Most cited article - PubMed ID 24551229
Potential of cometabolic transformation of polysaccharides and lignin in lignocellulose by soil Actinobacteria
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 diverse, although they share functions during the decomposition of organic matter. Thus, preferences for soil conditions and litter quality were explored to understand their niche partitioning. A 1-year-long litterbag transplant experiment evaluated how soil physicochemical traits of contrasting sites combined with chemically distinct litters of sedge (S), milkvetch (M) from a grassland, and beech (B) from forest site decomposition. Litter was assessed by mass loss; C, N, and P contents; and low-molecular-weight compounds. Decomposition was described by the succession of fungi, Actinobacteria, Alphaproteobacteria, and Firmicutes; bacterial diversity; and extracellular enzyme activities. The M litter decomposed faster at the nutrient-poor forest site, where the extracellular enzymes were more active, but microbial decomposers were not more abundant. Actinobacteria abundance was affected by site, while Firmicutes and fungi by litter type and Alphaproteobacteria by both factors. Actinobacteria were characterized as late-stage substrate generalists, while fungi were recognized as substrate specialists and site generalists, particularly in the grassland. Overall, soil conditions determined the decomposition rates in the grassland and forest, but successional patterns of the main decomposers (fungi and Actinobacteria) were determined by litter type. These results suggest that shifts in vegetation mostly affect microbial decomposer community composition.IMPORTANCE Anthropogenic disturbance may cause shifts in vegetation and alter the litter input. We studied the decomposition of different litter types under soil conditions of a nutrient-rich grassland and nutrient-poor forest to identify factors responsible for changes in the community structure and succession of microbial decomposers. This will help to predict the consequences of induced changes on the abundance and activity of microbial decomposers and recognize if the decomposition process and resulting quality and quantity of soil organic matter will be affected at various sites.
- Keywords
- enzyme activities, forest, grassland, organic matter, succession,
- MeSH
- Bacteria classification metabolism MeSH
- Biodiversity MeSH
- Ecosystem MeSH
- Fungi classification metabolism MeSH
- Forests MeSH
- Microbiota * MeSH
- Grassland MeSH
- Soil chemistry MeSH
- Soil Microbiology * MeSH
- RNA, Ribosomal, 16S MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Soil MeSH
- RNA, Ribosomal, 16S 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
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
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.
- Keywords
- bacteria, decomposition, ecosystem processes, forest ecology, global change, litter, nutrient cycling, soil,
- MeSH
- Bacteria metabolism MeSH
- Biomass MeSH
- Nitrogen metabolism MeSH
- Ecosystem * MeSH
- Fungi metabolism MeSH
- Climate Change * MeSH
- Nitrogen Cycle MeSH
- Forests * MeSH
- Microbial Consortia MeSH
- Soil Microbiology * MeSH
- Plants MeSH
- Carbon Sequestration MeSH
- Carbon metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
- Names of Substances
- Nitrogen MeSH
- Carbon MeSH
Identification of bacteria that produce carbohydrolytic enzymes is extremely important given the increased demand for these enzymes in many industries. Twenty lignocellulose-degrading bacterial isolates from Algerian compost and different soils were screened for their potential to produce different enzymes involved in biomass deconstruction. Based on 16S rRNA gene sequencing, the isolates belonged to Proteobacteria and Actinobacteria. Differences among species were reflected both as the presence/absence of enzymes or at the level of enzyme activity. Among the most active species, Bosea sp. FBZP-16 demonstrated cellulolytic activity on both amorphous cellulose (CMC) and complex lignocellulose (wheat straw) and was selected for whole-genomic sequencing. The genome sequencing revealed the presence of a complex enzymatic machinery required for organic matter decomposition. Analysis of the enzyme-encoding genes indicated that multiple genes for endoglucanase, xylanase, β-glucosidase and β-mannosidase are present in the genome with enzyme activities displayed by the bacterium, while other enzymes, such as certain cellobiohydrolases, were not detected at the genomic level. This indicates that a combination of functional screening of bacterial cultures with the use of genome-derived information is important for the prediction of potential enzyme production. These results provide insight into their possible exploitation for the production of fuels and chemicals derived from plant biomass.
- Keywords
- Bosea, Cellulases, Enzyme assays, Genome sequencing, Hemicellulases,
- MeSH
- Actinobacteria genetics isolation & purification MeSH
- Bacterial Proteins genetics metabolism MeSH
- Cellulase genetics metabolism MeSH
- Cellulose metabolism MeSH
- Phylogeny MeSH
- Glycoside Hydrolases genetics metabolism MeSH
- Lignin metabolism MeSH
- Proteobacteria genetics isolation & purification MeSH
- Soil MeSH
- Soil Microbiology MeSH
- Rhizobiaceae enzymology genetics isolation & purification MeSH
- RNA, Ribosomal, 16S genetics MeSH
- Sequence Analysis, RNA methods MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Bacterial Proteins MeSH
- Cellulase MeSH
- Cellulose MeSH
- Glycoside Hydrolases MeSH
- hemicellulase MeSH Browser
- Lignin MeSH
- lignocellulose MeSH Browser
- Soil MeSH
- RNA, Ribosomal, 16S MeSH
Evidence shows that bacteria contribute actively to the decomposition of cellulose and hemicellulose in forest soil; however, their role in this process is still unclear. Here we performed the screening and identification of bacteria showing potential cellulolytic activity from litter and organic soil of a temperate oak forest. The genomes of three cellulolytic isolates previously described as abundant in this ecosystem were sequenced and their proteomes were characterized during the growth on plant biomass and on microcrystalline cellulose. Pedobacter and Mucilaginibacter showed complex enzymatic systems containing highly diverse carbohydrate-active enzymes for the degradation of cellulose and hemicellulose, which were functionally redundant for endoglucanases, β-glucosidases, endoxylanases, β-xylosidases, mannosidases and carbohydrate-binding modules. Luteibacter did not express any glycosyl hydrolases traditionally recognized as cellulases. Instead, cellulose decomposition was likely performed by an expressed GH23 family protein containing a cellulose-binding domain. Interestingly, the presence of plant lignocellulose as well as crystalline cellulose both trigger the production of a wide set of hydrolytic proteins including cellulases, hemicellulases and other glycosyl hydrolases. Our findings highlight the extensive and unexplored structural diversity of enzymatic systems in cellulolytic soil bacteria and indicate the roles of multiple abundant bacterial taxa in the decomposition of cellulose and other plant polysaccharides.
- MeSH
- Bacteria chemistry classification isolation & purification metabolism MeSH
- Bacterial Proteins analysis MeSH
- Cellulose metabolism MeSH
- Quercus growth & development MeSH
- Genome, Bacterial MeSH
- Hydrolysis MeSH
- Forests MeSH
- Polysaccharides metabolism MeSH
- Proteome analysis MeSH
- Soil Microbiology * MeSH
- Sequence Analysis, DNA MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Bacterial Proteins MeSH
- Cellulose MeSH
- hemicellulose MeSH Browser
- Polysaccharides MeSH
- Proteome MeSH