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•Forest ecosystems are dynamic on a wide range of temporal scales.•Tree root activity and precipitation induce short-term responses of soil microbes.•Seasonality of tree activity and ...temperature drives the activity of forest microbes.•Succession on litter and deadwood is largely driven by fungal activity.•Forest stand development is a complex process where microbes play an important role.
Microbial activity in forest soils is driven by the dynamics of ecosystem processes, largely dependent on trees as the major primary producers. Diurnal variation of root activity, seasonality of photosynthate production or recalcitrance of decomposing plant biomass all affect microbial abundance, composition of their communities and activity. Due to low N content, fungi appear to be the major decomposers of complex plant biomass: litter and deadwood and to largely shape associated bacterial communities and their activity. On the other hand, bacteria are important in decomposition of fungal mycelia and N-cycle processes including N-fixation. Microbial activity is also affected in the short term by climatic events and in the long-term by ecosystem development after disturbances.
Abstract
The methodical developments in the fields of molecular biology and analytical chemistry significantly increased the level of detail that we achieve when exploring soils and their microbial ...inhabitants. High-resolution description of microbial communities, detection of taxa with minor abundances, screening of gene expression or the detailed characterization of metabolomes are nowadays technically feasible. Despite all of this, our understanding of soil is limited in many ways. The imperfect tools to describe microbial communities and limited possibilities to assign traits to community members make it difficult to link microbes to functions. Also the analysis of processes exemplified by enzyme activity measurements is still imperfect. In the future, it is important to look at soil at a finer detail to obtain a better picture on the properties of individual microbes, their in situ interactions, metabolic rates and activity at a scale relevant to individual microbes. Scaling up is needed as well to get answers at ecosystem or biome levels and to enable global modelling. The recent development of novel tools including metabolomics, identification of genomes in metagenomics sequencing datasets or collection of trait data have the potential to bring soil ecology further. It will, however, always remain a highly demanding scientific discipline.
Despite the significant achievements in soil microbial ecology over the past years, many common methodical approaches have important limitations that need to be addressed as well as our way of thinking about soil as the ecosystem component.
16S ribosomal RNA currently represents the most important target of study in bacterial ecology. Its use for the description of bacterial diversity is, however, limited by the presence of variable ...copy numbers in bacterial genomes and sequence variation within closely related taxa or within a genome. Here we use the information from sequenced bacterial genomes to explore the variability of 16S rRNA sequences and copy numbers at various taxonomic levels and apply it to estimate bacterial genome and DNA abundances. In total, 7,081 16S rRNA sequences were in silico extracted from 1,690 available bacterial genomes (1-15 per genome). While there are several phyla containing low 16S rRNA copy numbers, in certain taxa, e.g., the Firmicutes and Gammaproteobacteria, the variation is large. Genome sizes are more conserved at all tested taxonomic levels than 16S rRNA copy numbers. Only a minority of bacterial genomes harbors identical 16S rRNA gene copies, and sequence diversity increases with increasing copy numbers. While certain taxa harbor dissimilar 16S rRNA genes, others contain sequences common to multiple species. Sequence identity clusters (often termed operational taxonomic units) thus provide an imperfect representation of bacterial taxa of a certain phylogenetic rank. We have demonstrated that the information on 16S rRNA copy numbers and genome sizes of genome-sequenced bacteria may be used as an estimate for the closest related taxon in an environmental dataset to calculate alternative estimates of the relative abundance of individual bacterial taxa in environmental samples. Using an example from forest soil, this procedure would increase the abundance estimates of Acidobacteria and decrease these of Firmicutes. Using the currently available information, alternative estimates of bacterial community composition may be obtained in this way if the variation of 16S rRNA copy numbers among bacteria is considered.
