The thuEFGKAB Operon of Rhizobia and Agrobacterium tumefaciens Codes for Transport of Trehalose, Maltitol, and Isomers of Sucrose and Their Assimilation through the Formation of Their 3-Keto Derivatives

Ampomah OY, Avetisyan A, Hansen E, Svenson J, Huser T, Jensen JB, Bhuvaneswari TV (2013)
Journal Of Bacteriology 195(17): 3797-3807.

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Zeitschriftenaufsatz | Veröffentlicht | Englisch
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Abstract / Bemerkung
The thu operon (thuEFGKAB) in Sinorhizobium meliloti codes for transport and utilization functions of the disaccharide trehalose. Sequenced genomes of members of the Rhizobiaceae reveal that some rhizobia and Agrobacterium possess the entire thu operon in similar organizations and that Mesorhizobium loti MAFF303099 lacks the transport (thuEFGK) genes. In this study, we show that this operon is dedicated to the transport and assimilation of maltitol and isomers of sucrose (leucrose, palatinose, and trehalulose) in addition to trehalulose, not only in S. meliloti but also in Agrobacterium tumefaciens. By using genetic complementation, we show that the thuAB genes of S. meliloti, M. loti, and A. tumefaciens are functionally equivalent. Further, we provide both genetic and biochemical evidence to show that these bacteria assimilate these disaccharides by converting them to their respective 3-keto derivatives and that the thuAB genes code for this ketodisaccharide-forming enzyme(s). Formation of 3-ketotrehalose in real time in live S. meliloti is shown through Raman spectroscopy. The presence of an additional ketodisaccharide-forming pathway(s) in A. tumefaciens is also indicated. To our knowledge, this is the first report to identify the genes that code for the conversion of disaccharides to their 3-ketodisaccharide derivatives in any organism.
Erscheinungsjahr
Zeitschriftentitel
Journal Of Bacteriology
Band
195
Ausgabe
17
Seite(n)
3797-3807
ISSN
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Ampomah OY, Avetisyan A, Hansen E, et al. The thuEFGKAB Operon of Rhizobia and Agrobacterium tumefaciens Codes for Transport of Trehalose, Maltitol, and Isomers of Sucrose and Their Assimilation through the Formation of Their 3-Keto Derivatives. Journal Of Bacteriology. 2013;195(17):3797-3807.
Ampomah, O. Y., Avetisyan, A., Hansen, E., Svenson, J., Huser, T., Jensen, J. B., & Bhuvaneswari, T. V. (2013). The thuEFGKAB Operon of Rhizobia and Agrobacterium tumefaciens Codes for Transport of Trehalose, Maltitol, and Isomers of Sucrose and Their Assimilation through the Formation of Their 3-Keto Derivatives. Journal Of Bacteriology, 195(17), 3797-3807. doi:10.1128/JB.00478-13
Ampomah, O. Y., Avetisyan, A., Hansen, E., Svenson, J., Huser, T., Jensen, J. B., and Bhuvaneswari, T. V. (2013). The thuEFGKAB Operon of Rhizobia and Agrobacterium tumefaciens Codes for Transport of Trehalose, Maltitol, and Isomers of Sucrose and Their Assimilation through the Formation of Their 3-Keto Derivatives. Journal Of Bacteriology 195, 3797-3807.
Ampomah, O.Y., et al., 2013. The thuEFGKAB Operon of Rhizobia and Agrobacterium tumefaciens Codes for Transport of Trehalose, Maltitol, and Isomers of Sucrose and Their Assimilation through the Formation of Their 3-Keto Derivatives. Journal Of Bacteriology, 195(17), p 3797-3807.
O.Y. Ampomah, et al., “The thuEFGKAB Operon of Rhizobia and Agrobacterium tumefaciens Codes for Transport of Trehalose, Maltitol, and Isomers of Sucrose and Their Assimilation through the Formation of Their 3-Keto Derivatives”, Journal Of Bacteriology, vol. 195, 2013, pp. 3797-3807.
Ampomah, O.Y., Avetisyan, A., Hansen, E., Svenson, J., Huser, T., Jensen, J.B., Bhuvaneswari, T.V.: The thuEFGKAB Operon of Rhizobia and Agrobacterium tumefaciens Codes for Transport of Trehalose, Maltitol, and Isomers of Sucrose and Their Assimilation through the Formation of Their 3-Keto Derivatives. Journal Of Bacteriology. 195, 3797-3807 (2013).
Ampomah, Osei Yaw, Avetisyan, Anna, Hansen, Espen, Svenson, Johan, Huser, Thomas, Jensen, John Beck, and Bhuvaneswari, T. V. “The thuEFGKAB Operon of Rhizobia and Agrobacterium tumefaciens Codes for Transport of Trehalose, Maltitol, and Isomers of Sucrose and Their Assimilation through the Formation of Their 3-Keto Derivatives”. Journal Of Bacteriology 195.17 (2013): 3797-3807.

