Home Study of two glycosyltransferases related to polysaccharide biosynthesis in Rhodococcus jostii RHA1
Article
Licensed
Unlicensed Requires Authentication

Study of two glycosyltransferases related to polysaccharide biosynthesis in Rhodococcus jostii RHA1

  • Antonela Estefania Cereijo , María Victoria Ferretti , Alberto Alvaro Iglesias ORCID logo , Héctor Manuel Álvarez and Matías Damian Asencion Diez ORCID logo EMAIL logo
Published/Copyright: March 15, 2024
Biological Chemistry
From the journal Biological Chemistry Volume 405 Issue 5

Abstract

The bacterial genus Rhodococcus comprises organisms performing oleaginous behaviors under certain growth conditions and ratios of carbon and nitrogen availability. Rhodococci are outstanding producers of biofuel precursors, where lipid and glycogen metabolisms are closely related. Thus, a better understanding of rhodococcal carbon partitioning requires identifying catalytic steps redirecting sugar moieties to storage molecules. Here, we analyzed two GT4 glycosyl-transferases from Rhodococcus jostii (RjoGlgAb and RjoGlgAc) annotated as α-glucan-α-1,4-glucosyl transferases, putatively involved in glycogen synthesis. Both enzymes were produced in Escherichia coli cells, purified to homogeneity, and kinetically characterized. RjoGlgAb and RjoGlgAc presented the “canonical” glycogen synthase activity and were actives as maltose-1P synthases, although to a different extent. Then, RjoGlgAc is a homologous enzyme to the mycobacterial GlgM, with similar kinetic behavior and glucosyl-donor preference. RjoGlgAc was two orders of magnitude more efficient to glucosylate glucose-1P than glycogen, also using glucosamine-1P as a catalytically efficient aglycon. Instead, RjoGlgAb exhibited both activities with similar kinetic efficiency and preference for short-branched α-1,4-glucans. Curiously, RjoGlgAb presented a super-oligomeric conformation (higher than 15 subunits), representing a novel enzyme with a unique structure-to-function relationship. Kinetic results presented herein constitute a hint to infer on polysaccharides biosynthesis in rhodococci from an enzymological point of view.

Keywords: glycogen; methyl-glucose lipopolysaccharide; glucosamine-1P; glucose-1P; maltose-1P; gene redundancy
Corresponding author: Matías Damian Asencion Diez, Laboratorio de Enzimología Molecular, Instituto de Agrobiotecnología del Litoral. CCT-CONICET-Santa Fe,Colectora Ruta Nac. 168 km 0, Paraje “El Pozo”, 3000 Santa Fe, Argentina, E-mail:

Funding source: Fondo para la Investigación Científica y Tecnológica

Award Identifier / Grant number: PICT-2018-00698,PICT-2018-00929,PICT-2020-03326

Funding source: Consejo Nacional de Investigaciones Científicas y Técnicas

Award Identifier / Grant number: PIP2015-2016 0529

Acknowledgments

AAI, HMA and MDAD are career investigator members of the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina. AEC and MVF are fellowship holders from CONICET.

  1. Research ethics: This article does not contain any studies with human participants or animals performed by any of the authors.

  2. Author contributions: MDAD and HMA conceived and designed research. AEC, MVF and MDAD conducted experiments. MDAD, HMA and AAI contributed reagents and analytical tools. MDAD, AEC and MVF analyzed data. MDAD and AEC wrote the manuscript. All authors read, revised and approved the manuscript.

  3. Competing interests: The authors declare no conflict of interest.

  4. Research funding: This study was funded by grants from ANPCyT (PICT-2018-00929 and PICT-2020-03326 to AAI; and PICT-2018-00698 to MDAD) and CONICET (PIP2015-2016 0529 to HMA).

  5. Data availability: All data generated or analyzed during this study are included in this published article (and its supplementary information files).

References

Alarico, S., Empadinhas, N., and da Costa, M.S. (2013). A new bacterial hydrolase specific for the compatible solutes α-D-mannopyranosyl-(1→2)-D-glycerate and α-D-glucopyranosyl-(1→2)-D-glycerate. Enzyme Microb. Technol. 52: 77–83, https://doi.org/10.1016/j.enzmictec.2012.10.008.Search in Google Scholar PubMed

Álvarez-Lugo, A. and Becerra, A. (2021). The role of gene duplication in the divergence of enzyme function: a comparative approach. Front. Genet. 12: 1253, https://doi.org/10.3389/fgene.2021.641817.Search in Google Scholar PubMed PubMed Central

Alvarez, H.M., Hernández, M.A., Lanfranconi, M.P., Silva, R.A., Villalba, M.S. (2021). Rhodococcus as biofactories for microbial oil production. Molecules 26: 4871. https://doi.org/10.3390/molecules26164871.Search in Google Scholar PubMed PubMed Central

Asención Diez, M.D., Demonte, A.M., Syson, K., Arias, D.G., Gorelik, A., Guerrero, S.A., Bornemann, S., and Iglesias, A.A. (2015). Allosteric regulation of the partitioning of glucose-1-phosphate between glycogen and trehalose biosynthesis in Mycobacterium tuberculosis. Biochim. Biophys. Acta 1850: 13–21, https://doi.org/10.1016/j.bbagen.2014.09.023.Search in Google Scholar PubMed PubMed Central