High-throughput DNA sequencing has dramatically transformed several areas of biodiversity research including mycology. Despite limitations, high-throughput sequencing is nowadays a predominant method ...to characterize the alpha and beta diversity of fungal communities. Across the papers utilizing high-throughput sequencing approaches to study natural habitats in terrestrial ecosystems worldwide, > 200 studies published until 2019 have generated over 250 million sequences of the primary mycological metabarcoding marker, the nuclear ribosomal internal transcribed spacer 2 (ITS2). Here we show that at a 97% sequence similarity threshold, the total richness of non-singleton fungal taxa across the studies published so far is 1.08 million, mostly Ascomycota (56.8% of the taxa) and Basidiomycota (36.7% of the taxa). The Chao-1 estimate of the total extant fungal diversity based on this dataset is 6.28 million taxa, representing a conservative estimate of global fungal species richness. Soil and litter represent the habitats with the highest alpha diversity of fungi followed by air, plant shoots, plant roots and deadwood with Chao-1 predictions, for samples containing 5000 sequences, of 1219, 569, 392, 228, 215 and 140 molecular species, respectively. Based on the high-throughput sequencing data, the highest proportion of unknown fungal species is associated with samples of lichen and plant tissues. When considering the use of high-throughput sequencing for the estimation of global fungal diversity, the limitations of the method have to be taken into account, some of which are sequencing platform-specific while others are inherent to the metabarcoding approaches of species representation. In this respect, high-throughput sequencing data can complement fungal diversity predictions based on methods of traditional mycology and increase our understanding of fungal biodiversity.
In forest ecosystems, trees represent the major primary producers and affect the chemical composition and microbial processes in the ecosystem via specific litter chemistry and rhizodeposition. ...Effects of trees on the abundance of soil microorganisms have been previously observed but the extent to which trees affect the composition of microbial communities remains unknown. Here we analyse the factors affecting the composition of bacterial and fungal communities in forest litter and soil under seven tree species studied at twenty-eight spatially independent sites of similar age developed on the same initial substrate. Microbial communities differed between litter and soil. Bacterial communities were more diverse than fungal communities, especially in litter, and exhibited higher evenness. Eighty percent of the bacterial sequences belonged to the 200–250 most dominant operational taxonomic units (OTUs), and 80% of the fungal sequences were composed of only 23–28 OTUs. The effect of tree species on the microbial-community composition was significant in both litter and soil for fungi as well as bacteria. In bacteria, the tree effect was likely partly mediated by litter and soil pH. Fungal taxa showed a greater tendency to be tree-specific: 35–37% of the dominant fungal OTUs but only 0–3% of the bacterial OTUs were restricted to 1 or 2 trees, and 15–45% of the fungi and 80% of the bacteria were common under 6 or 7 trees. Microbial taxa were demonstrated to associate with less trees than would be expected based on the patterns of their abundance in samples and the tree identity thus affects their occurrence. The numbers of observed dominant fungal OTUs in the study area increased faster with an increasing numbers of trees, indicating high β-diversity. Although the proportion of the arbuscular mycorrhizal and ectomycorrhizal fungi differed among trees, the tree-specific fungal taxa were both root-symbiotic and saprotrophic. The effect of trees on the composition of microbial community was demonstrated to be stronger than other soil properties and to explain a large proportion of variation in community composition, especially in fungi.
•Forest trees affect community composition of bacteria and fungi in soil and litter.•More fungi than bacteria are tree-specific, especially in the litter.•Effects of trees on bacteria are likely mediated by litter or soil pH.•Both root-symbiotic and saprotrophic fungi are tree-specific.•Litter and soils under different trees are dominated by different fungi.
The ecology of forest soils is an important field of research due to the role of forests as carbon sinks. Consequently, a significant amount of information has been accumulated concerning their ...ecology, especially for temperate and boreal forests. Although most studies have focused on fungi, forest soil bacteria also play important roles in this environment. In forest soils, bacteria inhabit multiple habitats with specific properties, including bulk soil, rhizosphere, litter, and deadwood habitats, where their communities are shaped by nutrient availability and biotic interactions. Bacteria contribute to a range of essential soil processes involved in the cycling of carbon, nitrogen, and phosphorus. They take part in the decomposition of dead plant biomass and are highly important for the decomposition of dead fungal mycelia. In rhizospheres of forest trees, bacteria interact with plant roots and mycorrhizal fungi as commensalists or mycorrhiza helpers. Bacteria also mediate multiple critical steps in the nitrogen cycle, including N fixation. Bacterial communities in forest soils respond to the effects of global change, such as climate warming, increased levels of carbon dioxide, or anthropogenic nitrogen deposition. This response, however, often reflects the specificities of each studied forest ecosystem, and it is still impossible to fully incorporate bacteria into predictive models. The understanding of bacterial ecology in forest soils has advanced dramatically in recent years, but it is still incomplete. The exact extent of the contribution of bacteria to forest ecosystem processes will be recognized only in the future, when the activities of all soil community members are studied simultaneously.
