Physiological interactions between a mesophilic cellulolytic Clostridium and a non-cellulolytic bacterium

Cavedon, Katherine; Canale-Parola, E.

doi:10.1111/j.1574-6941.1991.tb01758.x

Cited by 8 publications

(8 citation statements)

References 25 publications

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“…This study is a ®rst step providing grounding for further investigation of the physiology and molecular biology of regulation of sporulation in C. cellulolyticum. Furthermore, understanding of the phenomena which allow favorable conditions for spore germination and thus cellulose degradation in the natural ecological niche requires that data from monospecies laboratory cultures must be extrapolated to microbiota where, as observed with the rumen micro¯ora, complex interactions between cellulolytic and noncellulolytic microorganisms and environmental conditions take place [7,9,32].…”

Section: Discussionmentioning

confidence: 99%

Sporulation of Clostridium cellulolyticum while Grown in Cellulose-Batch and Cellulose-Fed Continuous Cultures on a Mineral-Salt Based Medium

Desvaux

Petitdemange

2002

Microbial Ecology

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Clostridium cellulolyticum sporulation was investigated during growth on cellulose fibers in a mineral-salt based medium which corresponds to conditions linked to its natural ecological niche. At steady state of the continuous cultures under limitation and with an excess of cellulose and/or ammonium, bacterial cells mainly sporulated at low dilution rates (D), at least 10% sporulation being observed at the lowest D tested. Increasing the cellulose concentration in the feed-medium reservoir increased the percentage of spores in the bioreactor. It appeared that the remaining undigested cellulose could serve as an exogenous carbon source supply at a continuous but limited rate throughout the sporulation process. In addition to the proportion of carbon and nitrogen, the influence of the environmental pH on spore formation was studied. In cellulose-fed continuous cultures at a constant D and a pH decreasing from 7.2 to 6.4, the percentage of spores increased to 14% at the lowest pH tested. When C. cellulolyticum was grown in batch culture, the level of sporulation was dramatically higher in unregulated-pH fermentation compared to pH-controlled growth conditions at pH 7.2 since in the former it reached 45% within 5 days of cultivation. It then appeared that a low specific growth rate and a low environmental pH in the presence of an insoluble carbon substrate were the major factors inducing sporulation in C. cellulolyticum. Furthermore, since the spores adhere to the carbon substrate (the cellulose) the bacteria gain advantages when the environment allows germination thanks to the recovery of suitable growth conditions. By allowing the maintenance and the integrity of the bacteria in the microbiota, spore formation could then explain the successful survival of C. cellulolyticum in cellulosic anaerobic habitats where low environmental pH conditions are often found.

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Section: Discussionmentioning

confidence: 99%

Sporulation of Clostridium cellulolyticum while Grown in Cellulose-Batch and Cellulose-Fed Continuous Cultures on a Mineral-Salt Based Medium

Desvaux

Petitdemange

2002

Microbial Ecology

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“…On the other hand, the utilisation of soluble cellodextrins has received little attention, mainly for a reason of cost and feasibility. The understanding of cellulose degradation in the environment requires that data from monospecies laboratory cultures must be extrapolated to microbiota where, as observed with the rumen microflora, complex interactions between cellulolytic and non‐cellulolytic microorganisms and environmental conditions take place [29,193–196]. In this context, the feeding of non‐cellulolytic satellite bacteria either with cellodextrins synthesised de novo from cellulolytic bacteria hydrolysing cellulose via primarily cell‐associated enzymes, or with cellodextrins lost by diffusion from the cellulolytic site, or both is an intriguing issue [29].…”

