Decomposition Of Plant Biomass Research Articles

Comparative genomics unravels a rich set of biosynthetic gene clusters with distinct evolutionary trajectories across fungal species (Termitomyces) farmed by termites

The use of compounds produced by hosts or symbionts for defence against antagonists has been identified in many organisms, including in fungus-farming termites (Macrotermitinae). The obligate mutualistic fungus Termitomyces plays a pivotal role in plant biomass decomposition and as the primary food source for these termites. Despite the isolation of various specialized metabolites from different Termitomyces species, our grasp of their natural product repertoire remains incomplete. To address this knowledge gap, we conducted a comprehensive analysis of 39 Termitomyces genomes, representing 21 species associated with members of five termite host genera. We identified 754 biosynthetic gene clusters (BGCs) coding for specialized metabolites and categorized 660 BGCs into 61 biosynthetic gene cluster families (GCFs) spanning five compound classes. Seven GCFs were shared by all 21 Termitomyces species and 21 GCFs were present in all genomes of subsets of species. Evolutionary constraint analyses on the 25 most abundant GCFs revealed distinctive evolutionary histories, signifying that millions of years of termite-fungus symbiosis have influenced diverse biosynthetic pathways. This study unveils a wealth of non-random and largely undiscovered chemical potential within Termitomyces and contributes to our understanding of the intricate evolutionary trajectories of biosynthetic gene clusters in the context of long-standing symbiosis.

Linking microbial carbon‐degrading potential to organic carbon sequestration in fertilized soils: Insights from metagenomics

AbstractThe capacity of soils to store organic carbon (SOC) is vital for agricultural productivity. Soil microorganisms exert a critical role in carbon (C) flow and potentially influence C balance through the decomposition of plant and microbial dead biomass. However, the connection between the microbial degradation potential of plant‐derived and microbial‐derived C and soil organic carbon sequestration (SOCSR) under organic and inorganic nitrogen (N) fertilization treatments remains largely unexplored using metagenomics. In this study, metagenomics was used to investigate the effects of 4 years inorganic (N1: 250 kg N ha−1 yr−1 and N3: 450 kg N ha−1 yr−1) and organic N (O1: N1 + 11,250 kg ha−1 yr−1 sheep manure and O3: N1 + 18,750 kg ha−1 yr−1 sheep manure) fertilizer application on plant biomass decomposition genes, microbial biomass decomposition genes, and microbial properties related to different sources of C decomposition (species composition and diversity). Furthermore, the study explored the relationship between organic matter decomposition genes, microorganisms, and SOCSR. The results revealed that compared with N1 treatment, the increased application of inorganic N fertilizer (N3) significantly enhanced the abundance of genes related to plant and microbial biomass decomposition and microbial diversity involved in SOC decomposition, resulting in reduced SOC content. Conversely, the increased application of organic N fertilizer (O1 and O3) had a minor effect on the abundance of genes related to different sources of C decomposition and C decomposing microbial diversity, but reduced microbial entropy (the ratio of microbial biomass carbon to SOC) and increased SOC content. The random forest model highlighted that plant biomass decomposition genes and bacterial community composition were important factors affecting SOCSR. The Mantel test also indicated that the genes involved in the decomposition of lignin, cellulose, and hemicellulose were closely related to SOCSR. These findings highlighted that increased inorganic N fertilizers greatly enhanced the microbial capacity for SOC decomposition, resulting in reduced SOC accumulation. While the increased application of organic N fertilizer increased SOC stability and reduced the mineralization potential of SOC, contributing to SOCSR. Overall, these findings provide a greater understanding of the relationship between soil C turnover and microbial C‐degrading potential under short‐term fertilization. And in a long time, they may have important implications for global strategies aimed at increasing SOCSR to restore fertility and facilitate sustainable agricultural development.

Hydrogen Production from Barley Straw and Miscanthus by the Hyperthermophilic Bacterium, Cadicellulosirupter bescii.