Asención Diez, M.D., Miah, F., Stevenson, C.E.M., Lawson, D.M., Iglesias, A.A., and Bornemann, S. (2017). The production and utilization of GDP-glucose in the biosynthesis of trehalose 6-phosphate by Streptomyces venezuelae. J. Biol. Chem. 292: 945–954, https://doi.org/10.1074/jbc.M116.758664.Search in Google Scholar PubMed PubMed Central

Asención Diez, M.D., Peirú, S., Demonte, A.M., Gramajo, H., and Iglesias, A.A. (2012). Characterization of recombinant UDP- and ADP-glucose pyrophosphorylases and glycogen synthase to elucidate glucose-1-phosphate partitioning into oligo- and polysaccharides in Streptomyces coelicolor. J. Bacteriol. 194: 1485–1493, https://doi.org/10.1128/JB.06377-11.Search in Google Scholar PubMed PubMed Central

Ball, S.G. and Morell, M.K. (2003). From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule. Annu. Rev. Plant Biol. 54: 207–233, https://doi.org/10.1146/annurev.arplant.54.031902.134927.Search in Google Scholar PubMed

Ballicora, M., Iglesias, A., and Preiss, J. (2003). ADP-glucose pyrophosphorylase, a regulatory enzyme for bacterial glycogen synthesis. Microbiol. Mol. Biol. Rev. 67: 213–225, https://doi.org/10.1128/mmbr.67.2.213-225.2003.Search in Google Scholar PubMed PubMed Central

Ballicora, M.A., Erben, E.D., Yazaki, T., Bertolo, A.L., Demonte, A.M., Schmidt, Jr., Aleanzi, M., Bejar, C.M., Figueroa, C.M., Fusari, C.M., et al.. (2007). Identification of regions critically affecting kinetics and allosteric regulation of the Escherichia coli ADP-glucose pyrophosphorylase by modeling and pentapeptide-scanning mutagenesis. J. Bacteriol. 189: 5325–5333, https://doi.org/10.1128/jb.00481-07.Search in Google Scholar PubMed PubMed Central

Barchiesi, J., Hedin, N., Iglesias, A.A., Gomez-Casati, D.F., Ballicora, M.A., and Busi, M.V. (2017). Identification of a novel starch synthase III from the picoalgae Ostreococcus tauri. Biochimie 133: 37–44, https://doi.org/10.1016/j.biochi.2016.12.003.Search in Google Scholar PubMed

Barchiesi, J., Velazquez, M.B., Palopoli, N., Iglesias, A.A., Gomez-Casati, D.F., Ballicora, M.A., and Busi, M.V. (2018). Starch synthesis in Ostreococcus tauri: the starch-binding domains of starch synthase III-B are essential for catalytic activity. Front. Plant Sci. 9: 1541, https://doi.org/10.3389/fpls.2018.01541.Search in Google Scholar PubMed PubMed Central

Bar-Even, A., Noor, E., Savir, Y., Liebermeister, W., Davidi, D., Tawfik, D.S., and Milo, R. (2011). The moderately efficient enzyme: evolutionary and physicochemical trends shaping enzyme parameters. Biochemistry 50: 4402–4410, https://doi.org/10.1021/bi2002289.Search in Google Scholar PubMed

Bentley, S.D., Chater, K.F., Cerdeño-Tárraga, A.M., Challis, G.L., Thomson, N.R., James, K.D., Harris, D.E., Quail, M.A., Kieser, H., Harper, D., et al. (2002). Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417: 141–147, https://doi.org/10.1038/417141a.Search in Google Scholar PubMed

Bhayani, J., Iglesias, M.J., Minen, R.I., Cereijo, A.E., Ballicora, M.A., Iglesias, A.A., and Asencion Diez, M.D. (2022). Carbohydrate metabolism in bacteria: alternative specificities in ADP-glucose pyrophosphorylases open novel metabolic scenarios and biotechnological tools. Front. Microbiol. 13: 867384, https://doi.org/10.3389/fmicb.2022.867384.Search in Google Scholar PubMed PubMed Central

Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254, https://doi.org/10.1006/abio.1976.9999.Search in Google Scholar PubMed

Buschiazzo, A., Ugalde, J.E., Guerin, M.E., Shepard, W., Ugalde, R.A., and Alzari, P.M. (2004). Crystal structure of glycogen synthase: homologous enzymes catalyze glycogen synthesis and degradation. EMBO J. 23: 3196–3205, https://doi.org/10.1038/sj.emboj.7600324.Search in Google Scholar PubMed PubMed Central

Busi, M.V., Palopoli, N., Valdez, H.A., Fornasari, M.S., Wayllace, N.Z., Gomez-Casati, D.F., Parisi, G., and Ugalde, R.A. (2008). Functional and structural characterization of the catalytic domain of the starch synthase III from Arabidopsis thaliana. Proteins 70: 31–40, https://doi.org/10.1002/prot.21469.Search in Google Scholar PubMed

