A Multitask ATPase Serving Different ABC-Type Sugar Importers in
            <i>Bacillus subtilis</i>

Ferreira, Mário J.; Sá‐Nogueira, Isabel

doi:10.1128/jb.00832-10

Cited by 55 publications

(71 citation statements)

References 34 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…This phenomenon has often been suspected to occur in carbohydrate transport in a wide range of Gram-positive organisms, although rarely investigated (8,9). Previously, data in both Streptomyces and Bacillus subtilis have shown growth or transport defects for ATPase mutants on disparate substrates, suggesting sharing of the ATPase (10,34,35). In addition to growth, we show directly that MsmK is required for transport and that MsmK has ATP hydrolytic activity.…”

Section: Discussionmentioning

confidence: 68%

Identification of an ATPase, MsmK, Which Energizes Multiple Carbohydrate ABC Transporters in Streptococcus pneumoniae

et al. 2011

View full text Add to dashboard Cite

Streptococcus pneumoniae is the leading cause of community-acquired pneumonia and results in over 1 million deaths each year worldwide. Asymptomatic colonization of the airway precedes disease, and acquisition of carbohydrates from the host environment is necessary for bacterial survival. We previously demonstrated that S. pneumoniae cleaves sialic acid from human glycoconjugates to be used as a carbohydrate source. The satABC genes are required for growth and import of sialic acid. The satABC genes are predicted to encode components of an ABC transporter but not the ATPases essential to energize transport. As this subunit is essential, an ATPase must be encoded elsewhere in the genome. We identified msmK as a candidate based on similarity to other known carbohydrate ATPases. Recombinant MsmK hydrolyzed ATP, revealing that MsmK is an ATPase. An msmK mutant was reduced in growth on and transport of sialic acid, demonstrating that MsmK is the ATPase energizing the sialic acid transporter. In addition to satABC, S. pneumoniae contains five other loci that are predicted to encode CUT1 family carbohydrate ABC transporter components; each of these lacks a predicted ATPase. Data indicate that msmK is also required for growth on raffinose and maltotetraose, which are the substrates of two other characterized carbohydrate ABC transporters. Furthermore, an msmK mutant was reduced in airway colonization. Together, these data imply that in vivo, MsmK energizes multiple carbohydrate transporters in S. pneumoniae. This is the first demonstration of a shared ATPase in a pathogenic bacterium.

show abstract

Section: Discussionmentioning

confidence: 68%

Identification of an ATPase, MsmK, Which Energizes Multiple Carbohydrate ABC Transporters in Streptococcus pneumoniae

et al. 2011

View full text Add to dashboard Cite

show abstract

“…The resulting products, arabinose and arabinose oligomers, are transported by specific transport systems, AraE, a proton symporter, and AraNPQ, an ABCtype transporter for arabino-oligosaccharides, and presumably an additional, unidentified transporter (22). Inside the cell, arabino oligomers are further hydrolyzed by the concerted action of the two ␣-L-arabinofuranosidases (35).…”

Section: Discussionmentioning

confidence: 99%

“…The ABC transport systems, XynEF and BxlEFG, from G. stearothermophilus (68) and Streptomyces thermoviolaceus (72), respectively, were demonstrated to bind xylo-oligosaccharides. The ABC transporter, AraNPQ, from Bacillus subtilis is involved in the uptake of arabino-oligosaccharides (22). In the anaerobic bacterium Clostridium thermocellum, five sugar ABC transporters were characterized for cellodextrins (CbpB to -D), cellotriose (CbpA), and laminaribiose (Lbp) (52).…”