This work aimed to evaluate the feasibility of biohydrogen production from Barley Straw and Miscanthus. The primary obstacle in plant biomass decomposition is the recalcitrance of the biomass itself. Plant cell walls consist of cellulose, hemicellulose, and lignin, which make the plant robust to decomposition. However, the hyperthermophilic bacterium, Caldicellulosiruptor bescii, can efficiently utilize lignocellulosic feedstocks (Barley Straw and Miscanthus) for energy production, and C. bescii can now be metabolically engineered or isolated to produce more hydrogen and other biochemicals. In the present study, two strains, C. bescii JWCB001 (wild-type) and JWCB018 (ΔpyrFA Δldh ΔcbeI), were tested for their ability to increase hydrogen production from Barley Straw and Miscanthus. The JWCB018 resulted in a redirection of carbon and electron (carried by NADH) flow from lactate production to acetate and hydrogen production. JWCB018 produced ~54% and 63% more acetate and hydrogen from Barley Straw, respectively than its wild-type counterpart, JWCB001. Also, 25% more hydrogen from Miscanthus was obtained by the JWCB018 strain with 33% more acetate relative to JWCB001. It was supported that the engineered C. bescii, such as the JWCB018, can be a parental strain to get more hydrogen and other biochemicals from various biomass.

Tripartite Symbiotic Digestion of Lignocellulose in the Digestive System of a Fungus-Growing Termite.

Fungus-growing termites are efficient in degrading and digesting plant substrates, achieved through the engagement of symbiotic gut microbiota and lignocellulolytic Termitomyces fungi cultivated for protein-rich food. Insights into where specific plant biomass components are targeted during the decomposition process are sparse. In this study, we performed several analytical approaches on the fate of plant biomass components and did amplicon sequencing of the 16S rRNA gene to investigate the lignocellulose digestion in the symbiotic system of the fungus-growing termite Odontotermes formosanus (Shiraki) and to compare bacterial communities across the different stages in the degradation process. We observed a gradual reduction of lignocellulose components throughout the process. Our findings support that the digestive tract of young workers initiates the degradation of lignocellulose but leaves most of the lignin, hemicellulose, and cellulose, which enters the fresh fungus comb, where decomposition primarily occurs. We found a high diversity and quantity of monomeric sugars in older parts of the fungus comb, indicating that the decomposition of lignocellulose enriches the old comb with sugars that can be utilized by Termitomyces and termite workers. Amplicon sequencing of the 16S rRNA gene showed clear differences in community composition associated with the different stages of plant biomass decomposition which could work synergistically with Termitomyces to shape the digestion process. IMPORTANCE Fungus-farming termites have a mutualist association with fungi of the genus Termitomyces and gut microbiota to support the nearly complete decomposition of lignocellulose to gain access to nutrients. This elaborate strategy of plant biomass digestion makes them ecologically successful dominant decomposers in (sub)tropical Old World ecosystems. We employed acid detergent fiber analysis, high-performance anion-exchange chromatography (HPAEC), high-performance liquid chromatography (HPLC), scanning electron microscopy (SEM), Fourier transform infrared spectroscopy (FTIR), X-ray diffraction (XRD), pyrolysis gas chromatography-mass spectrometry (Py-GC-MS), and amplicon sequencing of the 16S rRNA gene to examine which lignocellulose components were digested and which bacteria were abundant throughout the decomposition process. Our findings suggest that although the first gut passage initiates lignocellulose digestion, the most prominent decomposition occurs within the fungus comb. Moreover, distinct bacterial communities were associated with different stages of decomposition, potentially contributing to the breakdown of particular plant components.

The Structure of Stable Cellulolytic Consortia Isolated from Natural Lignocellulosic Substrates.

