Handling Several Sugars at a Time: a Case Study of Xyloglucan Utilization by
            <i>Ruminiclostridium cellulolyticum</i>

Kampik, Clara; Liu, Nian; Mroueh, Mohamed; Franche, Nathalie; Borne, Romain; Denis, Yann; Gagnot, Séverine; Tardif, Chantal; Pagès, Sandrine; Perret, Stéphanie; Vita, Nicolas; Philip, Pascale de; Fierobe, Henri‐Pierre

doi:10.1128/mbio.02206-21

Cited by 9 publications

(8 citation statements)

References 57 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…R. cellulolyticum secretes cellulosomes and is a primary degrader able to grow on cellulose, arabinoxylan, and xyloglucan [ 20 – 22 , 27 , 32 , 41 ]. When assayed on xyloglucan, the purified cellulosomes generate large xyloglucan dextrins containing up to 9 monosaccharides as the end product.…”

Section: Discussionmentioning

confidence: 99%

“…As R. cellulolyticum was shown to grow on arabinose and xylose, it is highly likely that elemental monosaccharides released by cellulosomes (and other putative xylanases) during growth on arabinoxylan are imported by other transporters (Fig. 7 ), [ 41 ]. It is remarkable that none of the reported xylanolytic bacteria with a XOS/AXOS import system produce cellulosomes [ 8 – 12 , 17 ].…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Selfish uptake versus extracellular arabinoxylan degradation in the primary degrader Ruminiclostridium cellulolyticum, a new string to its bow

Liu

Gagnot

Denis

et al. 2022

Biotechnol Biofuels

Self Cite

View full text Add to dashboard Cite

Background Primary degraders of polysaccharides play a key role in anaerobic biotopes, where plant cell wall accumulates, providing extracellular enzymes to release fermentable carbohydrates to fuel themselves and other non-degrader species. Ruminiclostridium cellulolyticum is a model primary degrader growing amongst others on arabinoxylan. It produces large multi-enzymatic complexes called cellulosomes, which efficiently deconstruct arabinoxylan into fermentable monosaccharides. Results Complete extracellular arabinoxylan degradation was long thought to be required to fuel the bacterium during this plant cell wall deconstruction stage. We discovered and characterized a second system of “arabinoxylan” degradation in R. cellulolyticum, which challenged this paradigm. This “selfish” system is composed of an ABC transporter dedicated to the import of large and possibly acetylated arabinoxylodextrins, and a set of four glycoside hydrolases and two esterases. These enzymes show complementary action modes on arabinoxylo-dextrins. Two α-L-arabinofuranosidases target the diverse arabinosyl side chains, and two exo-xylanases target the xylo-oligosaccharides backbone either at the reducing or the non-reducing end. Together, with the help of two different esterases removing acetyl decorations, they achieve the depolymerization of arabinoxylo-dextrins in arabinose, xylose and xylobiose. The in vivo study showed that this new system is strongly beneficial for the fitness of the bacterium when grown on arabinoxylan, leading to the conclusion that a part of arabinoxylan degradation is achieved in the cytosol, even if monosaccharides are efficiently provided by the cellulosomes in the extracellular space. These results shed new light on the strategies used by anaerobic primary degrader bacteria to metabolize highly decorated arabinoxylan in competitive environments. Conclusion The primary degrader model Ruminiclostridium cellulolyticum has developed a “selfish” strategy consisting of importing into the bacterium, large arabinoxylan–dextrin fractions released from a partial extracellular deconstruction of arabinoxylan, thus complementing its efficient extracellular arabinoxylan degradation system. Genetic studies suggest that this system is important to support fitness and survival in a competitive biotope. These results provide a better understanding of arabinoxylan catabolism in the primary degrader, with biotechnological application for synthetic microbial community engineering for the production of commodity chemicals from lignocellulosic biomass.