Cappelletti, M., Zampolli, J., Di Gennaro, P., and Zannoni, D. (2019). Genomics of Rhodococcus. In: Alvarez, H. (Ed.). Biology of Rhodococcus, 2nd ed Springer, Cham, Switzerland, pp. 23–60.10.1007/978-3-030-11461-9_2Search in Google Scholar

Cereija, T.B., Alarico, S., Lourenço, EC., Manso, J.A., Ventura, M.R., Empadinhas, N., Macedo-Ribeiro, S., and Pereira, P.J.B. (2019). The structural characterization of a glucosylglycerate hydrolase provides insights into the molecular mechanism of mycobacterial recovery from nitrogen starvation. IUCrJ 6: 572–585, https://doi.org/10.1107/S2052252519005372.Search in Google Scholar PubMed PubMed Central

Cereijo, A., Alvarez, H., Iglesias, A., and Asencion Diez, M. (2020). Glucosamine-P and rhodococcal ADP-glucose pyrophosphorylases: a hint to (re)discover (actino)bacterial amino sugar metabolism. Biochimie 176: 158–161, https://doi.org/10.1016/j.biochi.2020.07.006.Search in Google Scholar PubMed

Cereijo, A.E., Asencion Diez, M.D., Ballicora, M.A., and Iglesias, A.A. (2018). Regulatory properties of the ADP-glucose pyrophosphorylase from the clostridial firmicutes member Ruminococcus albus. J. Bacteriol. 200: e00172-18, https://doi.org/10.1128/JB.00172-18.Search in Google Scholar

Cereijo, A.E., Asencion Diez, M.D., Dávila Costa, J.S., Alvarez, H.M., and Iglesias, A.A. (2016). On the kinetic and allosteric regulatory properties of the ADP-glucose pyrophosphorylase from Rhodococcus jostii: an approach to evaluate glycogen metabolism in oleaginous bacteria. Front. Microbiol. 7: 830, https://doi.org/10.3389/fmicb.2016.00830.Search in Google Scholar

Cereijo, A.E., Kuhn, M.L., Hernández, M.A., Ballicora, M.A., Iglesias, A.A., Alvarez, H.M., and Asencion Diez, M.D. (2021). Study of duplicated galU genes in Rhodococcus jostii and a putative new metabolic node for glucosamine-1P in rhodococci. Biochim. Biophys. Acta Gen. Subj. 1865: 129727, https://doi.org/10.1016/j.bbagen.2020.129727.Search in Google Scholar

Chandra, G., Chater, K.F., and Bornemann, S. (2011). Unexpected and widespread connections between bacterial glycogen and trehalose metabolism. Microbiology 157: 1565–1572, https://doi.org/10.1099/mic.0.044263-0.Search in Google Scholar

Chaudhuri, P., Basu, A., Sengupta, S., Lahiri, S., Dutta, T., and Ghosh, A.K. (2009). Studies on substrate specificity and activity regulating factors of trehalose-6-phosphate synthase of Saccharomyces cerevisiae. Biochim. Biophys. Acta Gen. Subj. 1790: 368–374, https://doi.org/10.1016/j.bbagen.2009.03.008.Search in Google Scholar

Cifuente, J.O., Comino, N., Trastoy, B., D’Angelo, C., and Guerin, M.E. (2019). Structural basis of glycogen metabolism in bacteria. Biochem. J. 476: 2059–2092, https://doi.org/10.1042/BCJ20170558.Search in Google Scholar

Cole, S.T. Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S.V., Eiglmeier, K., Gas, S., Barry, C.E., et al. (1998). Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537–544. https://doi.org/10.1038/31159.Search in Google Scholar

Colpaert, M., Kadouche, D., Ducatez, M., Pillonel, T., Kebbi-Beghdadi, C., Cenci, U., Huang, B., Chabi, M., Maes, E., Coddeville, B., et al. (2021). Conservation of the glycogen metabolism pathway underlines a pivotal function of storage polysaccharides in Chlamydiae. Commun. Biol. 4: 296, https://doi.org/10.1038/s42003-021-01794-y.Search in Google Scholar

Daffe, M., McNeil, M., and Brennan, P.J. (1993). Major structural features of the cell wall arabinogalactans of Mycobacterium, Rhodococcus, and Nocardia spp. Carbohydr. Res. 249: 383–398, https://doi.org/10.1016/0008-6215(93)84102-C.Search in Google Scholar

D’Ari, R. and Casadesús, J. (1998). Underground metabolism. Bioessays 20:181–186. https://doi.org/10.1002/(SICI)1521-1878(199802)20:2<181::AID-BIES10>3.0.CO;2-0.10.1002/(SICI)1521-1878(199802)20:2<181::AID-BIES10>3.3.CO;2-6Search in Google Scholar

Davidia, D., Noorb, E., Liebermeisterc, W., Bar-Evend, A., Flamholze, A., Tummlerf, K., Barenholza, U., Goldenfelda, M., Shlomig, T., and Miloa, R. (2016). Global characterization of in vivo enzyme catalytic rates and their correspondence to in vitro kcat measurements. Proc. Natl. Acad. Sci. U. S. A. 113: 3401–3406, https://doi.org/10.1073/pnas.1514240113.Search in Google Scholar PubMed PubMed Central

