Most cited article - PubMed ID 27125755
Cellulose and hemicellulose decomposition by forest soil bacteria proceeds by the action of structurally variable enzymatic systems
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.
- Keywords
- Bacterial community, Canopy cover, Deadwood, Decomposition, Ecology, Fine woody debris, Microclimate, Succession, Temperate forest,
- Publication type
- Journal Article MeSH
Cellulose degradation is a critical process in soil ecosystems, playing a vital role in nutrient cycling and organic matter decomposition. Enzymatic degradation of cellulosic biomass is the most sustainable and green method of producing liquid biofuel. It has gained intensive research interest with future perspective as the majority of terrestrial lignocellulose biomass has a great potential to be used as a source of bioenergy. However, the recalcitrant nature of lignocellulose limits its use as a source of energy. Noteworthy enough, enzymatic conversion of cellulose biomass could be a leading future technology. Fungal enzymes play a central role in cellulose degradation. Our understanding of fungal cellulases has substantially redirected in the past few years with the discovery of a new class of enzymes and Cellulosome. Efforts have been made from time to time to develop an economically viable method of cellulose degradation. This review provides insights into the current state of knowledge regarding cellulose degradation in soil and identifies areas where further research is needed.
- Keywords
- Biofuel, Cellulases, Cellulose degradation, Lignocellulose,
- Publication type
- Journal Article MeSH
Lignocellulosic materials are composed of three main structural polymers: hemicellulose, cellulose, and lignin. Cellulose is a long chain molecule of glucose requiring a small number of enzymes for degradation due to its simple structure while lignin is a complex polymer of phenylpropane making its biochemical decomposition difficult. Under anaerobic conditions, lignocellulose breakdown is much easier and more rapid than aerobic conditions. Various studies have been carried out to estimate the rate of degradation of lignocellulosic materials. Microorganisms play a key role in the degradation of lignocellulosic materials because they produce a variety of hydrolytic enzymes including cellulase, proteases, xylanases, lipases, laccase, and phosphatases during the degradation of lignocellulosic materials. Based on the body of literature, microorganismal activity can provide useful information about the process of organic matter decomposition.
- Keywords
- Cellulose, Enzyme, Hemicellulose, Lignin, Microorganisms,
- MeSH
- Cell Wall metabolism MeSH
- Cellulase * MeSH
- Cellulose metabolism MeSH
- Phosphoric Monoester Hydrolases MeSH
- Glucose MeSH
- Laccase MeSH
- Lignin * metabolism MeSH
- Polymers MeSH
- Peptide Hydrolases MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
- Names of Substances
- Cellulase * MeSH
- Cellulose MeSH
- Phosphoric Monoester Hydrolases MeSH
- Glucose MeSH
- Laccase MeSH
- Lignin * MeSH
- lignocellulose MeSH Browser
- Polymers MeSH
- Peptide Hydrolases MeSH
Invertebrate-microbial associations are widespread in the biosphere and are often related to the function of novel genes, fitness advantages, and even speciation events. Despite ~ 13,000 species of millipedes identified across the world, millipedes and their gut microbiota are markedly understudied compared to other arthropods. Exploring the contribution of individual host-associated microbes is often challenging as many are uncultivable. In this study, we conducted metatranscriptomic profiling of different body segments of a millipede at the holobiont level. This is the first reported transcriptome assembly of a tropical millipede Telodeinopus aoutii (Demange, 1971), as well as the first study on any Myriapoda holobiont. High-throughput RNA sequencing revealed that Telodeinopus aoutii contained > 90% of the core Arthropoda genes. Proteobacteria, Bacteroidetes, Firmicutes, and Euryarchaeota represented dominant and functionally active phyla in the millipede gut, among which 97% of Bacteroidetes and 98% of Firmicutes were present exclusively in the hindgut. A total of 37,831 predicted protein-coding genes of millipede holobiont belonged to six enzyme classes. Around 35% of these proteins were produced by microbiota in the hindgut and 21% by the host in the midgut. Our results indicated that although major metabolic pathways operate at the holobiont level, the involvement of some host and microbial genes are mutually exclusive and microbes predominantly contribute to essential amino acid biosynthesis, short-chain fatty acid metabolism, and fermentation.
- MeSH
- Bacteroidetes MeSH
- Arthropods * genetics MeSH
- Amino Acids, Essential MeSH
- Fatty Acids, Volatile MeSH
- Gastrointestinal Microbiome * genetics MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Amino Acids, Essential MeSH
- Fatty Acids, Volatile 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.
