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Deadwood-Inhabiting Bacteria Show Adaptations to Changing Carbon and Nitrogen Availability During Decomposition.

ABSTRACT: 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.

SUBMITTER: Tlaskal V

PROVIDER: S-EPMC8247643 | biostudies-literature | 2021

REPOSITORIES: biostudies-literature

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Deadwood-Inhabiting Bacteria Show Adaptations to Changing Carbon and Nitrogen Availability During Decomposition.

Tláskal Vojtěch V Baldrian Petr P

Frontiers in microbiology 20210617

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 bio ...[more]

PMID: 34220772

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Project description:Forests accumulate and store large amounts of carbon (C), and a substantial fraction of this stock is contained in deadwood. This transient pool is subject to decomposition by deadwood-associated organisms, and in this process it contributes to CO2 emissions. Although fungi and bacteria are known to colonize deadwood, little is known about the microbial processes that mediate carbon and nitrogen (N) cycling in deadwood. In this study, using a combination of metagenomics, metatranscriptomics, and nutrient flux measurements, we demonstrate that the decomposition of deadwood reflects the complementary roles played by fungi and bacteria. Fungi were found to dominate the decomposition of deadwood and particularly its recalcitrant fractions, while several bacterial taxa participate in N accumulation in deadwood through N fixation, being dependent on fungal activity with respect to deadwood colonization and C supply. Conversely, bacterial N fixation helps to decrease the constraints of deadwood decomposition for fungi. Both the CO2 efflux and N accumulation that are a result of a joint action of deadwood bacteria and fungi may be significant for nutrient cycling at ecosystem levels. Especially in boreal forests with low N stocks, deadwood retention may help to improve the nutritional status and fertility of soils.IMPORTANCE Wood represents a globally important stock of C, and its mineralization importantly contributes to the global C cycle. Microorganisms play a key role in deadwood decomposition, since they possess enzymatic tools for the degradation of recalcitrant plant polymers. The present paradigm is that fungi accomplish degradation while commensalist bacteria exploit the products of fungal extracellular enzymatic cleavage, but this assumption was never backed by the analysis of microbial roles in deadwood. This study clearly identifies the roles of fungi and bacteria in the microbiome and demonstrates the importance of bacteria and their N fixation for the nutrient balance in deadwood as well as fluxes at the ecosystem level. Deadwood decomposition is shown as a process where fungi and bacteria play defined, complementary roles.

Project description:Abstract: A large part of the nitrogen in forest soils is found in recalcitrant organic matter-protein complexes. Ectomycorrhizal fungi are thought to have a key role in the decomposition and mobilization of nitrogen from such complexes. The knowledge on the functional mechanisms of these processes, and how they are regulated by carbon from the host plant and the availability of more easily available forms of nitrogen sources are limited. We used spectroscopic analyses and transcriptome profiling to examine how the presence/absence of glucose and ammonium regulates the decomposition and mobilization of nitrogen from litter material by the ectomycorrhizal fungus Paxillus involutus. Amendments of glucose triggered the assimilation of nitrogen and the decomposition of the litter material. Concomitantly, the expression of genes encoding enzymes involved in oxidative (i.e. Fenton chemistry) degradation of polysaccharides and polyphenols, peptidases, nitrogen transporters and enzymes in pathways of the nitrogen and carbon metabolism were upregulated in concert. Addition of ammonium had minute effects on both the expression of transcripts and decomposition of litter material, and only when glucose was present. Based on the spectroscopic analyses, three major types of chemical modifications of the litter material were observed. Each of them was correlated with the expression of specific sets of genes encoding extracellular enzymes. Our data suggests that the expression of the decomposition and nitrogen assimilation machinery of ectomycorrhizal fungi can be firmly regulated by the host carbon supply, i.e. priming, and that the availability of inorganic nitrogen as such has limited effects on the saprotrophic activities. Rineau F, Shah F., Smits M.M., Persson P., Johansson T., Carleer R., Troein C., Tunlid A. (2013) Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus (submitted) A one-chip study (data from 12 subarrays collected from a 12-plex Nimblegen microarray (ID 467991) using total RNA recovered from three separate glass-bead cultures of Paxillus involutus (ATCC200175) after amendments of various soil-derived substrates. Transcriptome profiling to examine how the presence/absence of glucose and ammonium regulates the decomposition and mobilization of nitrogen from litter material by the ectomycorrhizal fungus Paxillus involutus.

Project description:BackgroundDeadwood decomposition is an essential ecological process in forest ecosystems, playing a key role in nutrient cycling and carbon sequestration by enriching soils with organic matter. This process is driven by diverse microbial communities encompassing specialized functions in breaking down organic matter, but the specific roles of individual microorganisms in this process are still not fully understood.ResultsHere, we characterized the deadwood microbiome in a natural mixed temperate forest in Central Europe using PacBio HiFi long-read sequencing and a genome-resolved transcriptomics approach in order to uncover key microbial contributors to wood decomposition. We obtained high quality assemblies, which allowed attribution of complex microbial functions such as nitrogen fixation to individual microbial taxa and enabled the recovery of metagenome-assembled genomes (MAGs) from both abundant and rare deadwood bacteria. We successfully assembled 69 MAGs (including 14 high-quality and 7 single-contig genomes) from 4 samples, representing most of the abundant bacterial phyla in deadwood. The MAGs exhibited a rich diversity of carbohydrate-active enzymes (CAZymes), with Myxococcota encoding the highest number of CAZymes and the full complement of enzymes required for cellulose decomposition. For the first time we observed active nitrogen fixation by Steroidobacteraceae, as well as hemicellulose degradation and chitin recycling by Patescibacteria. Furthermore, PacBio HiFi sequencing identified over 1000 biosynthetic gene clusters, highlighting a vast potential for secondary metabolite production in deadwood, particularly in Pseudomonadota and Myxococcota.ConclusionsPacBio HiFi long-read sequencing offers comprehensive insights into deadwood decomposition processes by advancing the identification of functional features involving multiple genes. It represents a robust tool for unraveling novel microbial genomes in complex ecosystems and allows the identification of key microorganisms contributing to deadwood decomposition.

Dataset Information

Deadwood-Inhabiting Bacteria Show Adaptations to Changing Carbon and Nitrogen Availability During Decomposition.

Publications

Deadwood-Inhabiting Bacteria Show Adaptations to Changing Carbon and Nitrogen Availability During Decomposition.

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