Species associations overwhelm abiotic conditions to dictate the structure and function of wood-decay fungal communities.

Environmental conditions exert strong controls on the activity of saprotrophic microbes, yet abiotic factors often fail to adequately predict wood decomposition rates across broad spatial scales. Given that species interactions can have significant positive and negative effects on wood-decay fungal activity, one possibility is that biotic processes serve as the primary controls on community function, with abiotic controls emerging only after species associations are accounted for. Here we explore this hypothesis in a factorial field warming- and nitrogen-addition experiment by examining relationships among wood decomposition rates, fungal activity, and fungal community structure. We show that functional outcomes and community structure are largely unrelated to abiotic conditions, with microsite and plot-level abiotic variables explaining at most 19% of the total variability in decomposition and fungal activity, and 2% of the variability in richness and evenness. In contrast, taxonomic richness, evenness, and species associations (i.e., co-occurrence patterns) exhibited strong relationships with community function, accounting for 52% of the variation in decomposition rates and 73% in fungal activity. A greater proportion of positive vs. negative species associations in a community was linked to strong declines in decomposition rates and richness. Evenness emerged as a key mediator between richness and function, with highly even communities exhibiting a positive richness-function relationship and uneven communities exhibiting a negative or null response. These results suggest that community-assembly processes and species interactions are important controls on the function of wood-decay fungal communities, ultimately overwhelming substantial differences in abiotic conditions.

Fungi exposed to chronic nitrogen enrichment are less able to decay leaf litter.

Saprotrophic fungi are the primary decomposers of plant litter in temperate forests, and their activity is critical for carbon (C) and nitrogen (N) cycling. Simulated atmospheric N deposition is associated with reduced fungal biomass, shifts in fungal community structure, slowed litter decay, and soil C accumulation. Although rarely studied, N deposition may also result in novel selective pressures on fungi, affecting evolutionary trajectories. To directly test if long-term N enrichment reshapes fungal responses to N, we isolated decomposer fungi from a long-term (28 yr) N-addition experiment and used a common garden approach to compare growth rates and decay abilities of isolates from control and N-amended plots. Both growth and decay were significantly altered by long-term exposure to N enrichment. Changes in growth rates were idiosyncratic, as different species grew either more quickly or more slowly after exposure to N, but litter decay by N isolates was consistent and generally lower compared to control isolates of the same species, a response not readily reversed when N isolates were grown in control (low N) environments. Changes in fungal responses accompany and perhaps drive previously observed N-induced shifts in fungal diversity, community composition, and litter decay dynamics.

A high-quality draft genome sequence of Neonectria faginata, causative agent of beech bark disease of Fagus grandifolia.

The draft genome of Neonectria faginata was sequenced with Oxford Nanopore and Illumina 250 bp paired-end sequencing technologies. The assembled genome was 42.9 Mb distributed over 24 contigs, with N50 of 4.4 Mb and 98.6% BUSCO completeness. This genome sequence will aid in understanding N. faginata population structure and ecology.

Characterization of mating type genes in heterothallic Neonectria species, with emphasis on N. coccinea, N. ditissima, and N. faginata.

Neonectria ditissima and N. faginata are canker pathogens involved in an insect-fungus disease complex of American beech (Fagus grandifolia) in North America commonly known as beech bark disease (BBD). In Europe, both N. ditissima and N. coccinea are involved in BBD on European beech (Fagus sylvatica). Field observations across the range of BBD indicate ascospores to be the dominant spore type in the environment. Several studies report a heterothallic (self-sterile) mating strategy for Neonectria fungi, but one study reported homothallism (self-fertility) for N. ditissima. As such, investigations into mating strategy are important for understanding both the disease cycle and population genetics of Neonectria. This is particularly important in the United States given that over time N. faginata dominates the BBD pathosystem despite high densities of nonbeech hosts for N. ditissima. This study utilized whole-genome sequences of BBD-associated Neonectria spp. along with other publicly available Neonectria and Corinectria genomes and in vitro mating assays to characterize mating type (MAT) locus and confirm thallism for select members of Neonectria and Corinectria. MAT gene-specific primer pairs were developed to efficiently characterize the mating types of additional single-ascospore strains of N. ditissima, N. faginata, and N. coccinea and several other related species lacking genomic data. These assays also confirmed the sexual compatibility among N. ditissima strains from different plant hosts. Maximum likelihood phylogenetic analyses of both MAT1-1-1 and MAT1-2-1 sequences recovered trees with similar topology to previously published phylogenies of Neonectria and Corinectria. The results of this study indicate that all Neonectria and Corinectria tested are heterothallic based on our limited sampling and, as such, thallism cannot help explain the inevitable dominance of N. faginata in the BBD pathosystem.

Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria.

The strategy that microbial decomposers take with respect to using substrate for growth versus maintenance is one essential biological determinant of the propensity of carbon to remain in soil. To quantify the environmental sensitivity of this key physiological trade-off, we characterized the carbon use efficiency (CUE) of 23 soil bacterial isolates across seven phyla at three temperatures and with up to four substrates. Temperature altered CUE in both an isolate-specific manner and a substrate-specific manner. We searched for genes correlated with the temperature sensitivity of CUE on glucose and deemed those functional genes which were similarly correlated with CUE on other substrates to be validated as markers of CUE. Ultimately, we did not identify any such robust functional gene markers of CUE or its temperature sensitivity. However, we found a positive correlation between rRNA operon copy number and CUE, opposite what was expected. We also found that inefficient taxa increased their CUE with temperature, while those with high CUE showed a decrease in CUE with temperature. Together, our results indicate that CUE is a flexible parameter within bacterial taxa and that the temperature sensitivity of CUE is better explained by observed physiology than by genomic composition across diverse taxa. We conclude that the bacterial CUE response to temperature and substrate is more variable than previously thought.IMPORTANCE Soil microbes respond to environmental change by altering how they allocate carbon to growth versus respiration-or carbon use efficiency (CUE). Ecosystem and Earth System models, used to project how global soil C stocks will continue to respond to the climate crisis, often assume that microbes respond homogeneously to changes in the environment. In this study, we quantified how CUE varies with changes in temperature and substrate quality in soil bacteria and evaluated why CUE characteristics may differ between bacterial isolates and in response to altered growth conditions. We found that bacterial taxa capable of rapid growth were more efficient than those limited to slow growth and that taxa with high CUE were more likely to become less efficient at higher temperatures than those that were less efficient to begin with. Together, our results support the idea that the CUE temperature response is constrained by both growth rate and CUE and that this partly explains how bacteria acclimate to a warming world.

Drought and plant litter chemistry alter microbial gene expression and metabolite production.

Drought represents a significant stress to microorganisms and is known to reduce microbial activity and organic matter decomposition in Mediterranean ecosystems. However, we lack a detailed understanding of the drought stress response of microbial decomposers. Here we present metatranscriptomic and metabolomic data on the physiological response of in situ microbial communities on plant litter to long-term drought in Californian grass and shrub ecosystems. We hypothesised that drought causes greater microbial allocation to stress tolerance relative to growth pathways. In grass litter, communities from the decade-long ambient and reduced precipitation treatments had distinct taxonomic and functional profiles. The most discernable physiological signatures of drought were production or uptake of compatible solutes to maintain cellular osmotic balance, and synthesis of capsular and extracellular polymeric substances as a mechanism to retain water. The results show a clear functional response to drought in grass litter communities with greater allocation to survival relative to growth that could affect decomposition under drought. In contrast, communities on chemically more diverse and complex shrub litter had smaller physiological differences in response to long-term drought but higher investment in resource acquisition traits across precipitation treatments, suggesting that the functional response to drought is constrained by substrate quality. Our findings suggest, for the first time in a field setting, a trade off between microbial drought stress tolerance, resource acquisition and growth traits in plant litter microbial communities.