with predicted environmental changes. Interspecific interactions drive community development, so it is important to understand how microclimatic environment affects outcomes of interactions between species from different successional stages in natural substrata. Interactions between eight wood decay fungi were performed in beech (Fagus sylvatica) wood at seven temperatures (12–30 °C), and in soil microcosms and wood that had been pre-colonised for different lengths of time. The hierarchy of combative ability could be altered by changes in temperature: at higher temperatures early secondary colonisers were able to outcompete usually later colonising cord-forming species. Length of pre-colonisation had a species-specific effect on combative ability, probably attributable to biochemical changes rather than the state of decay of the resource. Abiotic variables have clear effects on fungal interactions, underlining the importance of stochastic factors in fungal community succession

Fungal control of early-stage bacterial community development in decomposing wood

The earliest stages of bacterial colonisation of wood have received little attention, particularly with respect to how the colonisation process may be affected by the presence of wood-decay fungi. This study used 16s rRNA gene sequencing to examine the bacterial community in wood that had been incubated in the field for 14 or 84 d, either in wood uncolonised by fungi or pre-colonised by Vuilleminia comedens, Trametes versicolor or Hypholoma fasciculare. All three fungal species significantly delayed bacterial colonisation of the wood. V. comedens and H. fasciculare also reduced bacterial OTU richness and altered bacterial community composition, increasing the relative abundance of Burkholderiales and reducing the proportion of Enterobacteriaceae and Bacteroidetes. Wood that had not been pre-colonised showed seasonal differences between autumn and spring: bacterial richness increased between 14 d and 84 d in the spring, but not in the autumn. Community composition at 84 d in spring was also different to the other time points, with reduced dominance of Gamma-proteobacteria. Archaea were also detected in nearly a third of samples, but with no apparent pattern, and always at low abundances

Priority effects during fungal community establishment in beech wood

Assembly history of fungal communities has a crucial role in the decomposition of woody resources, and hence nutrient cycling and ecosystem function. However, it has not been clearly determined whether the fungal species that arrive first may, potentially, dictate the subsequent pathway of community development, that is, whether there is a priority effect at the species level. We used traditional culture-based techniques coupled with sequencing of amplified genetic markers to profile the fungal communities in beech (Fagus sylvatica) disks that had been pre-colonised separately with nine species from various stages of fungal succession. Clear differences in community composition were evident following pre-colonisation by different species with three distinct successor communities identified, indicating that individual species may have pivotal effects in driving assembly history. Priority effects may be linked to biochemical alteration of the resource and combative ability of the predecessor