- Keywords
- bacterial genomes, cellulose, deadwood, mycophagy, nitrogen fixation,
- Publication type
- Journal Article MeSH
Soil microorganisms are important mediators of carbon cycling in nature. Although cellulose- and hemicellulose-degrading bacteria have been isolated from Algerian ecosystems, the information on the composition of soil bacterial communities and thus the potential of their members to decompose plant residues is still limited. The objective of the present study was to describe and compare the bacterial community composition in Algerian soils (crop, forest, garden, and desert) and the activity of cellulose- and hemicellulose-degrading enzymes. Bacterial communities were characterized by high-throughput 16S amplicon sequencing followed by the in silico prediction of their functional potential. The highest lignocellulolytic activity was recorded in forest and garden soils whereas activities in the agricultural and desert soils were typically low. The bacterial phyla Proteobacteria (in particular classes α-proteobacteria, δ-proteobacteria, and γ-proteobacteria), Firmicutes, and Actinobacteria dominated in all soils. Forest and garden soils exhibited higher diversity than agricultural and desert soils. Endocellulase activity was elevated in forest and garden soils. In silico analysis predicted higher share of genes assigned to general metabolism in forest and garden soils compared with agricultural and arid soils, particularly in carbohydrate metabolism. The highest potential of lignocellulose decomposition was predicted for forest soils, which is in agreement with the highest activity of corresponding enzymes.
- Keywords
- Algerian soils, Bacterial community, Cellulases, Decomposition, Hemicellulases, Lignocellulose,
- MeSH
- Bacteria classification enzymology genetics isolation & purification MeSH
- Bacterial Proteins genetics metabolism MeSH
- Cellulase genetics metabolism MeSH
- Ecosystem MeSH
- Phylogeny MeSH
- Glycoside Hydrolases genetics metabolism MeSH
- Forests MeSH
- Soil chemistry MeSH
- Soil Microbiology * MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Algeria MeSH
- Names of Substances
- Bacterial Proteins MeSH
- Cellulase MeSH
- Glycoside Hydrolases MeSH
- hemicellulase MeSH Browser
- Soil MeSH
Due to the ability of soil bacteria to solubilize minerals, fix N2 and mobilize nutrients entrapped in the organic matter, their role in nutrient turnover and plant fitness is of high relevance in forest ecosystems. Although several authors have already studied the organic matter decomposing enzymes produced by soil and plant root-interacting bacteria, most of the works did not account for the activity of cell wall-attached enzymes. Therefore, the enzyme deployment strategy of three bacterial collections (genera Luteibacter, Pseudomonas and Arthrobacter) associated with Quercus spp. roots was investigated by exploring both cell-bound and freely-released hydrolytic enzymes. We also studied the potential of these bacterial collections to produce enzymes involved in the transformation of plant and fungal biomass. Remarkably, the cell-associated enzymes accounted for the vast majority of the total activity detected among Luteibacter strains, suggesting that they could have developed a strategy to maintain the decomposition products in their vicinity, and therefore to reduce the diffusional losses of the products. The spectrum of the enzymes synthesized and the titres of activity were diverse among the three bacterial genera. While cellulolytic and hemicellulolytic enzymes were rather common among Luteibacter and Pseudomonas strains and less detected in Arthrobacter collection, the activity of lipase was widespread among all the tested strains. Our results indicate that a large fraction of the extracellular enzymatic activity is due to cell wall-attached enzymes for some bacteria, and that Quercus spp. root bacteria could contribute at different levels to carbon (C), phosphorus (P) and nitrogen (N) cycles.
- MeSH
- Bacteria cytology enzymology metabolism MeSH
- Cell Wall enzymology MeSH
- Quercus microbiology MeSH
- Endophytes * MeSH
- Hydrolysis MeSH
- Organic Chemicals metabolism MeSH
- Soil chemistry MeSH
- Rhizosphere * MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Organic Chemicals MeSH
- Soil MeSH
The concept of operational taxonomic units (OTUs), which constructs "mathematically" defined taxa, is widely accepted and applied to describe bacterial communities using amplicon sequencing of 16S rRNA gene. OTUs are often used to infer functional traits since they are considered to fairly represent of community members. However, the link between molecular taxa, real taxa, and OTUs seems to be much more complicated. Strains of the same bacterial species (ideally belonging to the same OTU) typically only share some genes (the core genome), while other genes are strain-specific and unique. It is thus unclear to what extent are important functional traits homogeneous within an OTU and how correctly can functional traits be inferred for individual OTU members. Here, we have tested in silico the similarity of all genes and, more specifically, the set of genes encoding for glycoside hydrolases (GH) in bacterial genomes that belong to the same OTU. Genome similarity varied among OTUs, but as many as 5-78% of genes were not shared between the two bacterial genomes in the pair. The complement of GH families (the presence of gene families and the number of genes per family) differed in 95% of OTUs. In average, 43% of GH families either differed in gene counts or were present in one genome and absent in the other. These results show a serious limitation of the OTU-based approaches when used to infer the functional traits of bacterial communities and open the questions how to link environmental sequencing data and microbial functions.