Demonte, A.M., Asencion Diez, M.D., Naleway, C., Iglesias, A.A., and Ballicora, M.A. (2017). Monofluorophosphate blocks internal polysaccharide synthesis in Streptococcus mutans. PLoS One 12: e0170483, https://doi.org/10.1371/journal.pone.0170483.Search in Google Scholar PubMed PubMed Central

De Smet, K.A.L., Weston, A., Brown, I.N., Young, D.B., and Robertson, B.D. (2000). Three pathways for trehalose biosynthesis in mycobacteria. Microbiology 146: 199–208, https://doi.org/10.1099/00221287-146-1-199.Search in Google Scholar PubMed

Díaz-Mejía, J.J., Pérez-Rueda, E., and Segovia, L. (2007). A network perspective on the evolution of metabolism by gene duplication. Genome Biol. 8: R26, https://doi.org/10.1186/gb-2007-8-2-r26.Search in Google Scholar PubMed PubMed Central

Donini, E., Firrincieli, A., and Cappelletti, M. (2021). Systems biology and metabolic engineering of Rhodococcus for bioconversion and biosynthesis processes. Folia Microbiol. 66: 701–713, https://doi.org/10.1007/S12223-021-00892-y.Search in Google Scholar

Drepper, A., Peitzmann, R., and Pape, H. (1996). Maltokinase (ATP:maltose 1-phosphotransferase) from Actinoplanes sp.: demonstration of enzyme activity and characterization of the reaction product. FEBS Lett. 388: 177–179, https://doi.org/10.1016/0014-5793(96)00554-6.Search in Google Scholar PubMed

Drula, E., Garron, M.-L., Dogan, S., Lombard, V., Henrissat, B., and Terrapon, N. (2021). The carbohydrate-active enzyme database: functions and literature. Nucleic Acids Res. 50: D571–D577, https://doi.org/10.1093/nar/gkab1045.Search in Google Scholar PubMed PubMed Central

Elbein, A.D. and Mitchell, M. (1973). Levels of glycogen and trehalose in Mycobacterium smegmatis and the purification and properties of the glycogen synthetase. J. Bacteriol. 113: 863–873, https://doi.org/10.1128/jb.113.2.863-873.1973.Search in Google Scholar PubMed PubMed Central

Elbein, A.D., Pastuszak, I., Tackett, A.J., Wilson, T., and Pan, Y.T. (2010). Last step in the conversion of trehalose to glycogen: a mycobacterial enzyme that transfers maltose from maltose 1-phosphate to glycogen. J. Biol. Chem. 285: 9803–9812, https://doi.org/10.1074/jbc.M109.033944.Search in Google Scholar PubMed PubMed Central

Figueroa, C.M., Asencion Diez, M.D., Ballicora, M.A., Iglesias, A.A. (2022). Structure, function, and evolution of plant ADP-glucose pyrophosphorylase. Plant Mol. Biol. 2022 1:1–17. https://doi.org/10.1007/S11103-021-01235-8.Search in Google Scholar PubMed

Fraga, J., Maranha, A., Mendes, V., Pereira, P.J.B., Empadinhas, N., Macedo-Ribeiro, S. (2015). Structure of mycobacterial maltokinase, the missing link in the essential GlgE-pathway. Sci. Rep. 2015 51:1–12. https://doi.org/10.1038/srep08026.Search in Google Scholar PubMed PubMed Central

Galet, C., Le Bourhis, C.M., Chopineau, M., Le Griec, G., Perrin, A., Magallon, T., Attal, J., Viglietta, C., Houdebine, L.M., and Guillou, F. (2001). Expression of a single betaalpha chain protein of equine LH/CG in milk of transgenic rabbits and its biological activity. Mol. Cell. Endocrinol. 174: 31–40, https://doi.org/10.1016/s0303-7207(00)00452-4.Search in Google Scholar PubMed

Glasner, M.E., Truong, D.P., and Morse, B.C. (2020). How enzyme promiscuity and horizontal gene transfer contribute to metabolic innovation. FEBS J. 287: 1323–1342, https://doi.org/10.1111/febs.15185.Search in Google Scholar PubMed PubMed Central

Gouy, M., Guindon, S., and Gascuel, O. (2010). SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 27: 221–224, https://doi.org/10.1093/molbev/msp259.Search in Google Scholar PubMed

Hall, T.A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. 41: 95–98.Search in Google Scholar

Hernandez, M.A. and Alvarez, H.M. (2010). Glycogen formation by Rhodococcus species and the effect of inhibition of lipid biosynthesis on glycogen accumulation in Rhodococcus opacus PD630. FEMS Microbiol. Lett. 312: 93–99, https://doi.org/10.1111/j.1574-6968.2010.02108.x.Search in Google Scholar PubMed

Hernández, M.A., Mohn, W.W., Martínez, E., Rost, E., Alvarez, A.F., and Alvarez, H.M. (2008). Biosynthesis of storage compounds by Rhodococcus jostii RHA1 and global identification of genes involved in their metabolism. BMC Genomics 9: 600, https://doi.org/10.1186/1471-2164-9-600.Search in Google Scholar PubMed PubMed Central