Section: Concluding Remarks and Perspectivesmentioning

confidence: 99%

Clostridium cellulolyticum: model organism of mesophilic cellulolytic clostridia

Desvaux¹

2005

FEMS Microbiol Rev

182

102

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Clostridium cellulolyticum ATCC 35319 is a non-ruminal mesophilic cellulolytic bacterium originally isolated from decayed grass. As with most truly cellulolytic clostridia, C. cellulolyticum possesses an extracellular multi-enzymatic complex, the cellulosome. The catalytic components of the cellulosome release soluble cello-oligosaccharides from cellulose providing the primary carbon substrates to support bacterial growth. As most cellulolytic bacteria, C. cellulolyticum was initially characterised by limited carbon consumption and subsequent limited growth in comparison to other saccharolytic clostridia. The first metabolic studies performed in batch cultures suggested nutrient(s) limitation and/or by-product(s) inhibition as the reasons for this limited growth. In most recent investigations using chemostat cultures, metabolic flux analysis suggests a self-intoxication of bacterial metabolism resulting from an inefficiently regulated carbon flow. The investigation of C. cellulolyticum physiology with cellobiose, as a model of soluble cellodextrin, and with pure cellulose, as a carbon source more closely related to lignocellulosic compounds, strengthen the idea of a bacterium particularly well adapted, and even restricted, to a cellulolytic lifestyle. The metabolic flux analysis from continuous cultures revealed that (i) in comparison to cellobiose, the cellulose hydrolysis by the cellulosome introduces an extra regulation of entering carbon flow resulting in globally lower metabolic fluxes on cellulose than on cellobiose, (ii) the glucose 1-phosphate/glucose 6-phosphate branch point controls the carbon flow directed towards glycolysis and dissipates carbon excess towards the formation of cellodextrins, glycogen and exopolysaccharides, (iii) the pyruvate/acetyl-CoA metabolic node is essential to the regulation of electronic and energetic fluxes. This in-depth analysis of C. cellulolyticum metabolism has permitted the first attempt to engineer metabolically a cellulolytic microorganism.

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“…The beneficiaries of community metabolism should be expected to shed energetically costly traits, resulting in adaptive gene loss and evolution of metabolic dependency [20]. For example, noncellulolytic bacteria can complement the metabolic functions of cellulolytic bacteria in vitro, through catabolic reactions [21,22], vitamin biosynthesis [23], amino acid biosynthesis [24], or biosynthesis of other essential metabolites [25]. Such metabolic dependency can occur through specific, tightly coupled interactions, such as those of syntrophic partners, but it can also be loosely coupled and nonspecific, such as when cells obtain metabolites or other nutrients from extracellular pools replenished by mortality of community members [26,27].…”

Section: Introductionmentioning

confidence: 99%

Competitive exclusion and metabolic dependency among microorganisms structure the cellulose economy of agricultural soil

Wilhelm¹,

Pepe-Ranney

Weisenhorn

et al. 2020

Preprint

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Many cellulolytic microorganisms degrade cellulose through extracellular processes that yield free intermediates which promote interactions with non-cellulolytic organisms. We hypothesize that these interactions determine the ecological and physiological traits that govern the fate of cellulosic carbon (C) in soil. We evaluated the genomic potential of soil microorganisms that access C from 13 C-labeled cellulose. We used metagenomic-SIP and metaproteomics to evaluate whether cellulolytic and non-cellulolytic microbes that access 13 C from cellulose encode traits indicative of metabolic dependency or competitive exclusion. The most highly 13 C-enriched taxa were cellulolytic Cellvibrio ( Gammaproteobacteria ) and Chaetomium ( Ascomycota ), which exhibited a strategy of self-sufficiency (prototrophy), rapid growth, and competitive exclusion via antibiotic production. These ruderal taxa were common indicators of soil disturbance in agroecosystems, such as tillage and fertilization. Auxotrophy was more prevalent in cellulolytic Actinobacteria than in cellulolytic Proteobacteria , demonstrating differences in dependency among cellulose degraders. Non-cellulolytic taxa that accessed 13 C from cellulose ( Planctomycetales , Verrucomicrobia and Vampirovibrionales ) were highly dependent, as indicated by patterns of auxotrophy and 13 C-labeling (i.e. partial labelling or labeling at later-stages). Major 13 C-labeled cellulolytic microbes ( e.g. Sorangium, Actinomycetales, Rhizobiales and Caulobacteraceae ) possessed adaptations for surface colonization ( e.g. gliding motility, hyphae, attachment structures) signifying the importance of surface ecology in decomposition. These results suggest that access to cellulose was accompanied by ecological trade-offs characterized by differing degrees of metabolic dependency and competitive exclusion. These trade-offs likely influence microbial growth dynamics on particulate organic carbon and reveal that the fate of carbon is governed by a complex economy within the microbial community.

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Physiological interactions between a mesophilic cellulolytic Clostridium and a non-cellulolytic bacterium

Cited by 8 publications

References 25 publications

Sporulation of Clostridium cellulolyticum while Grown in Cellulose-Batch and Cellulose-Fed Continuous Cultures on a Mineral-Salt Based Medium

Sporulation of Clostridium cellulolyticum while Grown in Cellulose-Batch and Cellulose-Fed Continuous Cultures on a Mineral-Salt Based Medium

Clostridium cellulolyticum: model organism of mesophilic cellulolytic clostridia

Competitive exclusion and metabolic dependency among microorganisms structure the cellulose economy of agricultural soil

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