The virulome of in response to cello-oligosaccharide elicitors Open Access

Abstract

The development of spots or lesions symptomatic of common scab on root and tuber crops is caused by few pathogenic with 87–22 as the model species. Thaxtomin phytotoxins are the primary virulence determinants, mainly acting by impairing cellulose synthesis, and their production in is in turn boosted by cello-oligosaccharides released from host plants. In this work we aimed to determine which molecules and which biosynthetic gene clusters (BGCs) of the specialized metabolism of 87–22 show a production and/or a transcriptional response to cello-oligosaccharides. Comparative metabolomic analyses revealed that molecules of the virulome of induced by cellobiose and cellotriose include (i) thaxtomin and concanamycin phytotoxins, (ii) desferrioxamines, scabichelin and turgichelin siderophores in order to acquire iron essential for housekeeping functions, (iii) ectoine for protection against osmotic shock once inside the host, and (iv) bottromycin and concanamycin antimicrobials possibly to prevent other microorganisms from colonizing the same niche. Importantly, both cello-oligosaccharides reduced the production of the spore germination inhibitors germicidins thereby giving the ‘green light’ to escape dormancy and trigger the onset of the pathogenic lifestyle. For most metabolites - either with induced or reduced production - cellotriose was revealed to be a slightly stronger elicitor compared to cellobiose, supporting an earlier hypothesis which suggested the trisaccharide was the real trigger for virulence released from the plant cell wall through the action of thaxtomins. Interestingly, except for thaxtomins, none of these BGCs’ expression seems to be under direct control of the cellulose utilization repressor CebR suggesting the existence of a yet unknown mechanism for switching on the virulome. Finally, a transcriptomic analysis revealed nine additional cryptic BGCs that have their expression awakened by cello-oligosaccharides, suggesting that other and yet to be discovered metabolites could be part of the virulome of .

Funding
This study was supported by the:
  • Bijzonder Onderzoeksfonds (Award grant 01B08915)
    • Principle Award Recipient: BartDevreese
  • Fonds pour la Formation à la Recherche dans l’Industrie et dans l’Agriculture (Award FRIA 1.E.116.21)
    • Principle Award Recipient: NudzejmaStulanovic
  • Fonds De La Recherche Scientifique - FNRS (Award FRIA 1.E.031.18-20)
    • Principle Award Recipient: SinaedaAnderssen
  • Fonds De La Recherche Scientifique - FNRS (Award grant 1.A618.18)
    • Principle Award Recipient: BenoitDeflandre
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000760
2022-01-17
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/mgen/8/1/mgen000760.html?itemId=/content/journal/mgen/10.1099/mgen.0.000760&mimeType=html&fmt=ahah

References

  1. Goyer C, Beaulieu C. Host range of streptomycete strains causing common scab. Plant Dis 1997; 81:901–904 [View Article] [PubMed]
    [Google Scholar]
  2. Loria R, Bukhalid RA, Fry BA, King RR. Plant pathogenicity in the genus streptomyces. Plant Dis 1997; 81:836–846 [View Article] [PubMed]
    [Google Scholar]
  3. Wanner LA, Kirk WW. Streptomyces – from basic microbiology to role as a plant pathogen. Am J Potato Res 2015; 92:236–242 [View Article]
    [Google Scholar]
  4. King RR, Lawrence CH, Clark MC. Correlation of phytotoxin production with pathogenicity ofStreptomyces scabies isolates from scab infected potato tubers. American Potato Journal 1991; 68:675–680 [View Article]
    [Google Scholar]
  5. Healy FG, Wach M, Krasnoff SB, Gibson DM, Loria R. The txtAB genes of the plant pathogen Streptomyces acidiscabies encode a peptide synthetase required for phytotoxin thaxtomin A production and pathogenicity. Mol Microbiol 2000; 38:794–804 [View Article] [PubMed]
    [Google Scholar]
  6. King RR, Calhoun LA. The thaxtomin phytotoxins: Sources, synthesis, biosynthesis, biotransformation and biological activity. Phytochemistry 2009; 70:833–841 [View Article] [PubMed]
    [Google Scholar]
  7. Loria R, Bignell DRD, Moll S, Huguet-Tapia JC, Joshi MV et al. Thaxtomin biosynthesis: the path to plant pathogenicity in the genus Streptomyces. Antonie Van Leeuwenhoek 2008; 94:3–10 [View Article]
