The CebE/MsiK Transporter is a Doorway to the Cello-oligosaccharide-mediated Induction of Streptomyces scabies Pathogenicity

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Jourdan, Samuel ^a   Francis, Isolde Maria ^b,c   Kim, Min Jung ^c   Salazar, Joren Jeico C ^b   Planckaert, Sören ^d   Frère, Jean Marie ^a   Matagne, André ^a   Kerff, Frédéric ^a   Devreese, Bart ^d   Loria, Rosemary ^c   Rigali, Sébastien ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b CALIFORNIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

^d GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; CELLOBIOSE; INDOLE DERIVATIVE; MSIK PROTEIN, STREPTOMYCES; OLIGOSACCHARIDE; PIPERAZINE DERIVATIVE; PLANT PROTEIN; THAXTOMINE A;

GENE EXPRESSION REGULATION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYLOGENY; PLANT DISEASE; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; STREPTOMYCES;

ADENOSINE TRIPHOSPHATASES; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; CELLOBIOSE; GENE EXPRESSION REGULATION, BACTERIAL; INDOLES; OLIGOSACCHARIDES; PHYLOGENY; PIPERAZINES; PLANT DISEASES; PLANT PROTEINS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; STREPTOMYCES;

EID: 84973277679     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep27144     Document Type: Article

References (43)