Recycling plant matter is one of the challenges facing humanity today and depends on efficient lignocellulose degradation. Although many bacterial strains from natural substrates demonstrate cellulolytic activities, the CAZymes (Carbohydrate-Active enZYmes) responsible for these activities are very diverse and usually distributed among different bacteria in one habitat. Thus, using microbial consortia can be a solution to rapid and effective decomposition of plant biomass. Four cellulolytic consortia were isolated from enrichment cultures from composting natural lignocellulosic substrates—oat straw, pine sawdust, and birch leaf litter. Enrichment cultures facilitated growth of similar, but not identical cellulose-decomposing bacteria from different substrates. Major components in all consortia were from Proteobacteria, Actinobacteriota and Bacteroidota, but some were specific for different substrates—Verrucomicrobiota and Myxococcota from straw, Planctomycetota from sawdust and Firmicutes from leaf litter. While most members of the consortia were involved in the lignocellulose degradation, some demonstrated additional metabolic activities. Consortia did not differ in the composition of CAZymes genes, but rather in axillary functions, such as ABC-transporters and two-component systems, usually taxon-specific and associated with CAZymes. Our findings show that enrichment cultures can provide reproducible cellulolytic consortia from various lignocellulosic substrates, the stability of which is ensured by tight microbial relations between its components.

Impact of Collembola on the Winter Wheat Growth in Soil Infected by Soil-Borne Pathogenic Fungi

The activity of some soil organisms can significantly influence the growth of plants. One of the more common are Collembola, which play an important role in suppressing soil-borne pathogens such as Fusarium spp. Here, Folsomia candida was taken for laboratory studies. The aim of the study was to assess whether springtails influence the growth of wheat and pea plants. The purpose was also to evaluate whether Collembola will reduce the occurrence of fungal diseases, presumably by feeding on fungi. The factors tested were (1) wheat grown individually or in the mixture with pea; (2) number of Collembola; and (3) the pathogenic presence of the plant fungus Fusarium culmorum. The experiment was carried out in four replicates for each treatment in two series. The soil used for the test was a mixture of field soil, sand, and peat. The following analyses were performed: measuring plant growth and decomposition rate, assessment of plant infection, and assessment of F. culmorum in springtails bodies. There was no effect of F. culmorum infection on plant growth, although the pathogen was present in the root neck of the plants incubated with this fungus. Collembola decreased the number of fungus colonies isolated from plants by about 45% in comparison to pots incubated without these organisms. The decomposition of plant biomass was accelerated by springtails by about 7% in the pots with moderate Collembola number. However, this was not related to improved plant growth. Additionally, F. culmorum was isolated from the bodies of Collembola, indicating its ability to feed on this fungus. To conclude, it was found that Collembola can decrease pathogenic fungal growth. This issue needs further studies in relation to other plants and fungus species, as well to study observed effects in the field conditions.

Long-Term Cellulose Enrichment Selects for Highly Cellulolytic Consortia and Competition for Public Goods.

