Bacterial contributions to delignification and lignocellulose degradation in forest soils with metagenomic and quantitative stable isotope probing

Abstract

Delignification, or lignin-modification, facilitates the decomposition of lignocellulose in woody plant biomass. The extant diversity of lignin-degrading bacteria and fungi is underestimated by culture-dependent methods, limiting our understanding of the functional and ecological traits of decomposers populations. Here, we describe the use of stable isotope probing (SIP) coupled with amplicon and shotgun metagenomics to identify and characterize the functional attributes of lignin, cellulose and hemicellulose-degrading fungi and bacteria in coniferous forest soils from across North America. We tested the extent to which catabolic genes partitioned among different decomposer taxa; the relative roles of bacteria and fungi, and whether taxa or catabolic genes correlated with variation in lignocellulolytic activity, measured as the total assimilation of 13C-label into DNA and phospholipid fatty acids. We found high overall bacterial degradation of our model lignin substrate, particularly by gram-negative bacteria (Comamonadaceae and Caulobacteraceae), while fungi were more prominent in cellulose-degradation. Very few taxa incorporated 13C-label from more than one lignocellulosic polymer, suggesting specialization among decomposers. Collectively, members of Caulobacteraceae could degrade all three lignocellulosic polymers, providing new evidence for their importance in lignocellulose degradation. Variation in lignin-degrading activity was better explained by microbial community properties, such as catabolic gene content and community structure, than cellulose-degrading activity. SIP significantly improved shotgun metagenome assembly resulting in the recovery of several high-quality draft metagenome-assembled genomes and over 7500 contigs containing unique clusters of carbohydrate-active genes. These results improve understanding of which organisms, conditions and corresponding functional genes contribute to lignocellulose decomposition.

Dissimilar responses of fungal and bacterial communities to soil transplantation simulating abrupt climate changes

“…As a result, fungi play a major role in mediating below‐ground carbon cycling in terrestrial ecosystems (Baldrian et al, ; Zifcakova, Vetrovsky, Howe, & Baldrian, ). However, bacteria are increasingly recognized to play a more important role in litter decomposition than previously thought (Glassman et al, ; Lopez‐Mondejar et al, ; Wilhelm, Singh, Eltis, & Mohn, ). Shifts in bacterial composition were found to have a stronger effect on grassland litter decomposition rates than fungi, while initial bacterial or fungal abundance appeared not to affect litter decomposition (Glassman et al, ).…”

Dispersal and nutrient limitations of decomposition above the forest floor: Evidence from experimental manipulations of epiphytes and macronutrients

“…Similarly, when separated from epiphyte mats and soil, decomposer communities have fewer termites, fungal saprotrophs and nutrient‐translocating fungi (Boddy, ; Gora, Lucas, et al, ; Law et al, ). Canopy soil presumably facilitates bacterial colonization as well, but the importance of bacteria during decomposition is chronically underestimated (Bhatnagar et al, ; Wilhelm, Singh, Eltis, & Mohn, ) and little information exists regarding arboreal prokaryotes (Lambais, Crowley, Cury, Büll, & Rodrigues, ). If nutrient availability and fungal dispersal limit canopy‐level decomposition, then rapidly decomposing substrates on epiphyte mats should exhibit elevated nutrient concentrations and support saprotroph‐dominated microbial communities.…”

Organic soil amendment with Spent Mushroom Substrate results in fungal colonisation, alters bacterial-fungal co-occurrence patterns and improves plant productivity

“…In contrast, none of the bacterial hubs were detected in the SMS substrate community, suggesting they were part of the indigenous soil microbiota. Soil-borne bacterial hub taxa tended to increase their relative abundance with time ( Figure S8 ), and included taxa known for containing cellulose-degrading strains, such as the Proteobacteria families Bulkholderiaceae (Wilhelm et al, 2019) and Polyangiaceae (Garcia and Müller, 2014). Hub microbes with ecologically relevant roles in the community are more likely to function as keystones (Agler et al, 2016), which are taxa that may exert major influences on community structure and functioning and ecosystem processes (Agler et al, 2016; Banerjee et al, 2018).…”