Mathematical modeling of hydrolysate diffusion and utilization in cellulolytic biofilms of the extreme thermophile Caldicellulosiruptor obsidiansis

Wang, Zhiwu; Hamilton-Brehm, Scott D.; Lochner, Adriane; Elkins, James G.; Morrell‐Falvey, Jennifer L.

doi:10.1016/j.biortech.2010.10.104

Cited by 16 publications

(16 citation statements)

References 22 publications

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“…In contrast, low soluble substrate availability supports only thin biofilms because mass diffusion is no longer a rate-limiting step, and thus dense and uniform biofilms are formed (Park et al 1998). Our previous work on the modeling of hydrolysate diffusion and utilization in cellulose feeding biofilms are consistent with this inference (Wang et al 2011). These modeling studies predicted that the hydrolysate concentration profile is quite uniform throughout the cellulolytic biofilm and that the growth of the biofilm is limited by hydrolysate utilization rates, rather than hydrolysate diffusion rates (Wang et al 2011).…”

Section: Discussionsupporting

confidence: 80%

“…After 72 h incubation, the cellulose chad displayed significant degradation with irregular holes being visible (Figure 4c) in comparison with the new chad at the 0 h time point (Figure 4b). Our previous work indicated that a C. obsidiansis biofilm growing on cellulose generates more hydrolysate than it can utilize in order to establish an intra-biofilm substrate concentration high enough to support growth (Wang et al 2011). The excess hydrolysate diffuses through the biofilm and is released into the bulk liquid where it can support planktonic cell growth (Wang et al 2011).…”

Section: Resultsmentioning

confidence: 99%

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Spatial and temporal dynamics of cellulose degradation and biofilm formation by Caldicellulosiruptor obsidiansis and Clostridium thermocellum

et al. 2011

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Cellulose degradation is one of the major bottlenecks of a consolidated bioprocess that employs cellulolytic bacterial cells as catalysts to produce biofuels from cellulosic biomass. In this study, we investigated the spatial and temporal dynamics of cellulose degradation by Caldicellulosiruptfor obsidiansis, which does not produce cellulosomes, and Clostridium thermocellum, which does produce cellulosomes. Results showed that the degradation of either regenerated or natural cellulose was synchronized with biofilm formation, a process characterized by the formation and fusion of numerous crater-like depressions on the cellulose surface. In addition, the dynamics of biofilm formation were similar in both bacteria, regardless of cellulosome production. Only the areas of cellulose surface colonized by microbes were significantly degraded, highlighting the essential role of the cellulolytic biofilm in cellulose utilization. After initial attachment, the microbial biofilm structure remained thin, uniform and dense throughout the experiment. A cellular automaton model, constructed under the assumption that the attached cells divide and produce daughter cells that contribute to the hydrolysis of the adjacent cellulose, can largely simulate the observed process of biofilm formation and cellulose degradation. This study presents a model, based on direct observation, correlating cellulolytic biofilm formation with cellulose degradation.

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Section: Discussionsupporting

confidence: 80%

Section: Resultsmentioning

confidence: 99%

Spatial and temporal dynamics of cellulose degradation and biofilm formation by Caldicellulosiruptor obsidiansis and Clostridium thermocellum

et al. 2011

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“…5, I and II); these enzymes are responsible for the production and conversion of cyclic di-GMP and are known to be involved in regulating the switch from planktonic growth to biofilm formation (44). In fact, C. saccharolyticus generates elevated intracellular levels of cyclic di-GMP during biofilm formation (45), and another Caldicellulosiruptor species, C. obsidiansis, forms cellulose-degrading biofilms (46,47). The precise relationship between the DGC/PDE and the Che-type system has not been studied for Caldicellulosiruptor.…”

Section: Resultsmentioning

confidence: 99%

Comparative Analysis of Extremely Thermophilic Caldicellulosiruptor Species Reveals Common and Unique Cellular Strategies for Plant Biomass Utilization

