Cross-utilization of β-galactosides and cellobiose in Geobacillus stearothermophilus

Abstract

Strains of the Gram-positive, thermophilic bacterium Geobacillus stearothermophilus possess elaborate systems for the utilization of hemicellulolytic polysaccharides, including xylan, arabinan, and galactan. These systems have been studied extensively in strains T-1 and T-6, representing microbial models for the utilization of soil polysaccharides, and many of their components have been characterized both biochemically and structurally. Here, we characterized routes by which G. stearothermophilus utilizes mono- and disaccharides such as galactose, cellobiose, lactose, and galactosyl-glycerol. The G. stearothermophilus genome encodes a phosphoenolpyruvate carbohydrate phosphotransferase system (PTS) for cellobiose. We found that the cellobiose-PTS system is induced by cellobiose and characterized the corresponding GH1 6-phospho-β-glucosidase, Cel1A. The bacterium also possesses two transport systems for galactose, a galactose-PTS system and an ABC galactose transporter. The ABC galactose transport system is regulated by a three-component sensing system. We observed that both systems, the sensor and the transporter, utilize galactose-binding proteins that also bind glucose with the same affinity. We hypothesize that this allows the cell to control the flux of galactose into the cell in the presence of glucose. Unexpectedly, we discovered that G. stearothermophilus T-1 can also utilize lactose and galactosyl-glycerol via the cellobiose-PTS system together with a bifunctional 6-phospho-β-gal/glucosidase, Gan1D. Growth curves of strain T-1 growing in the presence of cellobiose, with either lactose or galactosyl-glycerol, revealed initially logarithmic growth on cellobiose and then linear growth supported by the additional sugars. We conclude that Gan1D allows the cell to utilize residual galactose-containing disaccharides, taking advantage of the promiscuity of the cellobiose-PTS system. Strains of the Gram-positive, thermophilic bacterium Geobacillus stearothermophilus possess elaborate systems for the utilization of hemicellulolytic polysaccharides, including xylan, arabinan, and galactan. These systems have been studied extensively in strains T-1 and T-6, representing microbial models for the utilization of soil polysaccharides, and many of their components have been characterized both biochemically and structurally. Here, we characterized routes by which G. stearothermophilus utilizes mono- and disaccharides such as galactose, cellobiose, lactose, and galactosyl-glycerol. The G. stearothermophilus genome encodes a phosphoenolpyruvate carbohydrate phosphotransferase system (PTS) for cellobiose. We found that the cellobiose-PTS system is induced by cellobiose and characterized the corresponding GH1 6-phospho-β-glucosidase, Cel1A. The bacterium also possesses two transport systems for galactose, a galactose-PTS system and an ABC galactose transporter. The ABC galactose transport system is regulated by a three-component sensing system. We observed that both systems, the sensor and the transporter, utilize galactose-binding proteins that also bind glucose with the same affinity. We hypothesize that this allows the cell to control the flux of galactose into the cell in the presence of glucose. Unexpectedly, we discovered that G. stearothermophilus T-1 can also utilize lactose and galactosyl-glycerol via the cellobiose-PTS system together with a bifunctional 6-phospho-β-gal/glucosidase, Gan1D. Growth curves of strain T-1 growing in the presence of cellobiose, with either lactose or galactosyl-glycerol, revealed initially logarithmic growth on cellobiose and then linear growth supported by the additional sugars. We conclude that Gan1D allows the cell to utilize residual galactose-containing disaccharides, taking advantage of the promiscuity of the cellobiose-PTS system. Geobacillus stearothermophilus T-1 is a thermophilic, Gram-positive, soil bacterium, which is capable of utilizing plant cell wall–derived polysaccharides, including xylan, arabinan, and galactan (1Shulami S. Gat O. Sonenshein A.L. Shoham Y. The glucuronic acid utilization gene cluster from Bacillus stearothermophilus T-6.J. Bacteriol. 1999; 181 (10368143): 3695-370410.1128/JB.181.12.3695-3704.1999Crossref PubMed Google Scholar, 2Shulami S. Raz-Pasteur A. Tabachnikov O. Gilead-Gropper S. Shner I. Shoham Y. The l-arabinan utilization system of Geobacillus stearothermophilus.J. Bacteriol. 2011; 193 (21460081): 2838-285010.1128/JB.00222-11Crossref PubMed Scopus (44) Google Scholar, 3Tabachnikov O. Shoham Y. Functional characterization of the galactan utilization system of Geobacillus stearothermophilus.FEBS J. 2013; 280 (23216604): 950-96410.1111/febs.12089PubMed Google Scholar). Utilization of these polysaccharides includes extracellular and intracellular hemicellulolytic enzymes, ABC sugar-transport systems, carbohydrate-sensing systems, sugar metabolism enzymes, and regulatory proteins (4Bravman T. Mechaly A. Shulami S. Belakhov V. Baasov T. Shoham G. Shoham Y. Glutamic acid 160 is the acid-base catalyst of β-xylosidase from Bacillus stearothermophilus T-6: a family 39 glycoside hydrolase.FEBS Lett. 2001; 495 (11322958): 115-11910.1016/S0014-5793(01)02371-7Crossref PubMed Scopus (41) Google Scholar, 5Zaide G. Shallom D. Shulami S. Zolotnitsky G. Golan G. Baasov T. Shoham G. Shoham Y. Biochemical characterization and identification of catalytic residues in α-glucuronidase from Bacillus stearothermophilus T-6.Eur. J. Biochem. 