    [Google Scholar]
  8. Bischoff V, Cookson SJ, 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 2009; 60:955–965 [View Article]
    [Google Scholar]
  9. Duval I, Beaudoin N. Transcriptional profiling in response to inhibition of cellulose synthesis by thaxtomin a and isoxaben in arabidopsis thaliana suspension cells. Plant Cell Rep 2009; 28:811–830 [View Article]
    [Google Scholar]
  10. Tateno M, Brabham C, DeBolt S. Cellulose biosynthesis inhibitors – a multifunctional toolbox. EXBOTJ 2016; 67:533–542 [View Article] [PubMed]
    [Google Scholar]
  11. Li Y, Liu J, Díaz-Cruz G, Cheng Z, Bignell DRD. Virulence mechanisms of plant-pathogenic Streptomyces species: an updated review. Microbiology (Reading) 2019; 165:1025–1040 [View Article] [PubMed]
    [Google Scholar]
  12. Khatri BB, Tegg RS, Brown PH, Wilson CR. Temporal association of potato tuber development with susceptibility to common scab and Streptomyces scabiei-induced responses in the potato periderm. Plant Pathol 2011; 60:776–786 [View Article]
    [Google Scholar]
  13. Natsume M, Tashiro N, Doi A, Nishi Y, Kawaide H. Effects of concanamycins produced by Streptomyces scabies on lesion type of common scab of potato. J Gen Plant Pathol 2017; 83:78–82 [View Article]
    [Google Scholar]
  14. Gimenez-Ibanez S, Chini A, Solano R. How microbes twist jasmonate signaling around their little fingers. Plants (Basel) 2016; 5:323–329 [View Article] [PubMed]
    [Google Scholar]
  15. Fyans JK, Altowairish MS, Li Y, Bignell DRD. Characterization of the coronatine-like phytotoxins produced by the common scab pathogen Streptomyces scabies . Mol Plant Microbe Interact 2015; 28:443–454 [View Article] [PubMed]
    [Google Scholar]
  16. Bignell DRD, Cheng Z, Bown L. The coronafacoyl phytotoxins: structure, biosynthesis, regulation and biological activities. Antonie Van Leeuwenhoek 2018; 111:649–666 [View Article] [PubMed]
    [Google Scholar]
  17. Planckaert S, Deflandre B, de Vries A-M, Ameye M, Martins JC et al. Identification of novel rotihibin analogues in Streptomyces scabies, including discovery of its biosynthetic gene cluster. Microbiol Spectr 2021; 9:e0057121 [View Article] [PubMed]
    [Google Scholar]
  18. Arias AA, Lambert S, Martinet L, Adam D, Tenconi E et al. Growth of desferrioxamine-deficient Streptomyces mutants through xenosiderophore piracy of airborne fungal contaminations. FEMS Microbiology Ecology 2015; 91:fiv080 [View Article]
    [Google Scholar]
  19. Kodani S, Bicz J, Song L, Deeth RJ, Ohnishi-Kameyama M et al. Structure and biosynthesis of scabichelin, a novel tris-hydroxamate siderophore produced by the plant pathogen Streptomyces scabies 87.22. Org Biomol Chem 2013; 11:4686–4694 [View Article] [PubMed]
    [Google Scholar]
  20. Seipke RF, Song L, Bicz J, Laskaris P, Yaxley AM et al. The plant pathogen Streptomyces scabies 87-22 has a functional pyochelin biosynthetic pathway that is regulated by TetR- and AfsR-family proteins. Microbiology (Reading) 2011; 157:2681–2693 [View Article] [PubMed]
    [Google Scholar]
  21. 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 1999; 65:2636–2643 [View Article] [PubMed]
    [Google Scholar]
  22. Francis IM, Jourdan S, Fanara S, Loria R, Rigali S. The cellobiose sensor CebR is the gatekeeper of Streptomyces scabies pathogenicity. mBio 2015; 6:e02018 [View Article] [PubMed]
    [Google Scholar]
  23. Jourdan S, Francis IM, Kim MJ, Salazar JJC, Planckaert S et al. The CebE/MsiK transporter is a doorway to the cello-oligosaccharide-mediated induction of Streptomyces scabies pathogenicity. Sci Rep 2016; 6:27144 [View Article] [PubMed]
    [Google Scholar]
  24. Joshi MV, Bignell DRD, Johnson EG, Sparks JP, Gibson DM et al. The AraC/XylS regulator TxtR modulates thaxtomin biosynthesis and virulence in Streptomyces scabies . Mol Microbiol 2007; 66:633–642 [View Article] [PubMed]
    [Google Scholar]
  25. Johnson EG, Joshi MV, Gibson DM, Loria R. Cello-oligosaccharides released from host plants induce pathogenicity in scab-causing Streptomyces species. Physiological and Molecular Plant Pathology 2007; 71:18–25 [View Article]
    [Google Scholar]