Horcajada, C., Guinovart, J.J., Fita, I., and Ferrer, J.C. (2006). Crystal structure of an archaeal glycogen synthase: insights into oligomerization and substrate binding of eukaryotic glycogen synthases. J. Biol. Chem. 281: 2923–2931, https://doi.org/10.1074/jbc.M507394200.Search in Google Scholar PubMed

Jackson, M. and Brennan, P. (2009). Polymethylated polysaccharides from Mycobacterium species revisited. J. Biol. Chem. 284: 1949–1953, https://doi.org/10.1074/jbc.r800047200.Search in Google Scholar PubMed PubMed Central

Jarling, M., Cauvet, T., Grundmeier, M., Kuhnert, K., and Pape, H. (2004). Isolation of mak1 from Actinoplanes missouriensis and evidence that Pep2 from Streptomyces coelicolor is a maltokinase. J. Basic Microbiol. 44: 360–373, https://doi.org/10.1002/jobm.200410403.Search in Google Scholar PubMed

Jeanmougin, F., Thompson, J.D., Gouy, M., Higgins, D.G., and Gibson, T.J. (1998). Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23: 403–405, https://doi.org/10.1016/S0968-0004(98)01285-7.Search in Google Scholar

Kadouche, D., Ducatez, M., Cenci, U., Tirtiaux, C., Suzuki, E., Nakamura, Y., Putaux, J.-L., Terrasson, A.D., Diaz-Troya, S., Florencio, F.J., et al. (2016). Characterization of function of the GlgA2 glycogen/starch synthase in cyanobacterium sp. Clg1 highlights convergent evolution of glycogen metabolism into starch granule aggregation. Plant Physiol. 171: 1879–1892; https://doi.org/10.1104/pp.16.00049.Search in Google Scholar PubMed PubMed Central

Kalscheuer, R. and Jacobs, W.R. (2010). The significance of GlgE as a new target for tuberculosis. Drug News Perspect 23: 619–624, https://doi.org/10.1358/dnp.2010.23.10.1534855.Search in Google Scholar PubMed

Kalscheuer, R., Syson, K., Veeraraghavan, U., Weinrick, B., Biermann, K.E., Liu, Z., Sacchettini, J.C., Besra, G., Bornemann, S., and Jacobs, W.R. (2010). Self-poisoning of Mycobacterium tuberculosis by targeting GlgE in an alpha-glucan pathway. Nat. Chem. Biol. 6: 376–384, https://doi.org/10.1038/nchembio.340.Search in Google Scholar PubMed PubMed Central

Kaur, D., Pham, H., Larrouy-Maumus, G., Rivière, M., Vissa, V., Guerin, M.E., Puzo, G., Brennan, P.J., and Jackson, M. (2009). Initiation of methylglucose lipopolysaccharide biosynthesis in Mycobacteria. PLoS One 4: e5447, https://doi.org/10.1371/journal.pone.0005447.Search in Google Scholar PubMed PubMed Central

Koliwer-Brandl, H., Syson, K., van de Weerd, R., Chandra, G., Appelmelk, B., Alber, M., Ioerger, T.R., Jacobs, W.R.Jr., Geurtsen, J., Bornemann, S., et al.. (2016). Metabolic network for the biosynthesis of intra- and extracellular α-glucans required for virulence of Mycobacterium tuberculosis. PLoS Pathog. 12: e1005768, https://doi.org/10.1371/journal.ppat.1005768.Search in Google Scholar PubMed PubMed Central

Kopp, D. and Sunna, A. (2020). Alternative carbohydrate pathways–enzymes, functions and engineering. Crit. Rev. Biotechnol. 40: 895–912, https://doi.org/10.1080/07388551.2020.1785386.Search in Google Scholar PubMed

Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685, https://doi.org/10.1038/227680a0.Search in Google Scholar PubMed

Lanfranconi, M.P. and Alvarez, H.M. (2017). Rewiring neutral lipids production for the de novo synthesis of wax esters in Rhodococcus opacus PD630. J. Biotechnol. 260: 67–73, https://doi.org/10.1016/j.jbiotec.2017.09.009.Search in Google Scholar PubMed

Lewin, G.R., Carlos, C., Chevrette, M.G., Horn, H.A., McDonald, B.R., Stankey, R.J., Fox, B.G., and Currie, C.R. (2016). Evolution and ecology of Actinobacteria and their bioenergy applications. Annu. Rev. Microbiol. 70: 235–254, https://doi.org/10.1146/annurev-micro-102215-095748.Search in Google Scholar PubMed PubMed Central

Liu, Q.H., Tang, J.W., Wen, P.B., Wang, M.M., Zhang, X., and Wang, L. (2021). From prokaryotes to eukaryotes: insights into the molecular structure of glycogen particles. Front. Mol. Biosci. 8: 673315, https://doi.org/10.3389/fmolb.2021.673315.Search in Google Scholar PubMed PubMed Central

Maranha, A., Moynihan, P.J., Miranda, V., Correia Lourenço, E., Nunes-Costa, D., Fraga, J.S., Barbosa Pereira, J.P., MacEdo-Ribeiro, S., Ventura, M.R., Clarke, A.J., et al. (2015). Octanoylation of early intermediates of mycobacterial methylglucose lipopolysaccharides. Sci. Rep. 2015 51:1–18. https://doi.org/10.1038/srep13610.Search in Google Scholar PubMed PubMed Central

Marella, E.R., Holkenbrink, C., Siewers, V., and Borodina, I. (2018). Engineering microbial fatty acid metabolism for biofuels and biochemicals. Curr. Opin. Biotechnol. 50: 39–46, https://doi.org/10.1016/j.copbio.2017.10.002.Search in Google Scholar PubMed

Matsui, M., Kakut, M., and Misaki, A. (1996). Fine structural features of oyster glycogen: mode of multiple branching. Carbohydr. Polym. 31: 227–235, https://doi.org/10.1016/S0144-8617(96)00116-6.Search in Google Scholar

Matsui, M., Kakuta, M., and Misaki, A. (1993). Comparison of the unit-chain distributions of glycogens from different biological sources, revealed by anion exchange chromatography. Biosci. Biotechnol. Biochem. 57: 623–627, https://doi.org/10.1271/bbb.57.623.Search in Google Scholar

McLeod, M.P., Warren, R.L., Hsiao, W.W.L., Araki, N., Myhre, M., Fernandes, C., Miyazawa, D., Wong, W., Lillquist, A.L., Wang, D., et al. (2006). The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse. Proc. Natl. Acad. Sci. U.S.A. 103: 15582–15587, https://doi.org/10.1073/pnas.0607048103.Search in Google Scholar PubMed PubMed Central

Mendes, V., Maranha, A., Alarico, S., and Empadinhas, N. (2012). Biosynthesis of mycobacterial methylglucose lipopolysaccharides. Nat. Prod. Rep. 29: 834–844, https://doi.org/10.1039/C2NP20014G.Search in Google Scholar

Mendes, V., Maranha, A., Lamosa, P., da Costa, M.S., and Empadinhas, N. (2010). Biochemical characterization of the maltokinase from Mycobacterium bovis BCG. BMC Biochem. 11: 21, https://doi.org/10.1186/1471-2091-11-21.Search in Google Scholar PubMed PubMed Central

Mohan, A., Padiadpu, J., Baloni, P., and Chandra, N. (2015). Complete genome sequences of a Mycobacterium smegmatis laboratory strain (MC2 155) and isoniazid-resistant (4XR1/R2) mutant strains. Genome Announc. 3: e01520-14, https://doi.org/10.1128/genomea.01520-14.Search in Google Scholar PubMed PubMed Central

Moremen, K.W. and Haltiwanger, R.S. (2019). Emerging structural insights into glycosyltransferase-mediated synthesis of glycans. Nat. Chem. Biol. 15: 853, https://doi.org/10.1038/S41589-019-0350-2.Search in Google Scholar PubMed PubMed Central

Niehues, B., Jossek, R., Kramer, U., Koch, A., Jarling, M., Schröder, W., and Pape, H. (2003). Isolation and characterization of maltokinase (ATP:maltose 1-phosphotransferase) from Actinoplanes missouriensis. Arch. Microbiol. 180: 233–239, https://doi.org/10.1007/s00203-003-0575-y.Search in Google Scholar PubMed

Nouioui, I., Carro, L., García-López, M., Meier-Kolthoff, J.P., Woyke, T., Kyrpides, N.C., Pukall, R., Klenk, H.P., Goodfellow, M., and Göker, M. (2018). Genome-based taxonomic classification of the phylum Actinobacteria. Front. Microbiol. 9: 2007, https://doi.org/10.3389/fmicb.2018.02007.Search in Google Scholar PubMed PubMed Central

Nunes-Costa, D., Maranha, A., Costa, M., Alarico, S., and Empadinhas, N. (2017). Glucosylglycerate metabolism, bioversatility and mycobacterial survival. Glycobiology 27: 213–227, https://doi.org/10.1093/GLYCOB/CWW132.Search in Google Scholar

Palopoli, N., Busi, M.V., Fornasari, M.S., Gomez-Casati, D., Ugalde, R., and Parisi, G. (2006). Starch-synthase III family encodes a tandem of three starch-binding domains. Proteins Struct. Funct. Genet. 65: 27–31, https://doi.org/10.1002/prot.21007.Search in Google Scholar PubMed

Peracchi, A. (2018). The limits of enzyme specificity and the evolution of metabolism. Trends Biochem. Sci. 43: 984–996, https://doi.org/10.1016/j.tibs.2018.09.015.Search in Google Scholar PubMed

Preiss, J. (2009). Glycogen: biosynthesis and regulation. EcoSal Plus 3: 1–26, https://doi.org/10.1128/ecosalplus.4.7.4.Search in Google Scholar PubMed

