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Solid-, solution-, and gas-state NMR monitoring of ¹³C-cellulose degradation in an anaerobic microbial ecosystem.

ABSTRACT: Anaerobic digestion of biomacromolecules in various microbial ecosystems is influenced by the variations in types, qualities, and quantities of chemical components. Nuclear magnetic resonance (NMR) spectroscopy is a powerful tool for characterizing the degradation of solids to gases in anaerobic digestion processes. Here we describe a characterization strategy using NMR spectroscopy for targeting the input solid insoluble biomass, catabolized soluble metabolites, and produced gases. ¹³C-labeled cellulose produced by Gluconacetobacter xylinus was added as a substrate to stirred tank reactors and gradually degraded for 120 h. The time-course variations in structural heterogeneity of cellulose catabolism were determined using solid-state NMR, and soluble metabolites produced by cellulose degradation were monitored using solution-state NMR. In particular, cooperative changes between the solid NMR signal and ¹³C-¹³C/¹³C-¹²C isotopomers in the microbial degradation of ¹³C-cellulose were revealed by a correlation heat map. The triple phase NMR measurements demonstrated that cellulose was anaerobically degraded, fermented, and converted to methane gas from organic acids such as acetic acid and butyric acid.

SUBMITTER: Yamazawa A

PROVIDER: S-EPMC6269877 | biostudies-literature | 2013 Jul

REPOSITORIES: biostudies-literature

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Solid-, solution-, and gas-state NMR monitoring of ¹³C-cellulose degradation in an anaerobic microbial ecosystem.

Yamazawa Akira A Iikura Tomohiro T Shino Amiu A Date Yasuhiro Y Kikuchi Jun J

Molecules (Basel, Switzerland) 20130729 8

Anaerobic digestion of biomacromolecules in various microbial ecosystems is influenced by the variations in types, qualities, and quantities of chemical components. Nuclear magnetic resonance (NMR) spectroscopy is a powerful tool for characterizing the degradation of solids to gases in anaerobic digestion processes. Here we describe a characterization strategy using NMR spectroscopy for targeting the input solid insoluble biomass, catabolized soluble metabolites, and produced gases. ¹³C-labeled ...[more]

PMID: 23899835

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Project description:Chitin is massively produced by freshwater plankton species as a structural element of their exoskeleton or cell wall. At the same time, chitin does not accumulate in the predominantly anoxic sediments, underlining its importance as carbon and nitrogen sources for sedimentary microorganisms. We studied chitin degradation in littoral sediment of Lake Constance, Central Europe's third largest lake. Turnover of the chitin analog methyl-umbelliferyl-N,N-diacetylchitobioside (MUF-DC) was highest in the upper oxic sediment layer, with 5.4?nmol MUF-DC h-1 (g sediment [dry weight])-1 In the underlying anoxic sediment layers, chitin hydrolysis decreased with depth from 1.1 to 0.08?nmol MUF-DC h-1 (g sediment [dry weight])-1 Bacteria involved in chitin degradation were identified by 16S rRNA (gene) amplicon sequencing of anoxic microcosms incubated in the presence of chitin compared to microcosms amended either with N-acetylglucosamine as the monomer of chitin or no substrate. Chitin degradation was driven by a succession of bacteria responding specifically to chitin only. The early phase (0 to 9?days) was dominated by Chitinivibrio spp. (Fibrobacteres). The intermediate phase (9 to 21?days) was characterized by a higher diversity of chitin responders, including, besides Chitinivibrio spp., also members of the phyla Bacteroidetes, Proteobacteria, Spirochaetes, and Chloroflexi In the late phase (21 to 43?days), the Chitinivibrio populations broke down with a parallel strong increase of Ruminiclostridium spp. (formerly Clostridium cluster III, Firmicutes), which became the dominating chitin responders. Our study provides quantitative insights into anaerobic chitin degradation in lake sediments and linked this to a model of microbial succession associated with this activity.IMPORTANCE Chitin is the most abundant biopolymer in aquatic environments, with a direct impact on the carbon and nitrogen cycles. Despite its massive production as a structural element of crustaceans, insects, or algae, it does not accumulate in sediments. Little is known about its turnover in predominantly anoxic freshwater sediments and the responsible microorganisms. We proved that chitin is readily degraded under anoxic conditions and linked this to a succession of the members of the responsible microbial community over a 43-day period. While Fibrobacteres and Firmicutes members were driving the early and late phases of chitin degradation, respectively, a more diverse community was involved in chitin degradation in the intermediate phase. Entirely different microorganisms responded toward the chitin monomer N-acetylglucosamine, which underscores that soluble monomers are poor and misleading substrates to study polymer-utilizing microorganisms. Our study provides quantitative insights into the microbial ecology driving anaerobic chitin degradation in freshwater sediments.

Project description:BackgroundCellulose is the most abundant organic polymer mainly produced by plants in nature. It is insoluble and highly resistant to enzymatic hydrolysis. Cellulolytic microorganisms that are capable of producing a battery of related enzymes play an important role in recycling cellulose-rich plant biomass. Effective cellulose degradation by multiple synergic microorganisms has been observed within a defined microbial consortium in the lab culture. Metagenomic analysis may enable us to understand how microbes cooperate in cellulose degradation in a more complex microbial free-living ecosystem in nature.ResultsHere we investigated a typical cellulose-rich and alkaline niche where constituent microbes survive through inter-genera cooperation in cellulose utilization. The niche has been generated in an ancient paper-making plant, which has served as an isolated habitat for over 7 centuries. Combined amplicon-based sequencing of 16S rRNA genes and metagenomic sequencing, our analyses showed a microbial composition with 6 dominant genera including Cloacibacterium, Paludibacter, Exiguobacterium, Acetivibrio, Tolumonas, and Clostridium in this cellulose-rich niche; the composition is distinct from other cellulose-rich niches including a modern paper mill, bamboo soil, wild giant panda guts, and termite hindguts. In total, 11,676 genes of 96 glucoside hydrolase (GH) families, as well as 1,744 genes of carbohydrate transporters were identified, and modeling analysis of two representative genes suggested that these glucoside hydrolases likely evolved to adapt to alkaline environments. Further reconstruction of the microbial draft genomes by binning the assembled contigs predicted a mutualistic interaction between the dominant microbes regarding the cellulolytic process in the niche, with Paludibacter and Clostridium acting as helpers that produce endoglucanases, and Cloacibacterium, Exiguobacterium, Acetivibrio, and Tolumonas being beneficiaries that cross-feed on the cellodextrins by oligosaccharide uptake.ConclusionThe analysis of the key genes involved in cellulose degradation and reconstruction of the microbial draft genomes by binning the assembled contigs predicted a mutualistic interaction based on public goods regarding the cellulolytic process in the niche, suggesting that in the studied microbial consortium, free-living bacteria likely survive on each other by acquisition and exchange of metabolites. Knowledge gained from this study will facilitate the design of complex microbial communities with a better performance in industrial bioprocesses.

Dataset Information

Solid-, solution-, and gas-state NMR monitoring of ¹³C-cellulose degradation in an anaerobic microbial ecosystem.

Publications

Solid-, solution-, and gas-state NMR monitoring of ¹³C-cellulose degradation in an anaerobic microbial ecosystem.

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