Duplication of Genes in an ATP-binding Cassette Transport System Increases Dynamic Range While Maintaining Ligand Specificity

Ghimire-Rijal, Sudipa; Lu, Xiaozhi; Myles, Dean A. A.; Cuneo, M.J.

doi:10.1074/jbc.m114.590992

Cited by 16 publications

(21 citation statements)

References 39 publications

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“…The transporter is composed of two TransMembrane Domains (TMD 2456 and TMD 2457 ) likely to form a heterodimer transmembrane channel, and a family-1 Solute Binding Protein (SBP 2458 ) exhibiting a very high affinity for xyloglucan oligosaccharides, especially for XXXG. To our knowledge, this is the first ABC-transporter ever described as a xyloglucan oligosaccharides importer, and the observed affinity of SBP 2458 for XXXG is among the highest ever reported for a solute binding protein and its glycosidic ligand 42 43 . The ABC-transporter, which was shown to be essential for growth on xyloglucan, would thus import voluminous oligosaccharides composed of up to 9 monosaccharides (in the case of XLLG) at a rather low energy cost.…”

Section: Discussionmentioning

confidence: 83%

Mechanisms involved in xyloglucan catabolism by the cellulosome-producing bacterium Ruminiclostridium cellulolyticum

Ravachol

Philip

Borne

et al. 2016

Sci Rep

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Xyloglucan, a ubiquitous highly branched plant polysaccharide, was found to be rapidly degraded and metabolized by the cellulosome-producing bacterium Ruminiclostridium cellulolyticum. Our study shows that at least four cellulosomal enzymes displaying either endo- or exoxyloglucanase activities, achieve the extracellular degradation of xyloglucan into 4-glucosyl backbone xyloglucan oligosaccharides. The released oligosaccharides (composed of up to 9 monosaccharides) are subsequently imported by a highly specific ATP-binding cassette transporter (ABC-transporter), the expression of the corresponding genes being strongly induced by xyloglucan. This polysaccharide also triggers the synthesis of cytoplasmic β-galactosidase, α-xylosidase, and β-glucosidase that act sequentially to convert the imported oligosaccharides into galactose, xylose, glucose and unexpectedly cellobiose. Thus R. cellulolyticum has developed an energy-saving strategy to metabolize this hemicellulosic polysaccharide that relies on the action of the extracellular cellulosomes, a highly specialized ABC-transporter, and cytoplasmic enzymes acting in a specific order. This strategy appears to be widespread among cellulosome-producing mesophilic bacteria which display highly similar gene clusters encoding the cytosolic enzymes and the ABC-transporter.

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Section: Discussionmentioning

confidence: 83%

Mechanisms involved in xyloglucan catabolism by the cellulosome-producing bacterium Ruminiclostridium cellulolyticum

Ravachol

Philip

Borne

et al. 2016

Sci Rep

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“…This solute receptor is either present as a diffusible protein in the periplasm of Gram-negative bacteria, tethered to the outer face of the cytoplasmic membrane via a lipid anchor in Gram-positive bacteria, covalently attached to the TMD, or anchored to the cytoplasmic membrane by a hydrophobic protein segment in Archaea (van der Heide and Poolman, 2002;Albers et al, 2004;Davidson et al, 2008;Eitinger et al, 2011;Gouridis et al, 2015;Nguyen and G€ otz, 2016). However, representatives are also known where multiple binding proteins possessing different affinities or substrate specificities function with the same core components of the ABC transporter (Higgins and Ames, 1981;Oh et al, 1994;Leonard et al, 1996;Chen et al, 2010;Ghimire-Rijal et al, 2014), or where multiple binding proteins are fused to the same TMD (van der Heide and Poolman, 2002;Gouridis et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

From substrate specificity to promiscuity: hybrid ABC transporters for osmoprotectants

Teichmann

Chen

Hoffmann

et al. 2017

Molecular Microbiology

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The ABC-transporters OpuB and OpuC from Bacillus subtilis function as osmoprotectant import systems. Their structural genes have most likely evolved through a duplication event but the two transporters are remarkably different in their substrate profile. OpuB possesses narrow substrate specificity, while OpuC is promiscuous. We assessed the functionality of hybrids between these two ABC-transporters by reciprocally exchanging the coding regions for the OpuBC and OpuCC substrate-binding proteins between the corresponding opuB and opuC operons. Substantiating the critical role of the binding protein in setting the substrate specificity of ABC transporters, OpuB::OpuCC turned into a promiscuous system, while OpuC::OpuBC now exhibited narrow substrate specificity. Both hybrid transporters possessed a high affinity for their substrates but the transport capacity of the OpuB::OpuCC system was moderate due to the synthesis of only low amounts of the xenogenetic OpuCC protein. Suppressor mutations causing single amino acid substitutions in the GbsR repressor controlling the choline to glycine betaine biosynthesis pathway greatly improved OpuB::OpuCC-mediated compatible solute import through transcriptional up-regulation of the hybrid opuB::opuCC operon. Collectively, we demonstrate for the first time that one can synthetically switch the substrate specificity of a given ABC transporter by combining its core components with a xenogenetic ligand-binding protein.