2001; 268 (11358519): 3006-301610.1046/j.1432-1327.2001.02193.xCrossref PubMed Scopus (43) Google Scholar, 6Shallom D. Belakhov V. Solomon D. Shoham G. Baasov T. Shoham Y. 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The in PubMed Scopus Google Scholar). the we in G. stearothermophilus strain T-1 such systems for cellobiose and galactose and biochemically characterized the corresponding These the to glycoside family and the also to family we that the bacterium can utilize the lactose and galactosyl-glycerol, the cellobiose-PTS system together with the bifunctional Gan1D. of a for hemicellulolytic utilization systems in G. we in strain T-1 a gene which to in the utilization of cellobiose The cluster via analysis of the genome of strains T-1 and includes an of and a on the for a system. The is to proteins from the family that bind cellobiose or and the and which the from to the The gene in this encodes for a 6-phospho-β-glucosidase, which to a of GH1 including from and to the the gene for a to the The for the and proteins on the G. stearothermophilus T-1 is to on on cellobiose. the and in cellobiose we the corresponding in on cellobiose, or glucose. from and the with to and as as for the that for by as in The of the corresponding in the as with on or glucose. The of with the in These that the is induced by cellobiose and to in cellobiose The of and a catalytic on with glucose the and These that is a 6-phospho-β-glucosidase, with glucose as the The of on the The in a reaction The and for The and of The of in the of The is a which the of the two catalytic The the of and of and on of with GH1 enzymes, the and nucleophile catalytic residues and These residues with and the of the on the of the as the The catalytic of the catalytic and for and The with the and the with the the of a for an acid-base the of the the of the a The to the of the for the of the catalytic A. Thompson J. Y. into the of a from Biol. Chem. 2013; Full Text Full Text PDF PubMed Scopus Google Scholar). The of the nucleophile in a the of this to bind the and the glycoside the nucleophile is in a with the of the sugar D. T. A. Zaide G. Belakhov V. Shoham G. Schomburg D. Baasov T. Shoham Y. Biochemical characterization and identification of the catalytic residues of a family from Geobacillus stearothermophilus PubMed Scopus Google catalytic for the of and by Cel1A. The in in a We have that G. stearothermophilus T-1 galactan utilizing the galactan utilization gene O. Shoham Y. Functional characterization of the galactan utilization system of Geobacillus stearothermophilus.FEBS J. 2013; 280 (23216604): 950-96410.1111/febs.12089PubMed Google Scholar). analysis of the bacterium genome we a cluster that to in galactose cluster is of for a three-component regulatory sensing system an ABC sugar transport system a regulatory and two and to proteins with a acid of including two residues residues an extracellular and a the from the gene the which encodes for a with to in the for many a with an to a and proteins in Biochem. 2001; Full Text Full Text PDF PubMed Scopus Google Scholar). The residues a with the of the the a the A. K. family of Biol. 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The of the which is of a three-component sensing to and of the these the system to galactose, is that the sensing systems The of the systems also in on either galactose or glucose The of the gene in for a on that is of the galactose-PTS transporter, to galactose these that G. stearothermophilus T-1 two transport systems for The three-component system for galactose, and the galactose ABC transport both have proteins and that to the The of these proteins to bind galactose by The curves in and the in These that and to bind galactose with in the and of with cellobiose and lactose in a both proteins bind glucose in to glucose to bind these proteins is that can the corresponding sensing systems, the of the of these systems is by glucose for the of galactose or glucose to and in a The that the three-component sensing system for galactose is to a ABC transport system that the sensing system is to this transport system and that is a that the of the transporter. of of gene found in G. stearothermophilus also for the and utilization systems S. Raz-Pasteur A. Tabachnikov O. Gilead-Gropper S. Shner I. Shoham Y. The l-arabinan utilization system of Geobacillus stearothermophilus.J. Bacteriol. 2011; 193 (21460081): 2838-285010.1128/JB.00222-11Crossref PubMed Scopus (44) Google Scholar, S. Zaide G. Zolotnitsky G. Y. G. Sonenshein A.L. Shoham Y. system the of an ABC for in Geobacillus PubMed Scopus Google Scholar). analysis of the of revealed a which is a to the is by from the which from the Bacillus by A. S. S. in the Bacillus 2001; PubMed Scopus Google Scholar). The of the of the two by which as the for the of the can of the with the of the of of gene PubMed Scopus Google Scholar, A. A. 