Rashid, A.M., Batey, S.F.D., Syson, K., Koliwer-Brandl, H., Miah, F., Barclay, J.E., Findlay, K.C., Nartowski, K.P., Khimyak, Y.Z., Kalscheuer, R., et al. (2016). Assembly of α-glucan by GlgE and GlgB in mycobacteria and streptomycetes. Biochemistry 55: 3270–3284, https://doi.org/10.1021/acs.biochem.6b00209.Search in Google Scholar PubMed

Roach, P.J., Depaoli-Roach, A.A., Hurley, T.D., and Tagliabracci, V.S. (2012). Glycogen and its metabolism: some new developments and old themes. Biochem. J. 441: 763, https://doi.org/10.1042/bj20111416.Search in Google Scholar

Rosenberg, J. and Commichau, F.M. (2019). Harnessing underground metabolism for pathway development. Trends Biotechnol. 37: 29–37, https://doi.org/10.1016/j.tibtech.2018.08.001.Search in Google Scholar PubMed

Sambou, T., Dinadayala, P., Stadthagen, G., Barilone, N., Bordat, Y., Constant, P., Levillain, F., Neyrolles, O., Gicquel, B., Lemassu, A., et al. (2008). Capsular glucan and intracellular glycogen of Mycobacterium tuberculosis: biosynthesis and Impact on the Persistence in mice. Mol. Microbiol. 70: 762, https://doi.org/10.1111/J.1365-2958.2008.06445.X.Search in Google Scholar

Sheng, F., Jia, X., Yep, A., Preiss, J., and Geiger, J.H. (2009). The crystal structures of the open and catalytically competent closed conformation of Escherichia coli glycogen synthase. J. Biol. Chem. 284: 17796–17807, https://doi.org/10.1074/jbc.M809804200.Search in Google Scholar PubMed PubMed Central

Stadthagen, G., Sambou, T., Guerin, M., Barilone, N., Boudou, F., Korduláková, J., Charles, P., Alzari, P.M., Lemassu, A., Daffé, M., et al. (2007). Genetic basis for the biosynthesis of methylglucose lipopolysaccharides in Mycobacterium tuberculosis. J. Biol. Chem. 282: 27270–27276, https://doi.org/10.1074/jbc.M702676200.Search in Google Scholar PubMed

Stamler, R.A., Vereecke, D., Zhang, Y., Schilkey, F., Devitt, N., and Randall, J.J. (2016). Complete genome and plasmid sequences for Rhodococcus fascians D188 and draft sequences for Rhodococcus isolates PBTS 1 and PBTS 2. Genome Announc. 4: 495–511, https://doi.org/10.1128/genomea.00495-16.Search in Google Scholar PubMed PubMed Central

Syson, K., Stevenson, C.E.M., Lawson, D.M., and Bornemann, S. (2020). Structure of the Mycobacterium smegmatis a-maltose-1-phosphate synthase GlgM. Acta Crystallogr. Sec. F Struct. Biol. Commun. 76: 175–181, https://doi.org/10.1107/s2053230x20004343.Search in Google Scholar

Syson, K., Stevenson, C.E.M., Miah, F., Barclay, J.E., Tang, M., Gorelik, A., Rashid, A.M., Lawson, D.M., and Bornemann, S. (2016). Ligand-bound structures and site-directed mutagenesis identify the acceptor and secondary binding sites of Streptomyces coelicolor maltosyltransferase GlgE. J. Biol. Chem. 291: 21531–21540, https://doi.org/10.1074/jbc.m116.748160.Search in Google Scholar

Syson, K., Stevenson, C.E.M., Rashid, A.M., Saalbach, G., Tang, M., Tuukkanen, A., Svergun, D.I., Withers, S.G., Lawson, D.M., and Bornemann, S. (2014). Structural insight into how Streptomyces coelicolor maltosyl transferase GlgE binds α-maltose 1-phosphate and forms a maltosyl-enzyme intermediate. Biochemistry 53: 2494–2504, https://doi.org/10.1021/bi500183c.Search in Google Scholar PubMed PubMed Central

Tischler, D., Niescher, S., Kaschabek, S.R., and Schlömann, M. (2013). Trehalose phosphate synthases OtsA1 and OtsA2 of Rhodococcus opacus 1CP. FEMS Microbiol. Lett. 342: 113–122, https://doi.org/10.1111/1574-6968.12096.Search in Google Scholar PubMed

Valdez, H.A., Busi, M.V., Wayllace, N.Z., Parisi, G., Ugalde, R.A., and Gomez-Casati, D.F. (2008). Role of the N-terminal starch-binding domains in the kinetic properties of starch synthase III from Arabidopsis thaliana. Biochemistry 47: 3026–3032, https://doi.org/10.1021/bi702418h.Search in Google Scholar PubMed

van der Geize, R. and Dijkhuizen, L. (2004). Harnessing the catabolic diversity of rhodococci for environmental and biotechnological applications. Curr. Opin. Microbiol. 7: 255–261, https://doi.org/10.1016/j.mib.2004.04.001.Search in Google Scholar PubMed

van der Geize, R., Grommen, A.W.F., Hessels, G.I., Jacobs, A.A.C., and Dijkhuizen, L. (2011). The steroid catabolic pathway of the intracellular pathogen Rhodococcus equi is important for pathogenesis and a target for vaccine development. PLoS Pathog. 7: e1002181, https://doi.org/10.1371/journal.ppat.1002181.Search in Google Scholar PubMed PubMed Central

van der Geize, R., Yam, K., Heuser, T., Wilbrink, M.H., Hara, H., Anderton, M.C., Sim, E., Dijkhuizen, L., Davies, J.E., Mohn, W.W., et al. (2007). A gene cluster encoding cholesterol catabolism in a soil actinomycete provides insight into Mycobacterium tuberculosis survival in macrophages. Proc. Natl. Acad. Sci. U.S.A. 104: 1947–1952, https://doi.org/10.1073/pnas.0605728104/suppl_file/05728fig4.pdf.Search in Google Scholar