Zurawski

Conway

Lee

et al. 2015

Appl Environ Microbiol

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c Microbiological, genomic and transcriptomic analyses were used to examine three species from the bacterial genus Caldicellulosiruptor with respect to their capacity to convert the carbohydrate content of lignocellulosic biomass at 70°C to simple sugars, acetate, lactate, CO 2 , and H 2 . Caldicellulosiruptor bescii, C. kronotskyensis, and C. saccharolyticus solubilized 38%, 36%, and 29% (by weight) of unpretreated switchgrass (Panicum virgatum) (5 g/liter), respectively, which was about half of the amount of crystalline cellulose (Avicel; 5 g/liter) that was solubilized under the same conditions. The lower yields with C. saccharolyticus, not appreciably greater than the thermal control for switchgrass, were unexpected, given that its genome encodes the same glycoside hydrolase 9 (GH9)-GH48 multidomain cellulase (CelA) found in the other two species. However, the genome of C. saccharolyticus lacks two other cellulases with GH48 domains, which could be responsible for its lower levels of solubilization. Transcriptomes for growth of each species comparing cellulose to switchgrass showed that many carbohydrate ABC transporters and multidomain extracellular glycoside hydrolases were differentially regulated, reflecting the heterogeneity of lignocellulose. However, significant differences in transcription levels for conserved genes among the three species were noted, indicating unexpectedly diverse regulatory strategies for deconstruction for these closely related bacteria. Genes encoding the Che-type chemotaxis system and flagellum biosynthesis were upregulated in C. kronotskyensis and C. bescii during growth on cellulose, implicating motility in substrate utilization. The results here show that capacity for plant biomass deconstruction varies across Caldicellulosiruptor species and depends in a complex way on GH genome inventory, substrate composition, and gene regulation. T he genusCaldicellulosiruptor is comprised of Gram-positive, anaerobic bacteria that ferment a variety of simple and complex carbohydrates to primarily H 2 , CO 2 , acetate, and lactate at temperatures at or above 70°C (1). To date, Caldicellulosiruptor species have been isolated globally from terrestrial hot springs and thermal features in locations including the United States (C. owensensis [2,3] and C. obsidiansis [4,5]), Russia (C. bescii [6,7]), C. kronotskyensis [2,8], and C. hydrothermalis [2,8]), New Zealand (C. saccharolyticus [9-11]), and Iceland (C. kristjanssonii [2,12] and C. lactoaceticus [2,13]). Characteristic of Caldicellulosiruptor species are multidomain extracellular and S-layer-associated glycoside hydrolases (GHs) that mediate the microbial conversion of complex carbohydrates (14-16). Sequenced genomes for Caldicellulosiruptor species (2, 4, 6, 10) indicate that some, but not all, encode GH48-containing enzymes (17), and these appear to be essential for crystalline cellulose degradation (18). The cellulolytic Caldicellulosiruptor species also utilize novel binding proteins (ta pirins) to adhere to plant biomass (19). Sever...

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“…Mathematical modelling predicted that the establishment of a multilayered biofilm requires that the fraction of the cell population that accesses the surface particle produces more substrates than it actually consumes. This overproduction of solubilized substrate feeds the biofilm cell subpopulation at a distance from the particle surface and results in a substrate leakage outside the biofilm (Vetter et al ., ; Wang et al ., ). Hydrolysate leakage was indeed observed in biofilms during cellulose degradation, supporting the prediction of the model (Lu et al ., ; Wang et al ., ).…”

Section: Ecological and Social Aspects Of Biofilm Development On Partmentioning

confidence: 97%

Biofilm formation as a microbial strategy to assimilate particulate substrates

Sivadon

Barnier

Urios

et al. 2019

Environmental Microbiology Reports

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Summary In most ecosystems, a large part of the organic carbon is not solubilized in the water phase. Rather, it occurs as particles made of aggregated hydrophobic and/or polymeric natural or man‐made organic compounds. These particulate substrates are degraded by extracellular digestion/solubilization implemented by heterotrophic bacteria that form biofilms on them. Organic particle‐degrading biofilms are widespread and have been observed in aquatic and terrestrial natural ecosystems, in polluted and man‐driven environments and in the digestive tracts of animals. They have central ecological functions as they are major players in carbon recycling and pollution removal. The aim of this review is to highlight bacterial adhesion and biofilm formation as central mechanisms to exploit the nutritive potential of organic particles. It focuses on the mechanisms that allow access and assimilation of non‐dissolved organic carbon, and considers the advantage provided by biofilms for gaining a net benefit from feeding on particulate substrates. Cooperative and competitive interactions taking place in biofilms feeding on particulate substrates are also discussed.

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Mathematical modeling of hydrolysate diffusion and utilization in cellulolytic biofilms of the extreme thermophile Caldicellulosiruptor obsidiansis

Cited by 16 publications

References 22 publications

Spatial and temporal dynamics of cellulose degradation and biofilm formation by Caldicellulosiruptor obsidiansis and Clostridium thermocellum

Spatial and temporal dynamics of cellulose degradation and biofilm formation by Caldicellulosiruptor obsidiansis and Clostridium thermocellum

Comparative Analysis of Extremely Thermophilic Caldicellulosiruptor Species Reveals Common and Unique Cellular Strategies for Plant Biomass Utilization

Biofilm formation as a microbial strategy to assimilate particulate substrates

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