  26. Book AJ, Lewin GR, McDonald BR, Takasuka TE, Wendt-Pienkowski E et al. Evolution of high cellulolytic activity in symbiotic streptomyces through selection of expanded gene content and coordinated gene expression. PLoS Biol 2016; 14:1–21 [View Article] [PubMed]
    [Google Scholar]
  27. Jourdan S, Francis IM, Deflandre B, Loria R, Rigali S. Tracking the Subtle Mutations Driving Host Sensing by the Plant Pathogen. Streptomyces scabies 2020; 2:1 [View Article] [PubMed]
    [Google Scholar]
  28. Jourdan S, Francis IM, Deflandre B, Tenconi E, Riley J et al. Contribution of the β-glucosidase BglC to the onset of the pathogenic lifestyle of Streptomyces scabies. Mol Plant Pathol 2018; 19:1480–1490 [View Article] [PubMed]
    [Google Scholar]
  29. Liu J, Nothias L-F, Dorrestein PC, Tahlan K, Bignell DRD. Genomic and Metabolomic Analysis of the Potato Common Scab Pathogen. Streptomyces scabiei ACS Omega 2021; 6:11474–11487 [View Article] [PubMed]
    [Google Scholar]
  30. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  31. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article] [PubMed]
    [Google Scholar]
  32. Langmead B, Wilks C, Antonescu V, Charles R. Scaling read aligners to hundreds of threads on general-purpose processors. Bioinformatics 2019; 35:421–432 [View Article] [PubMed]
    [Google Scholar]
  33. Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 2014; 30:923–930 [View Article] [PubMed]
    [Google Scholar]
  34. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 2014; 15:1–21 [View Article] [PubMed]
    [Google Scholar]
  35. Adams KJ, Pratt B, Bose N, Dubois LG, St John-Williams L et al. Skyline for small molecules: a unifying software package for quantitative metabolomics. J Proteome Res 2020; 19:1447–1458 [View Article] [PubMed]
    [Google Scholar]
  36. Blin K, Shaw S, Steinke K, Villebro R, Ziemert N et al. antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 2019; 47:W81–W87 [View Article] [PubMed]
    [Google Scholar]
  37. Kautsar SA, Blin K, Shaw S, Navarro-Muñoz JC, Terlouw BR et al. MIBiG 2.0: a repository for biosynthetic gene clusters of known function. Nucleic Acids Res 2020; 48:D454–D458 [View Article] [PubMed]
    [Google Scholar]
  38. Vicente CM, Thibessard A, Lorenzi J-N, Benhadj M, Hôtel L et al. Comparative genomics among closely related Streptomyces strains revealed specialized metabolite biosynthetic gene cluster diversity. Antibiotics (Basel) 2018; 7:1–11 [View Article] [PubMed]
    [Google Scholar]
  39. Omura S, Shimizu H, Iwai Y, Hinotozawa K, Otoguro K et al. AM-2604 A, a new antiviral antibiotic produced by a strain of Streptomyces . J Antibiot 1982; 35:1632–1637 [View Article]
    [Google Scholar]
  40. Dröse S, Altendorf K. Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases. J Exp Biol 1997; 200:1–8 [View Article] [PubMed]
    [Google Scholar]
  41. Dröse S, Bindseil KU, Bowman EJ, Siebers A, Zeeck A et al. Inhibitory effect of modified bafilomycins and concanamycins on P- and V-type adenosinetriphosphatases. Biochemistry 1993; 32:3902–3906 [View Article] [PubMed]
    [Google Scholar]
  42. Hoskisson PA, Seipke RF. Cryptic or silent? the known unknowns, unknown knowns, and unknown unknowns of secondary metabolism. mBio 2020; 11:1–5 [View Article] [PubMed]
    [Google Scholar]
  43. Deflandre B, Thiébaut N, Planckaert S, Jourdan S, Anderssen S et al. Deletion of bglC triggers a genetic compensation response by awakening the expression of alternative beta-glucosidase. Biochim Biophys Acta Gene Regul Mech 2020; 1863:194615 [View Article] [PubMed]
    [Google Scholar]
  44. Bignell DRD, Seipke RF, Huguet-Tapia JC, Chambers AH, Parry RJ et al. Streptomyces scabies 87-22 contains a coronafacic acid-like biosynthetic cluster that contributes to plant-microbe interactions. Mol Plant Microbe Interact 2010; 23:161–175 [View Article] [PubMed]
    [Google Scholar]
  45. Spohn M, Edenhart S, Alanjary M, Ziemert N, Wibberg D et al. Identification of a novel aminopolycarboxylic acid siderophore gene cluster encoding the biosynthesis of ethylenediaminesuccinic acid hydroxyarginine (EDHA). Metallomics 2018; 10:722–734 [View Article] [PubMed]
    [Google Scholar]
