Nejvíce citovaný článek - PubMed ID 33436515
Complementary Roles of Wood-Inhabiting Fungi and Bacteria Facilitate Deadwood Decomposition
BACKGROUND: Fine woody debris (FWD; deadwood < 10 cm diameter) is a crucial but often overlooked component of forest ecosystems. It provides habitat for microbial communities and enhances soil fertility through nutrient cycling. This role is especially important in managed forests, which typically have limited deadwood stocks. Climate change is increasing forest disturbances and expanding early successional forests with low canopy cover, yet the effects on microbial communities and related processes remain poorly understood. RESULTS: In a ten-year canopy manipulation experiment, we examined the decomposition of FWD of Fagus sylvatica and Abies alba. Increased canopy openness significantly decreased bacterial diversity in decomposing FWD and altered the community composition in surrounding soil. Decomposition time was the main factor shaping bacterial community structure in FWD, with tree species and canopy cover also contributing. We identified bacterial groups involved in carbohydrate degradation, fungal biomass breakdown, and nitrogen fixation. Importantly, bacterial communities in fully decomposed FWD remained distinct from soil communities. CONCLUSIONS: Deadwood decomposition and nutrient cycling are driven by complex ecological interactions. Microbial community dynamics are influenced by the interplay of FWD decomposition stage, tree species, and microclimatic conditions. Bacterial communities, although less frequently studied in this context, appear more stable over time than previously studied fungi. This stability may help sustain decomposition processes and nutrient turnover under the environmental variability associated with global change.
- Klíčová slova
- Bacterial community, Canopy cover, Deadwood, Decomposition, Ecology, Fine woody debris, Microclimate, Succession, Temperate forest,
- Publikační typ
- časopisecké články MeSH
BACKGROUND: Deadwood decomposition is an essential ecological process in forest ecosystems, playing a key role in nutrient cycling and carbon sequestration by enriching soils with organic matter. This process is driven by diverse microbial communities encompassing specialized functions in breaking down organic matter, but the specific roles of individual microorganisms in this process are still not fully understood. RESULTS: Here, we characterized the deadwood microbiome in a natural mixed temperate forest in Central Europe using PacBio HiFi long-read sequencing and a genome-resolved transcriptomics approach in order to uncover key microbial contributors to wood decomposition. We obtained high quality assemblies, which allowed attribution of complex microbial functions such as nitrogen fixation to individual microbial taxa and enabled the recovery of metagenome-assembled genomes (MAGs) from both abundant and rare deadwood bacteria. We successfully assembled 69 MAGs (including 14 high-quality and 7 single-contig genomes) from 4 samples, representing most of the abundant bacterial phyla in deadwood. The MAGs exhibited a rich diversity of carbohydrate-active enzymes (CAZymes), with Myxococcota encoding the highest number of CAZymes and the full complement of enzymes required for cellulose decomposition. For the first time we observed active nitrogen fixation by Steroidobacteraceae, as well as hemicellulose degradation and chitin recycling by Patescibacteria. Furthermore, PacBio HiFi sequencing identified over 1000 biosynthetic gene clusters, highlighting a vast potential for secondary metabolite production in deadwood, particularly in Pseudomonadota and Myxococcota. CONCLUSIONS: PacBio HiFi long-read sequencing offers comprehensive insights into deadwood decomposition processes by advancing the identification of functional features involving multiple genes. It represents a robust tool for unraveling novel microbial genomes in complex ecosystems and allows the identification of key microorganisms contributing to deadwood decomposition.
- Klíčová slova
- Biosynthetic gene cluster, Carbohydrate-active enzyme, Deadwood microbiome, Metagenome-assembled genome, Metagenomics, Microbial decomposition, Nitrogen fixation,
- Publikační typ
- časopisecké články MeSH
Fomes fomentarius is a widespread, wood-rotting fungus of temperate, broadleaved forests. Although the fruiting bodies of F. fomentarius persist for multiple years, little is known about its associated microbiome or how these recalcitrant structures are ultimately decomposed. Here we used metagenomics and metatranscriptomics to analyse the microbial community associated with healthy living and decomposing F. fomentarius fruiting bodies to assess the functional potential of the fruiting body-associated microbiome and to determine the main players involved in fruiting body decomposition. F. fomentarius sequences in the metagenomes were replaced by bacterial sequences as the fruiting body decomposed. Most CAZymes expressed in decomposing fruiting bodies targeted components of the fungal cell wall with almost all chitin-targeting sequences, plus a high proportion of beta-glucan-targeting sequences, belonging to Arthropoda. We suggest that decomposing fruiting bodies of F. fomentarius represent a habitat rich in bacteria, while its decomposition is primarily driven by Arthropoda. Decomposing fruiting bodies thus represent a specific habitat supporting both microorganisms and microfauna.
- Klíčová slova
- Fomes fomentarius, deadwood fungi, fruiting body, microbial communities, mycelium decomposition, temperate forest,
- MeSH
- Ascomycota * MeSH
- Bacteria genetika MeSH
- členovci * MeSH
- Coriolaceae * MeSH
- mikrobiota * genetika MeSH
- plodnice hub MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Forests influence climate and mitigate global change through the storage of carbon in soils. In turn, these complex ecosystems face important challenges, including increases in carbon dioxide, warming, drought and fire, pest outbreaks and nitrogen deposition. The response of forests to these changes is largely mediated by microorganisms, especially fungi and bacteria. The effects of global change differ among boreal, temperate and tropical forests. The future of forests depends mostly on the performance and balance of fungal symbiotic guilds, saprotrophic fungi and bacteria, and fungal plant pathogens. Drought severely weakens forest resilience, as it triggers adverse processes such as pathogen outbreaks and fires that impact the microbial and forest performance for carbon storage and nutrient turnover. Nitrogen deposition also substantially affects forest microbial processes, with a pronounced effect in the temperate zone. Considering plant-microorganism interactions would help predict the future of forests and identify management strategies to increase ecosystem stability and alleviate climate change effects. In this Review, we describe the impact of global change on the forest ecosystem and its microbiome across different climatic zones. We propose potential approaches to control the adverse effects of global change on forest stability, and present future research directions to understand the changes ahead.
Deadwood decomposition and other environmental processes mediated by microbial communities are generally studied with composite sampling strategies, where deadwood is collected from multiple locations in a large volume, that produce an average microbial community. In this study, we used amplicon sequencing to compare fungal and bacterial communities sampled with either traditional, composite samples, or small, 1 cm3 cylinders from a discrete location within decomposing European beech (Fagus sylvatica L.) tree trunks. We found that bacterial richness and evenness is lower in small samples when compared to composite samples. There was no significant difference in fungal alpha diversity between different sampling scales, suggesting that visually defined fungal domains are not restricted to a single species. Additionally, we found that composite sampling may obscure variation in community composition and this affects the understanding of microbial associations that are detected. For future experiments in environmental microbiology, we recommend that scale is explicitly considered as a factor and properly selected to correspond with the questions asked. Studies of microbial functions or associations may require samples to be collected at a finer scale than is currently practised.
- Klíčová slova
- bacteria, deadwood, ecology, fungi, microbial communities, temperate forest, wood decay,
- MeSH
- Bacteria genetika MeSH
- buk (rod) * mikrobiologie MeSH
- houby genetika MeSH
- mikrobiota * MeSH
- mykobiom * MeSH
- stromy mikrobiologie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Wood decomposition is a central process contributing to global carbon and nutrient cycling. Quantifying the role of the major biotic agents of wood decomposition, i.e. insects and fungi, is thus important for a better understanding of this process. Methods to quantify wood decomposition, such as dry mass loss, suffer from several shortcomings, such as destructive sampling or subsampling. We developed and tested a new approach based on computed tomography (CT) scanning and semi-automatic image analysis of logs from a field experiment with manipulated beetle communities. We quantified the volume of beetle tunnels in wood and bark and the relative wood volume showing signs of fungal decay and compared both measures to classic approaches. The volume of beetle tunnels was correlated with dry mass loss and clearly reflected the differences between beetle functional groups. Fungal decay was identified with high accuracy and strongly correlated with ergosterol content. Our data show that this is a powerful approach to quantify wood decomposition by insects and fungi. In contrast to other methods, it is non-destructive, covers entire deadwood objects and provides spatially explicit information opening a wide range of research options. For the development of general models, we urge researchers to publish training data.
- MeSH
- brouci * MeSH
- dřevo * mikrobiologie MeSH
- ergosterol MeSH
- houby MeSH
- počítačová rentgenová tomografie MeSH
- strojové učení MeSH
- uhlík MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- ergosterol MeSH
- uhlík MeSH
Dead wood represents an important pool of carbon and nitrogen in forest ecosystems. This source of soil organic matter has diverse ecosystem functions that include, among others, carbon and nitrogen cycling. However, information is limited on how deadwood properties such as chemical composition, decomposer abundance, community composition, and age correlate and affect decomposition rate. Here, we targeted coarse dead wood of beech, spruce, and fir, namely snags and tree trunks (logs) in an old-growth temperate forest in central Europe; measured their decomposition rate as CO2 production in situ; and analyzed their relationships with other measured variables. Respiration rate of dead wood showed strong positive correlation with acid phosphatase activity and negative correlation with lignin content. Fungal biomass (ergosterol content) and moisture content were additional predictors. Our results indicate that dead wood traits, including tree species, age, and position (downed/standing), affected dead wood chemical properties, microbial biomass, moisture condition, and enzyme activity through changes in fungal communities and ultimately influenced the decomposition rate of dead wood.