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Defining the Genetic Basis of Plant⁻Endophytic Bacteria Interactions.
Pinski A, Betekhtin A, Hupert-Kocurek K, Mur LAJ, Hasterok R., Int J Mol Sci 20(8), 2019
PMID: 31010043
The Impact of Maltitol-Sweetened Chewing Gum on the Dental Plaque Biofilm Microbiota Composition.
Keijser BJF, van den Broek TJ, Slot DE, van Twillert L, Kool J, Thabuis C, Ossendrijver M, van der Weijden FA, Montijn RC., Front Microbiol 9(), 2018
PMID: 29559963
Genomic resources for identification of the minimal N2 -fixing symbiotic genome.
diCenzo GC, Zamani M, Milunovic B, Finan TM., Environ Microbiol 18(8), 2016
PMID: 26768651
RNA-seq analysis of the Rhizobium tropici CIAT 899 transcriptome shows similarities in the activation patterns of symbiotic genes in the presence of apigenin and salt.
Pérez-Montaño F, Del Cerro P, Jiménez-Guerrero I, López-Baena FJ, Cubo MT, Hungria M, Megías M, Ollero FJ., BMC Genomics 17(), 2016
PMID: 26951045
Organic acid mediated repression of sugar utilization in rhizobia.
Iyer B, Rajput MS, Jog R, Joshi E, Bharwad K, Rajkumar S., Microbiol Res 192(), 2016
PMID: 27664739
Genetic redundancy is prevalent within the 6.7 Mb Sinorhizobium meliloti genome.
diCenzo GC, Finan TM., Mol Genet Genomics 290(4), 2015
PMID: 25638282
Raman spectroscopy for physiological investigations of tissues and cells.
Huser T, Chan J., Adv Drug Deliv Rev 89(), 2015
PMID: 26144996
Examination of prokaryotic multipartite genome evolution through experimental genome reduction.
diCenzo GC, MacLean AM, Milunovic B, Golding GB, Finan TM., PLoS Genet 10(10), 2014
PMID: 25340565

59 References

Daten bereitgestellt von Europe PubMed Central.