ABSTRACTThe complexity of microbial communities hinders our understanding of how microbial diversity and microbe-microbe interactions impact community functions. Here, using six independent communities originating from the refuse dumps of leaf-cutter ants and enriched using the plant polymer cellulose as the sole source of carbon, we examine how changes in bacterial diversity and interactions impact plant biomass decomposition. Over up to 60 serial transfers (∼8 months) using Whatman cellulose filter paper, cellulolytic ability increased and then stabilized in four enrichment lines and was variable in two lines. Bacterial community characterization using 16S rRNA gene amplicon sequencing showed community succession differed between the highly cellulolytic enrichment lines and those that had slower and more variable cellulose degradation rates. Metagenomic and metatranscriptomic analyses revealed that Cellvibrio and/or Cellulomonas dominated each enrichment line and produced the majority of cellulase enzymes, while diverse taxa were retained within these communities over the duration of transfers. Interestingly, the less cellulolytic communities had a higher diversity of organisms competing for the cellulose breakdown product cellobiose, suggesting that cheating slowed cellulose degradation. In addition, we found competitive exclusion as an important factor shaping all of the communities, with a negative correlation of Cellvibrio and Cellulomonas abundance within individual enrichment lines and the expression of genes associated with the production of secondary metabolites, toxins, and other antagonistic compounds. Our results provide insights into how microbial diversity and competition affect the stability and function of cellulose-degrading communities.IMPORTANCE Microbial communities are a key driver of the carbon cycle through the breakdown of complex polysaccharides in diverse environments including soil, marine systems, and the mammalian gut. However, due to the complexity of these communities, the species-species interactions that impact community structure and ultimately shape the rate of decomposition are difficult to define. Here, we performed serial enrichment on cellulose using communities inoculated from leaf-cutter ant refuse dumps, a cellulose-rich environment. By concurrently tracking cellulolytic ability and community composition and through metagenomic and metatranscriptomic sequencing, we analyzed the ecological dynamics of the enrichment lines. Our data suggest that antagonism is prevalent in these communities and that competition for soluble sugars may slow degradation and lead to community instability. Together, these results help reveal the relationships between competition and polysaccharide decomposition, with implications in diverse areas ranging from microbial community ecology to cellulosic biofuels production.

Coupling plant litter quantity to a novel metric for litter quality explains C storage changes in a thawing permafrost peatland.

Permafrost thaw is a major potential feedback source to climate change as it can drive the increased release of greenhouse gases carbon dioxide (CO2) and methane (CH4). This carbon release from the decomposition of thawing soil organic material can be mitigated by increased net primary productivity (NPP) caused by warming, increasing atmospheric CO2, and plant community transition. However, the net effect on C storage also depends on how these plant community changes alter plant litter quantity, quality, and decomposition rates. Predicting decomposition rates based on litter quality remains challenging, but a promising new way forward is to incorporate measures of the energetic favorability to soil microbes of plant biomass decomposition. We asked how the variation in one such measure, the nominal oxidation state of carbon (NOSC), interacts with changing quantities of plant material inputs to influence the net C balance of a thawing permafrost peatland. We found: (1) Plant productivity (NPP) increased post‐thaw, but instead of contributing to increased standing biomass, it increased plant biomass turnover via increased litter inputs to soil; (2) Plant litter thermodynamic favorability (NOSC) and decomposition rate both increased post‐thaw, despite limited changes in bulk C:N ratios; (3) these increases caused the higher NPP to cycle more rapidly through both plants and soil, contributing to higher CO2 and CH4 fluxes from decomposition. Thus, the increased C‐storage expected from higher productivity was limited and the high global warming potential of CH4 contributed a net positive warming effect. Although post‐thaw peatlands are currently C sinks due to high NPP offsetting high CO2 release, this status is very sensitive to the plant community's litter input rate and quality. Integration of novel bioavailability metrics based on litter chemistry, including NOSC, into studies of ecosystem dynamics, is needed to improve the understanding of controls on arctic C stocks under continued ecosystem transition.

Using MALDI-FTICR-MS Imaging to Track Low-Molecular-Weight Aromatic Derivatives of Fungal Decayed Wood.

Low-molecular-weight (LMW) aromatics are crucial in meditating fungal processes for plant biomass decomposition. Some LMW compounds are employed as electron donors for oxidative degradation in brown rot (BR), an efficient wood-degrading strategy in fungi that selectively degrades carbohydrates but leaves modified lignins. Previous understandings of LMW aromatics were primarily based on “bulk extraction”, an approach that cannot fully reflect their real-time functions during BR. Here, we applied an optimized molecular imaging method that combines matrix-assisted laser desorption ionization (MALDI) with Fourier-transform ion cyclotron resonance mass spectrometry (FTICR-MS) to directly measure the temporal profiles of BR aromatics as Rhodonia placenta decayed a wood wafer. We found that some phenolics were pre-existing in wood, while some (e.g., catechin-methyl ether and dihydroxy-dimethoxyflavan) were generated immediately after fungal activity. These pinpointed aromatics might be recruited to drive early BR oxidative mechanisms by generating Fenton reagents, Fe2+ and H2O2. As BR progressed, ligninolytic products were accumulated and then modified into various aromatic derivatives, confirming that R. placenta depolymerizes lignin. Together, this work confirms aromatic patterns that have been implicated in BR fungi, and it demonstrates the use of MALDI-FTICR-MS imaging as a new approach to monitor the temporal changes of LMW aromatics during wood degradation.