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“…Carbohydrate utilization by T. maritima has been examined by studying the substrate specificities and affinities of its carbohydrate transporters (Nanavati et al 2005(Nanavati et al , 2006Cuneo et al 2009;Boucher and Noll 2011;Ghimire-Rijal et al 2014) and their transcriptional regulation in response to growth on different saccharides (Frock et al 2012). Information about substrate specificities, enzymatic activities, and catalytic mechanisms of many of T. maritima's glycoside hydrolases are also available (Kleine and Liebl 2006;Comfort et al 2007;Arti et al 2012), which has been used, for instance, to engineer an ␣-galactosidase from T. maritima into an efficient ␣-galactosynthase (Cobucci-Ponzano et al 2011).…”

Section: The Thermotogaementioning

confidence: 99%

Insights into thermoadaptation and the evolution of mesophily from the bacterial phylum Thermotogae

2015

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Thermophiles are extremophiles that grow optimally at temperatures >45°C. To survive and maintain function of their biological molecules, they have a suite of characteristics not found in organisms that grow at moderate temperature (mesophiles). At the cellular level, thermophiles have mechanisms for maintaining their membranes, nucleic acids, and other cellular structures. At the protein level, each of their proteins remains stable and retains activity at temperatures that would denature their mesophilic homologs. Conversely, cellular structures and proteins from thermophiles may not function optimally at moderate temperatures. These differences between thermophiles and mesophiles presumably present a barrier for evolutionary transitioning between the 2 lifestyles. Therefore, studying closely related thermophiles and mesophiles can help us determine how such lifestyle transitions may happen. The bacterial phylum Thermotogae contains hyperthermophiles, thermophiles, mesophiles, and organisms with temperature ranges wide enough to span both thermophilic and mesophilic temperatures. Genomic, proteomic, and physiological differences noted between other bacterial thermophiles and mesophiles are evident within the Thermotogae. We argue that the Thermotogae is an ideal group of organisms for understanding of the response to fluctuating temperature and of long-term evolutionary adaptation to a different growth temperature range.Key words: lateral gene transfer, Kosmotoga, Mesotoga, thermostability, stress response. Résumé :Les thermophiles sont des extrémophiles dont la température optimale de croissance se situe au-delà de 45°C. Pour survivre et permettre à leurs biomolécules de bien fonctionner, ils doivent se doter de caractéristiques qu'on ne retrouve pas chez des organismes se développant à des températures intermédiaires (mésophiles). Sur le plan cellulaire, les thermophiles ont des mécanismes permettant de préserver leurs membranes, acides nucléiques et autres structures cellulaires. Au chapitre des protéines, chacune d'entre elles demeure stable et active à des températures qui dénatureraient leurs homologues mésophiles. En revanche, les structures et protéines cellulaires des thermophiles pourraient ne pas fonctionner de manière optimale à des températures intermédiaires. De telles différences entre les thermophiles et les mésophiles auraient tendance à se dresser en travers d'une transition évolutive entre ces deux modes de vie. Par conséquent, l'étude de thermophiles et de mésophiles fortement apparentés pourrait nous permettre d'établir comment surviendraient de telles transitions du mode de vie. Le phylum bactérien Thermotogae regroupe des hyperthermophiles, des thermophiles, des mésophiles et des organismes dont l'intervalle de températures chevauche les plages thermophiles et mésophiles. On observe parmi les Thermotogae des différences sur le plan génomique, protéomique, et physiologique qu'on relève également entre d'autres thermophiles et méso-philes bactériens. Nous soutenons que les Thermot...

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Duplication of Genes in an ATP-binding Cassette Transport System Increases Dynamic Range While Maintaining Ligand Specificity

Cited by 16 publications

References 39 publications

Mechanisms involved in xyloglucan catabolism by the cellulosome-producing bacterium Ruminiclostridium cellulolyticum

Mechanisms involved in xyloglucan catabolism by the cellulosome-producing bacterium Ruminiclostridium cellulolyticum

From substrate specificity to promiscuity: hybrid ABC transporters for osmoprotectants

Insights into thermoadaptation and the evolution of mesophily from the bacterial phylum Thermotogae

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