How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model.
Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC., Nat. Rev. Microbiol. 5(8), 2007
PMID: 17632573
The metabolism of alpha,alpha-trehalose.
Elbein AD., Adv Carbohydr Chem Biochem 30(), 1974
PMID: 4377836
Disaccharides as a new class of nonaccumulated osmoprotectants for Sinorhizobium meliloti.
Gouffi K, Pica N, Pichereau V, Blanco C., Appl. Environ. Microbiol. 65(4), 1999
PMID: 10103242
The accumulation of trehalose in nodules of several cultivars of common bean () and its correlation with resistance to drought stress
Farías-Rodriguez R, Mellor RB, Arias C, Pena-Cabriales JJ., 1998
Trehalose induces antagonism towards Pythium debaryanum in Pseudomonas fluorescens ATCC 17400.
Gaballa A, Abeysinghe PD, Urich G, Matthijs S, De Greve H, Cornelis P, Koedam N., Appl. Environ. Microbiol. 63(11), 1997
PMID: 9361421
Regulation of trehalose mobilization in fungi.
Thevelein JM., Microbiol. Rev. 48(1), 1984
PMID: 6325857
Trehalose transport and metabolism in Escherichia coli.
Boos W, Ehmann U, Forkl H, Klein W, Rimmele M, Postma P., J. Bacteriol. 172(6), 1990
PMID: 2160944
Trehalose-6-phosphate hydrolase of Escherichia coli.
Rimmele M, Boos W., J. Bacteriol. 176(18), 1994
PMID: 8083158
Physiological role of beta-phosphoglucomutase in Lactococcus lactis.
Levander F, Andersson U, Radstrom P., Appl. Environ. Microbiol. 67(10), 2001
PMID: 11571154
Comparative genomic analyses of the bacterial phosphotransferase system.
Barabote RD, Saier MH Jr., Microbiol. Mol. Biol. Rev. 69(4), 2005
PMID: 16339738
Enzymes of alpha,alpha-Trehalose Metabolism in Soybean Nodules.
Salminen SO, Streeter JG., Plant Physiol. 81(2), 1986
PMID: 16664852
Stimulation of α-glucosidases from fast-growing rhizobia and by K, NH, and Rb
Hoelzle I, Streeter JG., 1990
Role of trehalose transport and utilization in Sinorhizobium meliloti--alfalfa interactions.
Jensen JB, Ampomah OY, Darrah R, Peters NK, Bhuvaneswari TV., Mol. Plant Microbe Interact. 18(7), 2005
PMID: 16042015
N-(carboxyalkyl)amino acids: occurrence, synthesis, and functions.
Thompson J, Donkersloot JA., Annu. Rev. Biochem. 61(), 1992
PMID: 1497319
Structure-based redesign of cofactor binding in putrescine oxidase.
Kopacz MM, Rovida S, van Duijn E, Fraaije MW, Mattevi A., Biochemistry 50(19), 2011
PMID: 21486042
Molecular cloning: a laboratory manual
Sambrook J, Fritsch EF, Maniatis T., 1989
Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti.
Ditta G, Stanfield S, Corbin D, Helinski DR., Proc. Natl. Acad. Sci. U.S.A. 77(12), 1980
PMID: 7012838
Transposon mutagenesis
de FJ, Rossbach S., 1994
Experiments in molecular genetics
Miller JH., 1972
The production of 3-ketosucrose by in batch culture
Kurowski MW, Darbyshire J., 1978
Micro methods for determination of 3-ketosucrose and 3-ketoglucose
Fukui S, Hayano K., 1969
Purification and properties of 3-ketosucrose-forming enzyme from cells of
Hayano K, Fukui S., 1967
The partitioned Rhizobium etli genome: genetic and metabolic redundancy in seven interacting replicons.
Gonzalez V, Santamaria RI, Bustos P, Hernandez-Gonzalez I, Medrano-Soto A, Moreno-Hagelsieb G, Janga SC, Ramirez MA, Jimenez-Jacinto V, Collado-Vides J, Davila G., Proc. Natl. Acad. Sci. U.S.A. 103(10), 2006
PMID: 16505379
Complete genome sequence of Rhizobium leguminosarum bv trifolii strain WSM2304, an effective microsymbiont of the South American clover Trifolium polymorphum.
Reeve W, O'Hara G, Chain P, Ardley J, Brau L, Nandesena K, Tiwari R, Malfatti S, Kiss H, Lapidus A, Copeland A, Nolan M, Land M, Ivanova N, Mavromatis K, Markowitz V, Kyrpides N, Melino V, Denton M, Yates R, Howieson J., Stand Genomic Sci 2(1), 2010
PMID: 21304679
Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti.
Kaneko T, Nakamura Y, Sato S, Asamizu E, Kato T, Sasamoto S, Watanabe A, Idesawa K, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Mochizuki Y, Nakayama S, Nakazaki N, Shimpo S, Sugimoto M, Takeuchi C, Yamada M, Tabata S., DNA Res. 7(6), 2000
PMID: 11214968
Identification of a dehydrogenase required for lactose metabolism in Caulobacter crescentus.
Arellano BH, Ortiz JD, Manzano J, Chen JC., Appl. Environ. Microbiol. 76(9), 2010
PMID: 20190087
Hexopyranoside: cytochrome c oxidoreductase from Agrobacterium tumefaciens.
Van Beeumen J, De Ley J., Eur. J. Biochem. 6(3), 1968
PMID: 5726844
Regioselective synthesis of new sucrose derivatives via 3-ketosucrose.
Pietsch M, Walter M, Buchholz K., Carbohydr. Res. 254(), 1994
PMID: 8180983
New regioselective derivatives of sucrose with amino acid and acrylic groups.
Anders J, Buczys R, Lampe E, Walter M, Yaacoub E, Buchholz K., Carbohydr. Res. 341(3), 2005
PMID: 16376867
Monitoring dynamic protein expression in living E. coli. Bacterial cells by laser tweezers Raman spectroscopy.
Chan JW, Winhold H, Corzett MH, Ulloa JM, Cosman M, Balhorn R, Huser T., Cytometry A 71(7), 2007
PMID: 17458881
Evaluation of Escherichia coli cell response to antibiotic treatment by use of Raman spectroscopy with laser tweezers.
Moritz TJ, Polage CR, Taylor DS, Krol DM, Lane SM, Chan JW., J. Clin. Microbiol. 48(11), 2010
PMID: 20861343
Metabolism of sucrose and its five isomers by Fusobacterium mortiferum.
Pikis A, Immel S, Robrish SA, Thompson J., Microbiology (Reading, Engl.) 148(Pt 3), 2002
PMID: 11882720
Purification and properties of glucoside 3-dehydrogenase from Flavobacterium saccharophilum.
Takeuchi M, Ninomiya K, Kawabata K, Asano N, Kameda Y, Matsui K., J. Biochem. 100(4), 1986
PMID: 3818559
Effect of growth substrates on production of new soluble glucose 3-dehydrogenase in Halomonas (Deleya) sp. alpha-15.
Kojima K, Tsugawa W, Hamahuji T, Watazu Y, Sode K., Appl. Biochem. Biotechnol. 77-79(), 1999
PMID: 15304701
Preparation of 3-amino-3-deoxy derivatives of trehalose and sucrose and their activities.
Asano N, Katayama K, Takeuchi M, Furumoto T, Kameda Y, Matsui K., J. Antibiot. 42(4), 1989
PMID: 2498271
Carbohydrate biotechnology protocols
Stoppok E, Buchholz K., 1999
Transformation of cellobiose to 3-ketocellobiose by the EDTA-treated Agrobacterium tumefaciens cells.
Maeda A, Kataoka H, Adachi S, Matsuno R., J. Biosci. Bioeng. 95(6), 2003
PMID: 16233465
A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria
Simon R, Priefer U, Pühler A., 1983

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