Complementary Contribution of Fungi and Bacteria to Lignocellulose Digestion in the Food Stored by a Neotropical Higher Termite

Lignocellulose digestion in termites is achieved through the functional synergy between gut symbionts and host enzymes. However, some species have evolved additional associations with nest microorganisms that collaborate in the decomposition of plant biomass. In a previous study, we determined that plant material packed with feces inside the nests of Cornitermes cumulans (Syntermitinae) harbors a distinct microbial assemblage. These food nodules also showed a high hemicellulolytic activity, possibly acting as an external place for complementary lignocellulose digestion. In this study, we used a combination of ITS sequence analysis, metagenomics, and metatranscriptomics to investigate the presence and differential expression of genes coding for carbohydrate-active enzymes (CAZy) in the food nodules and the gut of workers and soldiers. Our results confirm that food nodules express a distinct set of CAZy genes suggesting that stored plant material is initially decomposed by enzymes that target the lignin and complex polysaccharides from fungi and bacteria before the passage through the gut, where it is further targeted by a complementary set of cellulases, xylanases, and esterases produced by the gut microbiota and the termite host. We also showed that the expression of CAZy transcripts associated to endoglucanases and xylanases was higher in the gut of termites than in the food nodules. An additional finding in this study was the presence of fungi in the termite gut that expressed CAZy genes. This study highlights the importance of externalization of digestion by nest microbes and provides new evidence of complementary digestion in the context of higher termite evolution.

Onset of runaway fragmentation of salt marshes

Summary Salt marshes are valuable but vulnerable coastal ecosystems that adapt to relative sea level rise (RSLR) by accumulating organic matter and inorganic sediment. The natural limit of these processes defines a threshold rate of RSLR beyond which marshes drown, resulting in ponding and conversion to open waters. We develop a simplified formulation for sediment transport across marshes to show that pond formation leads to runaway marsh fragmentation, a process characterized by a self-similar hierarchy of pond sizes with power-law distributions. We find the threshold for marsh fragmentation scales primarily with tidal range and that sediment supply is only relevant where tides are sufficient to transport sediment to the marsh interior. Thus the RSLR threshold is controlled by organic accretion in microtidal marshes regardless of the suspended sediment concentration at the marsh edge. This explains the observed fragmentation of microtidal marshes and suggests a tipping point for widespread marsh loss.

A 16‐year investigation of legacy phosphorus discharge from Prairie Wolf Slough: a wetland restored on a former farmed field

Phosphorus (P) release to surface and groundwater often occurs in wetlands that were restored on former agricultural fields. We identified pore water, shallow groundwater, and plant biomass decomposition as sources of soluble reactive (SRP) and total phosphorus (TP) export to the Chicago River between 1998 and 2014 from Prairie Wolf Slough Wetland Demonstration Project (PWS), a wetland restored on a former farmed field in suburban Chicago, Illinois. We estimated the relative annual contributions of SRP from these sources to yearly discharge to the river and conducted an SRP mass balance. SRP and TP concentrations and loadings were consistently greater at the outlet compared to the inlet, suggesting PWS was a source of P. Twenty‐three grams of SRP was exported during the mass balance study. SRP concentration at the inlet accounted for less than 3% of the SRP exported annually at the outlet to the Chicago River. Plant biomass decomposition, pore water diffusion, and groundwater seepage together accounted for 85% of annual export. Twelve percent of annual SRP export remains unknown. PWS was ineffective in reducing P export, indicating an ecosystem disservice. Our study highlights the need to identify the sources of P exported from wetlands restored on farm fields to better understand the biogeochemical processes that determine whether a wetland will serve as a source or sink of P. Pre‐restoration measurement, followed by decadal‐scale post‐restoration monitoring, of source‐water and soil P are needed to evaluate the success of wetland restorations designed to sequester P from runoff.