Verma, M., Lal, D., Kaur, J., Saxena, A., Kaur, J., Anand, S., and Lal, R. (2013). Phylogenetic analyses of phylum Actinobacteria based on whole genome sequences. Res. Microbiol. 164: 718–728, https://doi.org/10.1016/j.resmic.2013.04.002.Search in Google Scholar PubMed

Villar-Palasf, C. and Guinovart, J.J. (1997). The role of glucose 6-phosphate in the control of glycogen synthase. FASEB J. 11:544–58,https://doi.org/10.1096/fasebj.11.7.9212078.Search in Google Scholar

Wang, L., Wang, M., Wise, M.J., Liu, Q., Yang, T., Zhu, Z., Li, C., Tan, X., Tang, D., and Wang, W. (2020). Recent progress in the structure of glycogen serving as a durable energy reserve in bacteria. World J. Microbiol. Biotechnol. 36: 14, https://doi.org/10.1007/S11274-019-2795-6.Search in Google Scholar PubMed

Wedel, N. and Soll, J. (1998). Evolutionary conserved light regulation of Calvin cycle activity by NADPH-mediated reversible phosphoribulokinase/CP12/glyceraldehyde-3-phosphate dehydrogenase complex dissociation. Proc. Natl. Acad. Sci. U.S.A. 95: 9699–9704, https://doi.org/10.1073/pnas.95.16.9699.Search in Google Scholar PubMed PubMed Central

Wu, R., Asención Diez, M.D., Figueroa, C.M., Machtey, M., Iglesias, A.A., Ballicora, M.A., and Liu, D. (2015). The crystal structure of Nitrosomonas europaea sucrose synthase reveals critical conformational changes and insights into sucrose metabolism in prokaryotes. J. Bacteriol. 197: 2734–2746, https://doi.org/10.1128/JB.00110-15.Search in Google Scholar PubMed PubMed Central

Yep, A., Ballicora, M.A., and Preiss, J. (2006). The ADP-glucose binding site of the Escherichia coli glycogen synthase. Arch. Biochem. Biophys. 453: 188–196, https://doi.org/10.1016/j.abb.2006.07.003.Search in Google Scholar PubMed

Supplementary Material

This article contains supplementary material (https://doi.org/10.1515/hsz-2023-0339).

Received: 2023-11-02
Accepted: 2024-02-23
Published Online: 2024-03-15
Published in Print: 2024-05-27

© 2024 Walter de Gruyter GmbH, Berlin/Boston

Articles in the same Issue

  1. Frontmatter
  2. Research Articles/Short Communications
  3. Protein Structure and Function
  4. In-depth analysis of Gαs protein activity by probing different fluorescently labeled guanine nucleotides
  5. Biochemical evidence for conformational variants in the anti-viral and pro-metastatic protein IFITM1
  6. Study of two glycosyltransferases related to polysaccharide biosynthesis in Rhodococcus jostii RHA1
  7. Molecular Medicine
  8. KCTD5 regulates Ikaros degradation induced by chemotherapeutic drug etoposide in hematological cells
  9. Proteolysis
  10. Cathepsin X deficiency alters the processing and localisation of cathepsin L and impairs cleavage of a nuclear cathepsin L substrate
https://doi.org/10.1515/hsz-2023-0339
Keywords for this article
glycogen; methyl-glucose lipopolysaccharide; glucosamine-1P; glucose-1P; maltose-1P; gene redundancy

Articles in the same Issue

  1. Frontmatter
  2. Research Articles/Short Communications
  3. Protein Structure and Function
  4. In-depth analysis of Gαs protein activity by probing different fluorescently labeled guanine nucleotides
  5. Biochemical evidence for conformational variants in the anti-viral and pro-metastatic protein IFITM1
  6. Study of two glycosyltransferases related to polysaccharide biosynthesis in Rhodococcus jostii RHA1
  7. Molecular Medicine
  8. KCTD5 regulates Ikaros degradation induced by chemotherapeutic drug etoposide in hematological cells
  9. Proteolysis
  10. Cathepsin X deficiency alters the processing and localisation of cathepsin L and impairs cleavage of a nuclear cathepsin L substrate
Sign up now to receive a 20% welcome discount
Institutional Access
How does access work?
Have an idea on how to improve our website?
Please write us.
© 2025 De Gruyter Brill
Downloaded on 26.10.2025 from https://www.degruyterbrill.com/document/doi/10.1515/hsz-2023-0339/html
Scroll to top button