- MeSH
- Bacteria classification genetics MeSH
- Genes, Bacterial genetics MeSH
- Databases, Nucleic Acid MeSH
- DNA, Bacterial genetics MeSH
- Phylogeny MeSH
- Genetic Variation MeSH
- Genome, Bacterial genetics MeSH
- Glycoside Hydrolases genetics MeSH
- Metagenomics * MeSH
- Microbiota MeSH
- RNA, Ribosomal, 16S genetics MeSH
- Sequence Analysis, DNA MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- DNA, Bacterial MeSH
- Glycoside Hydrolases MeSH
- RNA, Ribosomal, 16S MeSH
Forest soils represent important terrestrial carbon (C) pools where C is primarily fixed in the plant-derived biomass but it flows further through the biomass of fungi and bacteria before it is lost from the ecosystem as CO2 or immobilized in recalcitrant organic matter. Microorganisms are the main drivers of C flow in forests and play critical roles in the C balance through the decomposition of dead biomass of different origins. Here, we track the path of C that enters forest soil by following respiration, microbial biomass production, and C accumulation by individual microbial taxa in soil microcosms upon the addition of 13C-labeled biomass of plant, fungal, and bacterial origin. We demonstrate that both fungi and bacteria are involved in the assimilation and mineralization of C from the major complex sources existing in soil. Decomposer fungi are, however, better suited to utilize plant biomass compounds, whereas the ability to utilize fungal and bacterial biomass is more frequent among bacteria. Due to the ability of microorganisms to recycle microbial biomass, we suggest that the decomposer food web in forest soil displays a network structure with loops between and within individual pools. These results question the present paradigms describing food webs as hierarchical structures with unidirectional flow of C and assumptions about the dominance of fungi in the decomposition of complex organic matter.
- MeSH
- Bacteria classification genetics isolation & purification metabolism MeSH
- Biodegradation, Environmental MeSH
- Biomass MeSH
- Ecosystem MeSH
- Fungi classification genetics isolation & purification metabolism MeSH
- Forests MeSH
- Soil chemistry MeSH
- Soil Microbiology * MeSH
- Plants metabolism microbiology MeSH
- Carbon metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Soil MeSH
- Carbon MeSH
BACKGROUND: Evergreen coniferous forests contain high stocks of organic matter. Significant carbon transformations occur in litter and soil of these ecosystems, making them important for the global carbon cycle. Due to seasonal allocation of photosynthates to roots, carbon availability changes seasonally in the topsoil. The aim of this paper was to describe the seasonal differences in C source utilization and the involvement of various members of soil microbiome in this process. RESULTS: Here, we show that microorganisms in topsoil encode a diverse set of carbohydrate-active enzymes, including glycoside hydrolases and auxiliary enzymes. While the transcription of genes encoding enzymes degrading reserve compounds, such as starch or trehalose, was high in soil in winter, summer was characterized by high transcription of ligninolytic and cellulolytic enzymes produced mainly by fungi. Fungi strongly dominated the transcription in litter and an equal contribution of bacteria and fungi was found in soil. The turnover of fungal biomass appeared to be faster in summer than in winter, due to high activity of enzymes targeting its degradation, indicating fast growth in both litter and soil. In each enzyme family, hundreds to thousands of genes were typically transcribed simultaneously. CONCLUSIONS: Seasonal differences in the transcription of glycoside hydrolases and auxiliary enzyme genes are more pronounced in soil than in litter. Our results suggest that mainly fungi are involved in decomposition of recalcitrant biopolymers in summer, while bacteria replace them in this role in winter. Transcripts of genes encoding enzymes targeting plant biomass biopolymers, reserve compounds and fungal cell walls were especially abundant in the coniferous forest topsoil.
- Keywords
- Auxiliary activity enzymes, Bacteria, Carbohydrate-active enzymes, Carbon cycle, Coniferous forests, Decomposition, Fungi, Glycoside hydrolases, Lignocellulose-degradation, Seasonality, Transcriptomics,
- MeSH
- Bacteria genetics metabolism MeSH
- Biomass MeSH
- Bacterial Physiological Phenomena * genetics MeSH
- Fungi genetics MeSH
- Carbon Cycle * MeSH
- Forests * MeSH
- Microbiota genetics MeSH
- Soil Microbiology * MeSH
- Seasons MeSH
- Transcriptome MeSH
- Carbon metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Carbon MeSH