A Novel Digestive GH16 β-1,3(4)-Glucanase from the Fungus-Growing Termite Macrotermes barneyi.

β-1,3-glucanases are the main digestive enzymes of plant and fungal cell wall. Transcriptomic analysis of the fungus-growing termite Macrotermes barneyi revealed a high expression of a predicted β-1,3(4)-glucanase (Mbbgl) transcript in termite gut. Here, we described the cDNA cloning, heterologous expression, and enzyme characterization of Mbbgl. Sequence analysis and RT-PCR results showed that Mbbgl is a termite-origin GH16 β-1,3(4)-glucanase. The recombinant enzyme showed the highest activity towards laminarin and was active optimally at 50°C, pH5.5. The enzyme displayed endo/exo β-1,3(4)-glucanase activities. Moreover, Mbbgl had weak transglycosylation activity. The results indicate that Mbbgl is an endogenous digestive β-1,3(4)-glucanase, which contributes to the decomposition of plant biomass and fungal hyphae. Additionally, the multiple activities, pH, and ion stabilities make Mbbgl a potential candidate for application in the food industry.

Impact of vegetation harvesting on nutrient removal and plant biomass quality in wetland buffer zones

Fertiliser use in agriculture increases the non-point pollution of waters with nitrogen (N) and phosphorus (P). Wetland buffer zones (WBZs) are wetland ecosystems between agricultural lands and water bodies that protect surface waters from non-point source pollution. We assessed how vegetation harvesting within WBZs impacts their N and P removal efficiency, nutrient uptake by plants and their biomass quality. We surveyed vegetation of a spontaneously rewetted fen along a small river in Poland, and analysed plant biomass, its nutrient contents and nutrient-leaching potential and the water chemistry. Total N removal reached 34–92% and total P removal 17–63%. N removal was positively related to the initial N concentration, regardless of mowing status. We found a high N removal efficiency (92%) in the harvested site. Vegetation of mown sites differed from that of unmown sites by a higher water-leached carbon and P contents in the biomass. We found that vegetation harvesting may stimulate the overall N removal, but may increase potential biomass decomposability, which eases the recycling of plant-incorporated nutrients back to WBZ. Thus, mowing should always be followed by the removal of biomass. Neglecting already mown WBZs may temporarily lower their nutrient removal efficiency due to potentially faster decomposition of plant biomass.

Genomes and secretomes of Ascomycota fungi reveal diverse functions in plant biomass decomposition and pathogenesis