1. Hopwood, D. A. Streptomyces in Nature and Medicine: The Antibiotic Makers. (Oxford University Press, 2007).
2. Hodgson, D. A. Primary metabolism and its control in streptomycetes: a most unusual group of bacteria. Adv. Microb. Physiol. 42, 47-238 (2000).
3. Bertram, R. et al. In silico and transcriptional analysis of carbohydrate uptake systems of Streptomyces coelicolor A3(2). J. Bacteriol. 186, 1362-73 (2004).
4. Francis, I., Holsters, M. & Vereecke, D. The Gram-positive side of plant-microbe interactions. Environ. Microbiol. 12, 1-12 (2010).
5. Kinkel, L. L., Schlatter, D. C., Bakker, M. G. & Arenz, B. E. Streptomyces competition and co-evolution in relation to plant disease suppression. Res. Microbiol. 163, 490-499 (2012).
6. Seipke, R. F., Kaltenpoth, M. & Hutchings, M. I. Streptomyces as symbionts: An emerging and widespread theme? FEMS Microbiol. Rev. 36, 862-876 (2012).
7. Loria, R., Kers, J. & Joshi, M. Evolution of plant pathogenicity in Streptomyces. Annu. Rev. Phytopathol. 44, 469-487 (2006).
8. Scheible, W.-R. et al. An Arabidopsis mutant resistant to thaxtomin A, a cellulose synthesis inhibitor from Streptomyces species. Plant Cell 15, 1781-1794 (2003).
9. Bischoff, V., Cookson, S. J., Wu, S. & Scheible, W. R. Thaxtomin A affects CESA-complex density, expression of cell wall genes, cell wall composition, and causes ectopic lignification in Arabidopsis thaliana seedlings. J. Exp. Bot. 60, 955-965 (2009).
10. Bignell, D. R. D., Francis, I. M., Fyans, J. K. & Loria, R. Thaxtomin A production and virulence are controlled by several bld gene global regulators in Streptomyces scabies. Mol. Plant. Microbe. Interact. 27, 875-85 (2014).
11. Joshi, M. V. et al. The AraC/XylS regulator TxtR modulates thaxtomin biosynthesis and virulence in Streptomyces scabies. Mol. Microbiol. 66, 633-642 (2007).
12. Francis, I. M., Jourdan, S., Fanara, S., Loria, R. & Rigali, S. The cellobiose sensor CebR is the gatekeeper of Streptomyces scabies pathogenicity. MBio 6, e02018 (2015).
13. Johnson, E. G., Joshi, M. V., Gibson, D. M. & Loria, R. Cello-oligosaccharides released from host plants induce pathogenicity in scab-causing Streptomyces species. Physiol. Mol. Plant Pathol. 71, 18-25 (2007).
14. Schlösser, a. & Schrempf, H. A lipid-anchored binding protein is a component of an ATP-dependent cellobiose/cellotriose-transport system from the cellulose degrader Streptomyces reticuli. Eur. J. Biochem. 242, 332-338 (1996).
15. Schlösser, A., Jantos, J., Hackmann, K. & Schrempf, H. Characterization of the binding protein-dependent cellobiose and cellotriose transport system of the cellulose degrader Streptomyces reticuli. Appl. Environ. Microbiol. 65, 2636-2643 (1999).
16. Schlosser, a., Kampers, T. & Schrempf, H. The Streptomyces ATP-binding component MsiK assists in cellobiose and maltose transport. J. Bacteriol. 179, 2092-2095 (1997).
17. Kos, V. & Ford, R. C. The ATP-binding cassette family: A structural perspective. Cell. Mol. Life Sci. 66, 3111-3126 (2009).
18. Hurtubise, Y., Shareck, F., Kluepfel, D. & Morosoli, R. A cellulase/xylanase-negative mutant of Streptomyces lividans 1326 defective in cellobiose and xylobiose uptake is mutated in a gene encoding a protein homologous to ATP-binding proteins. Mol. Microbiol. 17, 367-77 (1995).
19. Saito, A. et al. The msiK gene, encoding the ATP-hydrolysing component of N,N'-diacetylchitobiose ABC transporters, is essential for induction of chitinase production in Streptomyces coelicolor A3(2). Microbiology 154, 3358-65 (2008).
20. Viens, P. et al. Uptake of chitosan-derived D-glucosamine oligosaccharides in Streptomyces coelicolor A3(2). FEMS Microbiol. Lett. 362 (2015).
21. Despalins, A., Marsit, S. & Oberto, J. Absynte: a web tool to analyze the evolution of orthologous archaeal and bacterial gene clusters. Bioinformatics 27, 2905-6 (2011).
22. Marushima, K., Ohnishi, Y. & Horinouchi, S. CebR as a master regulator for cellulose/cellooligosaccharide catabolism affects morphological development in Streptomyces griseus. J. Bacteriol. 191, 5930-5940 (2009).
23. Schlösser, A., Aldekamp, T. & Schrempf, H. Binding characteristics of CebR, the regulator of the ceb operon required for cellobiose/ cellotriose uptake in Streptomyces reticuli. FEMS Microbiol. Lett. 190, 127-132 (2000).
24. Lerat, S., Simao-Beaunoir, A.-M., Wu, R., Beaudoin, N. & Beaulieu, C. Involvement of the plant polymer Suberin and the disaccharide cellobiose in triggering thaxtomin A biosynthesis, a phytotoxin produced by the pathogenic agent streptomyces scabies. Phytopathology 100, 91-96 (2010).
25. Krieger, E. & Vriend, G. YASARA View-molecular graphics for all devices-from smartphones to workstations. Bioinformatics 30, 2981-2 (2014).
26. Loria, R., Bukhalid, R. A., Fry, B. A. & King, R. R. PLANT PATHOGENICITY IN THE GENUS STREPTOMYCES. Plant Dis. 81, 836-846 (1997).
27. Cangelosi, G. a, Ankenbauer, R. G. & Nester, E. W. Sugars induce the Agrobacterium virulence genes through a periplasmic binding protein and a transmembrane signal protein. Proc. Natl. Acad. Sci. USA 87, 6708-6712 (1990).
28. Hu, X., Zhao, J., DeGrado, W. F. & Binns, A. N. Agrobacterium tumefaciens recognizes its host environment using ChvE to bind diverse plant sugars as virulence signals. Proc. Natl. Acad. Sci. USA 110, 678-83 (2013).
29. Kemner, J. M., Liang, X. & Nester, E. W. The Agrobacterium tumefaciens virulence gene chvE is part of a putative ABC-type sugar transport operon. J. Bacteriol. 179, 2452-8 (1997).
30. He, F. et al. Molecular basis of ChvE function in sugar binding, sugar utilization, and virulence in Agrobacterium tumefaciens. J. Bacteriol. 191, 5802-5813 (2009).
31. Subramoni, S., Nathoo, N., Klimov, E. & Yuan, Z.-C. Agrobacterium tumefaciens responses to plant-derived signaling molecules. Front. Plant Sci. 5, 322 (2014).
32. Lawlor, E. J. & Baylis, H. a. & Chater, K. F. Pleiotropic morphological and antibiotic deficiencies result from mutations in a gene encoding a tRNA-like product in Streptomyces coelicolor A3(2). Genes Dev. 1, 1305-1310 (1987).
33. Lauzier, A. et al. Effect of potato suberin on Streptomyces scabies proteome. Mol. Plant Pathol. 9, 753-762 (2008).
34. Padilla-Reynaud, R., Simao-Beaunoir, A.-M., Lerat, S., Bernards, M. A. & Beaulieu, C. Suberin Regulates the Production of Cellulolytic Enzymes in Streptomyces scabiei, the Causal Agent of Potato Common Scab. Microbes Environ. 30, 245-53 (2015).
35. Komeil, D., Padilla-Reynaud, R., Lerat, S., Simao-Beaunoir, A.-M. & Beaulieu, C. Comparative secretome analysis of Streptomyces scabiei during growth in the presence or absence of potato suberin. Proteome Sci. 12, 35 (2014).
36. Gust, B., Challis, G. L., Fowler, K., Kieser, T. & Chater, K. F. PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc. Natl. Acad. Sci. USA 100, 1541-6 (2003).
37. Tenconi, E., Guichard, P., Motte, P., Matagne, A. & Rigali, S. Use of red autofluorescence for monitoring prodiginine biosynthesis. J. Microbiol. Methods 93, 138-13 (2013).
38. Devos, S. et al. The effect of imipenem and diffusible signaling factors on the secretion of outer membrane vesicles and associated Ax21 proteins in Stenotrophomonas maltophilia. Front. Microbiol. 6, 298 (2015).
39. Dereeper, A. et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36, 465-469 (2008).
40. Hiard, S. et al. PREDetector: A new tool to identify regulatory elements in bacterial genomes. Biochem. Biophys. Res. Commun. 357, 861-864 (2007).
41. Rigali, S., Nivelle, R. & Tocquin, P. On the necessity and biological significance of threshold-free regulon prediction outputs. Mol. BioSyst. 11, 333-337 (2015).
42. Kieser, T., Bibb, M. J., Buttner, M. J., Chater, K. F. & Hopwood, D. a. Practical Streptomyces Genetics. John Innes Centre Ltd. doi: 10.4016/28481.01 (2000).
43. Loria, R. et al. Differential Production of Thaxtomins by Pathogenic Streptomyces Species in Vitro. Phytopathology 85, 537-541 (1995).