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The of the linear growth to the the of the logarithmic in and These can by the of the the of the logarithmic that of the cellobiose is and that the the cellobiose-PTS the of the the of systems cell to that the of the growth is to the transport of lactose or galactosyl-glycerol into the via the of the cellobiose-PTS to in with the linear cell growth observed from this which is to the of cellobiose-PTS systems these as G. stearothermophilus T-1 is capable of utilizing the cellobiose-PTS system for and the Gan1D for of this is that G. stearothermophilus T-6, a of strain possesses a cellobiose-PTS system a the this strain on cellobiose to on lactose or galactosyl-glycerol in the presence of cellobiose G. stearothermophilus encodes for systems, to the of cellobiose, galactose, and The cellobiose-PTS system on the that the is in the presence of cellobiose and that The cellobiose-PTS system is regulated by an for includes an of and is the of the G. stearothermophilus can utilize cellobiose, for this bacterium to possess the to from the residual cellobiose, which is the of by The system for galactose in G. stearothermophilus on the of of the gene in the presence of The system is by a of a with the corresponding of and together an and a The gene in the is for an of the and by a that as a possesses an by two which to and the I. 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Functional characterization of the galactan utilization system of Geobacillus stearothermophilus.FEBS J. 2013; 280 (23216604): 950-96410.1111/febs.12089PubMed Google Scholar). galactose, as the is in the that also regulated by the same in the of the galactose metabolism which is regulated by a the GH1 two catalytic have been of and and galactose by the of their the an in and an in Gan1D catalytic sugar with or in their the that Gan1D as a These to in of the catalytic for GH1 many of which also to with to the sugar of their and with to the of the the of this sugar glucose D. T. A. Zaide G. Belakhov V. Shoham G. Schomburg D. Baasov T. Shoham Y. Biochemical characterization and identification of the catalytic residues of a family from Geobacillus stearothermophilus PubMed Scopus Google Scholar, A. K. family of Biol. PubMed Scopus Google Scholar). in for the utilization of lactose, which is into the cell via a system A.L. characterization and of the gene of the and the PubMed Scopus Google Scholar). the of G. the that strain T-1 encodes for an with a system to we to that strain T-1 can utilize lactose and galactosyl-glycerol in the presence of cellobiose. These that the cellobiose-PTS system also lactose and galactosyl-glycerol. Growth curves of strain growing in the presence of cellobiose together with either lactose or galactosyl-glycerol an logarithmic growth by a linear growth The curves of the linear growth to the the of the logarithmic These that cellobiose is logarithmic and either lactose or galactosyl-glycerol can the cell via the same cellobiose-PTS a affinity. The linear growth is to the that the of lactose is a and that in the of cellobiose, the cellobiose-PTS is this in that Gan1D in two in G. stearothermophilus allows the cell to utilize residual galactose-containing disaccharides, the galactosyl-glycerol, taking advantage of the promiscuity of the cellobiose-PTS system. the for the in the this a growth is also that the cellobiose-PTS system allows the of which in the cell and such Gan1D can these to their this the gene have a A. PubMed Scopus Google as for Gan1D. Growth for G. stearothermophilus S. O. Y. Gat O. Zaide G. A. Sonenshein A.L. Shoham Y. regulatory control the of the Geobacillus stearothermophilus gene for extracellular Biol. Chem. Full Text Full Text PDF PubMed Scopus Google with of the of of of and of to with of of of acid of and of and of of of and of The of the to with G. stearothermophilus T-1 to the by J. for the of acid from Biol. Scopus Google as by of for for Scholar). the by J. 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The and on a or and to with as the and to with as the on a or and the to the residual for or to the for either on a or by a by on and by with a and in on an with from and from a of in of to a of in The reaction for and then an additional by the reaction the to and with by the of of in The with of the with and the on on in the additional for The of in and in the for by the of the in for The reaction and then The the with and the to The by on to as a of two for a of in and the reaction by the reaction to and The reaction a and with for The observed from the in a of The reaction by the reaction the with and the by on to as for The and into The and their and of the to of the into the the and the The to the The to that the of and the or in J. with in to a of The in of by two a and for to The proteins a on an system the of the in with in growth then in the presence of for to a of The in of by two and for to The on an system to the and a The of and by the of and to of and in this into in a The of Gan1D the of the or The in and Gan1D. in the of The by of to of in a The for a The of and as the and in and the The kinetic with by the of glucose. 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Full Text Full Text PDF PubMed Scopus Google with cellobiose as the The logarithmic that with and then in a for with cellobiose and The with and for cell growth in a in the The the galactose utilization the cellobiose-PTS and the galactose-PTS system from G. stearothermophilus T-1 have been in the and We for the K. phosphotransferase system cellobiose lactose glycoside

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