mentioning

confidence: 99%

The l -Arabinan Utilization System of Geobacillus stearothermophilus

et al. 2011

View full text Add to dashboard Cite

Geobacillus stearothermophilus T-6 is a thermophilic soil bacterium that has a 38-kb gene cluster for the utilization of arabinan, a branched polysaccharide that is part of the plant cell wall. The bacterium encodes a unique three-component regulatory system (araPST) that includes a sugar-binding lipoprotein (AraP), a histidine sensor kinase (AraS), and a response regulator (AraT) and lies adjacent to an ATP-binding cassette (ABC) arabinose transport system (araEGH). The lipoprotein (AraP) specifically bound arabinose, and gel mobility shift experiments showed that the response regulator, AraT, binds to a 139-bp fragment corresponding to the araE promoter region. Taken together, the results showed that the araPST system appeared to sense extracellular arabinose and to activate a specific ABC transporter for arabinose (AraEGH). The promoter regions of the arabinan utilization genes contain a 14-bp inverted repeat motif resembling an operator site for the arabinose repressor, AraR. AraR was found to bind specifically to these sequences, and binding was efficiently prevented in the presence of arabinose, suggesting that arabinose is the molecular inducer of the arabinan utilization system. The expression of the arabinan utilization genes was reduced in the presence of glucose, indicating that regulation is also mediated via a catabolic repression mechanism. The cluster also encodes a second putative ABC sugar transporter (AbnEFJ) whose sugar-binding lipoprotein (AbnE) was shown to interact specifically with linear and branched arabino-oligosaccharides. The final degradation of the arabino-oligosaccharides is likely carried out by intracellular enzymes, including two ␣-L-arabinofuranosidases (AbfA and AbfB), a ␤-L-arabinopyranosidase (Abp), and an arabinanase (AbnB), all of which are encoded in the 38-kb cluster.The natural degradation of biomass from plants is a key step in the carbon cycle (53,69,79). This process is carried out mainly by microorganisms that can be found either free or as part of the digestive system in higher animals (76). The three main polysaccharides in the plant cell wall are cellulose, hemicellulose, and pectin, which are rigidified by lignin, a heterogeneous aromatic polymer (28, 60). Pectin is a complex polysaccharide and may account for up to 30% of the dry weight of the plant cell wall (46). Arabinan is a pectic polysaccharide consisting of a backbone of ␣-1,5-linked L-arabinofuranosyl units, which are further decorated mainly with ␣-1,2-and ␣-1,3-linked arabinofuranosides (46).Three general strategies are taken by the microbial world for plant cell wall degradation and can be described as follows. Anaerobic bacteria, such as Clostridium spp., have evolved unique multienzyme complexes, named cellulosomes, that integrate many cellulolytic and hemicellulolytic enzymes and mediate both the attachment of the cell to the crystalline polymer and its controlled hydrolysis (9,16,23,65). Aerobic fungi, such as Trichoderma and Aspergillus, secrete a large variety of free cellulases, hemicellulases...

show abstract

“…L-Arabinose can also be obtained through hydrolysis of arabinosides. In some bacteria, such as Bacillus subtilis and Geobacillus stearothermophilus, arabinosides are transported into the cell and further degraded into L-arabinose by intracellular enzymes, including ␣-arabinofuranosidase AbfA and arabinosidase Arb43 (glycoside hydrolase family 43) (8,36). L-Arabinose is consecutively converted to L-ribulose, L-ribulose-5-phosphate, and xylulose-5-phosphate by the action of L-arabinose isomerase AraA, L-ribulokinase AraB, and L-ribulose-5-phosphate 4-epimerase AraD, respectively, in many bacteria (e.g., B. subtilis).…”

mentioning

confidence: 99%

Ribulokinase and Transcriptional Regulation of Arabinose Metabolism in Clostridium acetobutylicum

Zhang

Leyn

et al. 2011

Journal of Bacteriology

View full text Add to dashboard Cite

The transcription factor AraR controls utilization of L-arabinose in Bacillus subtilis. In this study, we combined a comparative genomic reconstruction of AraR regulons in nine Clostridium species with detailed experimental characterization of AraRmediated regulation in Clostridium acetobutylicum. Based on the reconstructed AraR regulons, a novel ribulokinase, AraK, present in all analyzed Clostridium species was identified, which was a nonorthologous replacement of previously characterized ribulokinases. The predicted function of the araK gene was confirmed by inactivation of the araK gene in C. acetobutylicum and biochemical assays using purified recombinant AraK. In addition to the genes involved in arabinose utilization and arabinoside degradation, extension of the AraR regulon to the pentose phosphate pathway genes in several Clostridium species was revealed. The predicted AraR-binding sites in the C. acetobutylicum genome and the negative effect of L-arabinose on DNA-regulator complex formation were verified by in vitro binding assays. The predicted AraR-controlled genes in C. acetobutylicum were experimentally validated by testing gene expression patterns in both wild-type and araR-inactivated mutant strains during growth in the absence or presence of L-arabinose.

show abstract

A Multitask ATPase Serving Different ABC-Type Sugar Importers in Bacillus subtilis

Cited by 55 publications

References 34 publications

Identification of an ATPase, MsmK, Which Energizes Multiple Carbohydrate ABC Transporters in Streptococcus pneumoniae

Identification of an ATPase, MsmK, Which Energizes Multiple Carbohydrate ABC Transporters in Streptococcus pneumoniae

The l -Arabinan Utilization System of Geobacillus stearothermophilus

Ribulokinase and Transcriptional Regulation of Arabinose Metabolism in Clostridium acetobutylicum

Contact Info

Product

Resources

About