BackgroundThe dominant fungi in arid grasslands and shrublands are members of the Ascomycota phylum. Ascomycota fungi are important drivers in carbon and nitrogen cycling in arid ecosystems. These fungi play roles in soil stability, plant biomass decomposition, and endophytic interactions with plants. They may also form symbiotic associations with biocrust components or be latent saprotrophs or pathogens that live on plant tissues. However, their functional potential in arid soils, where organic matter, nutrients and water are very low or only periodically available, is poorly characterized.ResultsFive Ascomycota fungi were isolated from different soil crust microhabitats and rhizosphere soils around the native bunchgrass Pleuraphis jamesii in an arid grassland near Moab, UT, USA. Putative genera were Coniochaeta, isolated from lichen biocrust, Embellisia from cyanobacteria biocrust, Chaetomium from below lichen biocrust, Phoma from a moss microhabitat, and Aspergillus from the soil. The fungi were grown in replicate cultures on different carbon sources (chitin, native bunchgrass or pine wood) relevant to plant biomass and soil carbon sources. Secretomes produced by the fungi on each substrate were characterized. Results demonstrate that these fungi likely interact with primary producers (biocrust or plants) by secreting a wide range of proteins that facilitate symbiotic associations. Each of the fungal isolates secreted enzymes that degrade plant biomass, small secreted effector proteins, and proteins involved in either beneficial plant interactions or virulence. Aspergillus and Phoma expressed more plant biomass degrading enzymes when grown in grass- and pine-containing cultures than in chitin. Coniochaeta and Embellisia expressed similar numbers of these enzymes under all conditions, while Chaetomium secreted more of these enzymes in grass-containing cultures.ConclusionsThis study of Ascomycota genomes and secretomes provides important insights about the lifestyles and the roles that Ascomycota fungi likely play in arid grassland, ecosystems. However, the exact nature of those interactions, whether any or all of the isolates are true endophytes, latent saprotrophs or opportunistic phytopathogens, will be the topic of future studies.

The Cellulosome Paradigm in An Extreme Alkaline Environment.

Rapid decomposition of plant biomass in soda lakes is associated with microbial activity of anaerobic cellulose-degrading communities. The alkaliphilic bacterium, Clostridium alkalicellulosi, is the single known isolate from a soda lake that demonstrates cellulolytic activity. This microorganism secretes cellulolytic enzymes that degrade cellulose under anaerobic and alkaliphilic conditions. A previous study indicated that the protein fraction of cellulose-grown cultures showed similarities in composition and size to known components of the archetypical cellulosome Clostridium thermocellum. Bioinformatic analysis of the C. alkalicellulosi draft genome sequence revealed 44 cohesins, organized into 22 different scaffoldins, and 142 dockerin-containing proteins. The modular organization of the scaffoldins shared similarities to those of C. thermocellum and Acetivibrio cellulolyticus, whereas some exhibited unconventional arrangements containing peptidases and oxidative enzymes. The binding interactions among cohesins and dockerins assessed by ELISA, revealed a complex network of cellulosome assemblies and suggested both cell-associated and cell-free systems. Based on these interactions, C. alkalicellulosi cellulosomal systems have the genetic potential to create elaborate complexes, which could integrate up to 105 enzymatic subunits. The alkalistable C. alkalicellulosi cellulosomal systems and their enzymes would be amenable to biotechnological processes, such as treatment of lignocellulosic biomass following prior alkaline pretreatment.

Symbiotic Plant Biomass Decomposition in Fungus-Growing Termites.

Termites are among the most successful animal groups, accomplishing nutrient acquisition through long-term associations and enzyme provisioning from microbial symbionts. Fungus farming has evolved only once in a single termite sub-family: Macrotermitinae. This sub-family has become a dominant decomposer in the Old World; through enzymatic contributions from insects, fungi, and bacteria, managed in an intricate decomposition pathway, the termites obtain near-complete utilisation of essentially any plant substrate. Here we review recent insights into our understanding of the process of plant biomass decomposition in fungus-growing termites. To this end, we outline research avenues that we believe can help shed light on how evolution has shaped the optimisation of plant-biomass decomposition in this complex multipartite symbiosis.

Biodegradation of crop residue-derived organic matter is influenced by its heteroatomic stoichiometry and molecular composition