- Klíčová slova
- chemical properties, extracellular enzymes, fungal biomass, fungal community, respiration, structural equation modeling,
- Publikační typ
- časopisecké články MeSH
Fine woody debris (FWD) represents the majority of the deadwood stock in managed forests and serves as an important biodiversity hotspot and refuge for many organisms, including deadwood fungi. Wood decomposition in forests, representing an important input of nutrients into forest soils, is mainly driven by fungal communities that undergo continuous changes during deadwood decomposition. However, while the assembly processes of fungal communities in long-lasting coarse woody debris have been repeatedly explored, similar information for the more ephemeral habitat of fine deadwood is missing. Here, we followed the fate of FWD of Fagus sylvatica and Abies alba in a Central European forest to describe the assembly and diversity patterns of fungal communities over 6 years. Importantly, the effect of microclimate on deadwood properties and fungal communities was addressed by comparing FWD decomposition in closed forests and under open canopies because the large surface-to-volume ratio of FWD makes it highly sensitive to temperature and moisture fluctuations. Indeed, fungal biomass increases and pH decreases were significantly higher in FWD under closed canopy in the initial stages of decomposition indicating higher fungal activity and hence decay processes. The assembly patterns of the fungal community were strongly affected by both tree species and microclimatic conditions. The communities in the open/closed canopies and in each tree species were different throughout the whole succession with only limited convergence in time in terms of both species and ecological guild composition. Decomposition under the open canopy was characterized by high sample-to-sample variability, showing the diversification of fungal resources. Tree species-specific fungi were detected among the abundant species mostly during the initial decomposition, whereas fungi associated with certain canopy cover treatments were present evenly during decomposition. The species diversity of forest stands and the variability in microclimatic conditions both promote the diversity of fine woody debris fungi in a forest.
- Klíčová slova
- canopy cover, deadwood, decomposition, ecology, fungal community, microclimate, succession, temperate forest,
- Publikační typ
- časopisecké články MeSH
Deadwood represents significant carbon (C) stock in a temperate forests. Its decomposition and C mobilization is accomplished by decomposer microorganisms - fungi and bacteria - who also supply the foodweb of commensalist microbes. Due to the ecosystem-level importance of deadwood habitat as a C and nutrient stock with significant nitrogen fixation, the deadwood microbiome composition and function are critical to understanding the microbial processes related to its decomposition. We present a comprehensive suite of data packages obtained through environmental DNA and RNA sequencing from natural deadwood. Data provide a complex picture of the composition and function of microbiome on decomposing trunks of European beech (Fagus sylvatica L.) in a natural forest. Packages include deadwood metagenomes, metatranscriptomes, sequences of total RNA, bacterial genomes resolved from metagenomic data and the 16S rRNA gene and ITS2 metabarcoding markers to characterize the bacterial and fungal communities. This project will be of use to microbiologists, environmental biologists and biogeochemists interested in the microbial processes associated with the transformation of recalcitrant plant biomass.
- MeSH
- Bacteria klasifikace MeSH
- buk (rod) mikrobiologie MeSH
- dřevo mikrobiologie MeSH
- ekosystém MeSH
- houby klasifikace MeSH
- lesy MeSH
- metagenom * MeSH
- mezerníky ribozomální DNA genetika MeSH
- mikrobiota * MeSH
- RNA ribozomální 16S genetika MeSH
- stromy mikrobiologie MeSH
- taxonomické DNA čárové kódování MeSH
- Publikační typ
- časopisecké články MeSH
- dataset MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Česká republika MeSH
- Názvy látek
- mezerníky ribozomální DNA MeSH
- RNA ribozomální 16S MeSH
Deadwood decomposition is responsible for a significant amount of carbon (C) turnover in natural forests. While fresh deadwood contains mainly plant compounds and is extremely low in nitrogen (N), fungal biomass and N content increase during decomposition. Here, we examined 18 genome-sequenced bacterial strains representing the dominant deadwood taxa to assess their adaptations to C and N utilization in deadwood. Diverse gene sets for the efficient decomposition of plant and fungal cell wall biopolymers were found in Acidobacteria, Bacteroidetes, and Actinobacteria. In contrast to these groups, Alphaproteobacteria and Gammaproteobacteria contained fewer carbohydrate-active enzymes and depended either on low-molecular-mass C sources or on mycophagy. This group, however, showed rich gene complements for N2 fixation and nitrate/nitrite reduction-key assimilatory and dissimilatory steps in the deadwood N cycle. We show that N2 fixers can obtain C independently from either plant biopolymers or fungal biomass. The succession of bacteria on decomposing deadwood reflects their ability to cope with the changing quality of C-containing compounds and increasing N content.
- Klíčová slova
- bacterial genomes, cellulose, deadwood, mycophagy, nitrogen fixation,
- Publikační typ
- časopisecké články MeSH