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Selfish uptake versus extracellular arabinoxylan degradation in the primary degrader Ruminiclostridium cellulolyticum, a new string to its bow

Liu

Gagnot

Denis

et al. 2022

Biotechnol Biofuels

Self Cite

View full text Add to dashboard Cite

show abstract

“…Anaerostipes is a butyrate producer, which could convert lactate and acetic acid and sugar to butyrate ( 53 – 56 ). Ruminiclostridium is an anaerobic Gram-positive cellulolytic bacterium that produces a variety of carbohydrate-active enzymes (CAZymes) and catabolizes xyloglucan into glucose, xylose, galactose, and cellobiose ( 57 ). It includes extracellular multienzyme complexes known as fibrosomes with different specificities to enhance the degradation of cellulosic biomass ( 58 ).…”

Section: Discussionmentioning

confidence: 99%

Longitudinal Study of the Effects of Flammulina velutipes Stipe Wastes on the Cecal Microbiota of Laying Hens

et al. 2023

View full text Add to dashboard Cite

show abstract

“…6, panel A). Methane accumulation in the presence of bacterial antibiotics and favorability of XG over all other substrates tested would suggest this mode, however, the M. nevadense genome does not indicate any genes typically associated with XG breakdown, including glycoside hydrolases (Kampik et al ., 2021), rendering direct XG metabolism unlikely.…”

Section: Discussionmentioning

confidence: 99%

Mcr-dependent methanogenesis inArchaeoglobaceaeenriched from a terrestrial hot spring

Buessecker

Chadwick

Quan

et al. 2022

Preprint

View full text Add to dashboard Cite

The preeminent source of biological methane on Earth is methyl coenzyme M reductase (Mcr)-dependent archaeal methanogenesis. A growing body of evidence suggests a diversity of archaea possess Mcr, however, experimental validation of hypothesized methane metabolisms has been missing. Here, we provide evidence of a functional Mcr-based methanogenesis pathway in a novel member of the familyArchaeoglobaceae, designatedMethanoproducendum nevadense, which we enriched from a terrestrial hot spring on the polysaccharide xyloglucan. Our incubation assays demonstrate methane production that is highly sensitive to the Mcr-inhibitor bromoethanesulfonate, stimulated by xyloglucan and xyloglucan-derived sugars, concomitant with the consumption of molecular hydrogen, and causing a deuterium fractionation in methane characteristic of hydrogenotrophic and methylotrophic methanogens. Combined with the recovery and analysis of a high-qualityM. nevadensemetagenome-assembled genome encoding a divergent Mcr and diverse potential electron and carbon transfer pathways, our observations suggest methanogenesis inM. nevadenseoccurs via Mcr and is fueled by the consumption of cross-fed byproducts of xyloglucan fermentation mediated by other community members. Phylogenetic analysis shows close affiliation of theM. nevadenseMcr with those from Korarchaeota, Nezhaarchaeota, Verstraetearchaeota, and otherArchaeoglobalesthat are divergent from well-characterized Mcrs. We propose these archaea likely also use functional Mcr complexes to generate methane on the basis of our experimental validation inM. nevadense. Although our stable isotope approach reveals that microbial methanogenesis contributes only a small proportion of the overall methane abundance in the native habitat, divergent Mcr-encoding archaea may be underestimated sources of biological methane in terrestrial and marine hydrothermal environments.

show abstract

Handling Several Sugars at a Time: a Case Study of Xyloglucan Utilization by Ruminiclostridium cellulolyticum

Cited by 9 publications

References 57 publications

Selfish uptake versus extracellular arabinoxylan degradation in the primary degrader Ruminiclostridium cellulolyticum, a new string to its bow

Selfish uptake versus extracellular arabinoxylan degradation in the primary degrader Ruminiclostridium cellulolyticum, a new string to its bow

Longitudinal Study of the Effects of Flammulina velutipes Stipe Wastes on the Cecal Microbiota of Laying Hens

Mcr-dependent methanogenesis inArchaeoglobaceaeenriched from a terrestrial hot spring

Contact Info

Product

Resources

About