Fungi are considered the primary decomposers of dead plant biomass in terrestrial ecosystems. However, current knowledge regarding the successive changes in fungal communities during litter ...decomposition is limited. Here we explored the development of the fungal community over 24 months of litter decomposition in a temperate forest with dominant Quercus petraea using 454-pyrosequencing of the fungal internal transcribed spacer (ITS) region and cellobiohydrolase I (cbhI) genes, which encode exocellulases, to specifically address cellulose decomposers. To quantify the involvement of phyllosphere fungi in litter decomposition, the fungal communities in live leaves and leaves immediately before abscission were also analysed. The results showed rapid succession of fungi with dramatic changes in the composition of the fungal community. Furthermore, most of the abundant taxa only temporarily dominated in the substrate. Fungal diversity was lowest at leaf senescence, increased until month 4 and did not significantly change during subsequent decomposition. Highly diverse community of phyllosphere fungi inhabits live oak leaves 2 months before abscission, and these phyllosphere taxa comprise a significant share of the fungal community during early decomposition up to the fourth month. Sequences assigned to the Ascomycota showed highest relative abundances in live leaves and during the early stages of decomposition. In contrast, the relative abundance of sequences assigned to the Basidiomycota phylum, particularly basidiomycetous yeasts, increased with time. Although cellulose was available in the litter during all stages of decomposition, the community of cellulolytic fungi changed substantially over time. The results indicate that litter decomposition is a highly complex process mediated by various fungal taxa.
Community-level physiological profiling (CLPP) analyses from very diverse environments are frequently used with the aim of characterizing the metabolic versatility of whole environmental bacterial ...communities. While the limitations of the methodology for the characterization of whole communities are well known, we propose that CLPP combined with high-throughput sequencing and qPCR can be utilized to identify the copiotrophic, fast-growing fraction of the bacterial community of soil environments, where oligotrophic taxa are usually dominant. In the present work we have used this approach to analyze samples of litter and soil from a coniferous forest in the Czech Republic using BIOLOG GN2 plates. Monosaccharides and amino acids were utilized significantly faster than other C substrates, such as organic acids, in both litter and soil samples. Bacterial biodiversity in CLPP wells was significantly lower than in the original community, independently of the carbon source. Bacterial communities became highly enriched in taxa that typically showed low abundance in the original soil, belonging mostly to the Gammaproteobacteria and the genus Pseudomonas, indicating that the copiotrophic strains, favoured by the high nutrient content, are rare in forest litter and soil. In contrast, taxa abundant in the original samples were rarely found to grow at sufficient rates under the CLPP conditions. Our results show that CLPP is useful to detect copiotrophic bacteria from the soil environments and that bacterial growth is substrate specific.
Forests are essential biomes for global biogeochemical cycles, and belowground microorganisms have a key role in providing relevant ecosystem services. To predict the effects of environmental changes ...on these ecosystem services requires a comprehensive understanding of how biotic and abiotic factors drive the composition of microbial communities in soil. However, microorganisms are not homogeneously distributed in complex environments such as soil, with different features affecting microbes at different extent depending on the niche they occupy. Indeed, this spatial heterogeneity hampers the extrapolation of microbial diversity study results from particular habitats to the ecosystem level, even if the resolution of the more recent studies has increased significantly after the standardization of high-throughput sequencing techniques. The present work intends to give a comprehensive view of the knowledge accumulated until date defining the more important drivers determining the structure of forest soil microbial communities from fine to continental scales.
Fungi are major ecological players in both terrestrial and aquatic environments by cycling organic matter and channelling nutrients across trophic levels. High-throughput sequencing (HTS) studies of ...fungal communities are redrawing the map of the fungal kingdom by hinting at its enormous - and largely uncharted - taxonomic and functional diversity. However, HTS approaches come with a range of pitfalls and potential biases, cautioning against unwary application and interpretation of HTS technologies and results. In this Review, we provide an overview and practical recommendations for aspects of HTS studies ranging from sampling and laboratory practices to data processing and analysis. We also discuss upcoming trends and techniques in the field and summarize recent and noteworthy results from HTS studies targeting fungal communities and guilds. Our Review highlights the need for reproducibility and public data availability in the study of fungal communities. If the associated challenges and conceptual barriers are overcome, HTS offers immense possibilities in mycology and elsewhere.
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