Plant biomass is the primary source material for soil organic matter formation. Soil organic matter comprises the largest terrestrial pool of the global C cycle and provides critical ecosystem services. The objective of this study was to document microbially-driven molecular-level changes to the water-soluble organic matter (WSOM) fraction extracted from crop residues as it undergoes biodegradation in laboratory microcosms using ultrahigh resolution mass spectrometry. Crop residues from corn and soybean fields after harvest and a leguminous, hairy vetch green manure were the sources of the WSOM studied. The results show that, at the individual molecule-level, the biodegradation process does not follow the expected trends, i.e. that higher N and lower lignin concentrations in plant biomass should favor its decomposition compared to material with lower N and higher lignin. We also show that S- and P-containing molecules are consistently more biodegradable, as compared to N-containing molecules. In addition, the results suggest that carbohydrate molecules may be less biodegradable, and that aromatic compounds may be more biodegradable, than conventionally understood. Future studies are suggested to increase our knowledge of microbially-driven biodegradation of plant biomass. Understanding plant biomass decomposition at the molecular level is fundamental to understanding how soil organic matter forms and is stabilized. This knowledge is necessary to design management practices to preserve soil organic matter and the ecosystem services it provides.

Links Between Heathland Fungal Biomass Mineralization, Melanization, and Hydrophobicity.

Comprehending the decomposition process is crucial for our understanding of the mechanisms of carbon (C) sequestration in soils. The decomposition of plant biomass has been extensively studied. It revealed that extrinsic biomass properties that restrict its access to decomposers influence decomposition more than intrinsic ones that are only related to its chemical structure. Fungal biomass has been much less investigated, even though it contributes to a large extent to soil organic matter, and is characterized by specific biochemical properties. In this study, we investigated the extent to which decomposition of heathland fungal biomass was affected by its hydrophobicity (extrinsic property) and melanin content (intrinsic property). We hypothesized that, as for plant biomass, hydrophobicity would have a greater impact on decomposition than melanin content. Mineralization was determined as the mineralization of soil organic carbon (SOC) into CO2 by headspace GC/MS after inoculation by a heathland soil microbial community. Results show that decomposition was not affected by hydrophobicity, but was negatively correlated with melanin content. We argue that it may indicate that either melanin content is both an intrinsic and extrinsic property, or that some soil decomposers evolved the ability to use surfactants to access to hydrophobic biomass. In the latter case, biomass hydrophobicity should not be considered as a crucial extrinsic factor. We also explored the ecology of decomposition, melanin content, and hydrophobicity, among heathland soil fungal guilds. Ascomycete black yeasts had the highest melanin content, and hyaline Basidiomycete yeasts the lowest. Hydrophobicity was an all-or-nothing trait, with most isolates being hydrophobic.

Enzyme Activities at Different Stages of Plant Biomass Decomposition in Three Species of Fungus-Growing Termites.

ABSTRACTFungus-growing termites rely on mutualistic fungi of the genus Termitomyces and gut microbes for plant biomass degradation. Due to a certain degree of symbiont complementarity, this tripartite symbiosis has evolved as a complex bioreactor, enabling decomposition of nearly any plant polymer, likely contributing to the success of the termites as one of the main plant decomposers in the Old World. In this study, we evaluated which plant polymers are decomposed and which enzymes are active during the decomposition process in two major genera of fungus-growing termites. We found a diversity of active enzymes at different stages of decomposition and a consistent decrease in plant components during the decomposition process. Furthermore, our findings are consistent with the hypothesis that termites transport enzymes from the older mature parts of the fungus comb through young worker guts to freshly inoculated plant substrate. However, preliminary fungal RNA sequencing (RNA-seq) analyses suggest that this likely transport is supplemented with enzymes produced in situ. Our findings support that the maintenance of an external fungus comb, inoculated with an optimal mixture of plant material, fungal spores, and enzymes, is likely the key to the extraordinarily efficient plant decomposition in fungus-growing termites.IMPORTANCE Fungus-growing termites have a substantial ecological footprint in the Old World (sub)tropics due to their ability to decompose dead plant material. Through the establishment of an elaborate plant biomass inoculation strategy and through fungal and bacterial enzyme contributions, this farming symbiosis has become an efficient and versatile aerobic bioreactor for plant substrate conversion. Since little is known about what enzymes are expressed and where they are active at different stages of the decomposition process, we used enzyme assays, transcriptomics, and plant content measurements to shed light on how this decomposition of plant substrate is so effectively accomplished.