  46. Lambert S, Traxler MF, Craig M, Maciejewska M, Ongena M et al. Altered desferrioxamine-mediated iron utilization is a common trait of bald mutants of Streptomyces coelicolor. Metallomics 2014; 6:1390–1399 [View Article] [PubMed]
    [Google Scholar]
  47. Yamanaka K, Oikawa H, Ogawa H-O, Hosono K, Shinmachi F et al. Desferrioxamine E produced by Streptomyces griseus stimulates growth and development of Streptomyces tanashiensis. Microbiology (Reading) 2005; 151:2899–2905 [View Article] [PubMed]
    [Google Scholar]
  48. Traxler MF, Seyedsayamdost MR, Clardy J, Kolter R. Interspecies modulation of bacterial development through iron competition and siderophore piracy. Mol Microbiol 2012; 86:628–644 [View Article] [PubMed]
    [Google Scholar]
  49. Craig M, Lambert S, Jourdan S, Tenconi E, Colson S et al. Unsuspected control of siderophore production by N-acetylglucosamine in streptomycetes. Environ Microbiol Rep 2012; 4:512–521 [View Article] [PubMed]
    [Google Scholar]
  50. Planckaert S, Jourdan S, Francis IM, Deflandre B, Rigali S et al. Proteomic response to thaxtomin phytotoxin elicitor cellobiose and to deletion of cellulose utilization regulator CebR in Streptomyces scabies . J Proteome Res 2018; 17:3837–3852 [View Article] [PubMed]
    [Google Scholar]
  51. Bignell DRD, Huguet-Tapia JC, Joshi MV, Pettis GS, Loria R. What does it take to be a plant pathogen: genomic insights from Streptomyces species. Antonie van Leeuwenhoek 2010; 98:179–194 [View Article] [PubMed]
    [Google Scholar]
  52. Świątek-Połatyńska MA, Bucca G, Laing E, Gubbens J, Titgemeyer F et al. Genome-wide analysis of in vivo binding of the master regulator DasR in Streptomyces coelicolor identifies novel non-canonical targets. PLoS One 2015; 10:1–24 [View Article] [PubMed]
    [Google Scholar]
  53. Komatsu M, Tsuda M, Omura S, Oikawa H, Ikeda H. Identification and functional analysis of genes controlling biosynthesis of 2-methylisoborneol. Proc Natl Acad Sci U S A 2008; 105:7422–7427 [View Article] [PubMed]
    [Google Scholar]
  54. Seipke RF, Loria R. Hopanoids are not essential for growth of Streptomyces scabies 87-22. J Bacteriol 2009; 191:5216–5223 [View Article] [PubMed]
    [Google Scholar]
  55. Jiang J, He X, Cane DE. Biosynthesis of the earthy odorant geosmin by a bifunctional Streptomyces coelicolor enzyme. Nat Chem Biol 2007; 3:711–715 [View Article] [PubMed]
    [Google Scholar]
  56. Bignell DRD, Fyans JK, Cheng Z. Phytotoxins produced by plant pathogenic Streptomyces species. J Appl Microbiol 2014; 116:223–235 [View Article] [PubMed]
    [Google Scholar]
  57. Vior NM, Cea-Torrescassana E, Eyles TH, Chandra G, Truman AW. Regulation of bottromycin biosynthesis involves an internal transcriptional start site and a cluster-situated modulator. Front Microbiol 2020; 11:1–16 [View Article] [PubMed]
    [Google Scholar]
  58. Beauséjour J, Beaulieu C. Characterization of Streptomyces scabies mutants deficient in melanin biosynthesis. Can J Microbiol 2004; 50:705–709 [View Article] [PubMed]
    [Google Scholar]
  59. Bursy J, Kuhlmann AU, Pittelkow M, Hartmann H, Jebbar M et al. Synthesis and uptake of the compatible solutes ectoine and 5-hydroxyectoine by Streptomyces coelicolor A3(2) in response to salt and heat stresses. Appl Environ Microbiol 2008; 74:7286–7296 [View Article] [PubMed]
    [Google Scholar]
  60. Bown L, Li Y, Berrué F, Verhoeven JTP, Dufour SC et al. Coronafacoyl phytotoxin biosynthesis and evolution in the common scab pathogen Streptomyces scabiei . Appl Environ Microbiol 2017; 83:1–15 [View Article] [PubMed]
    [Google Scholar]
  61. Chemler JA, Buchholz TJ, Geders TW, Akey DL, Rath CM et al. Biochemical and structural characterization of germicidin synthase: analysis of a type III polyketide synthase that employs acyl-ACP as a starter unit donor. J Am Chem Soc 2012; 134:7359–7366 [View Article] [PubMed]
    [Google Scholar]
  62. Haydock SF, Appleyard AN, Mironenko T, Lester J, Scott N et al. Organization of the biosynthetic gene cluster for the macrolide concanamycin A in Streptomyces neyagawaensis ATCC 27449. Microbiology (Reading) 2005; 151:3161–3169 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000760
Loading
/content/journal/mgen/10.1099/mgen.0.000760
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed