1887

Abstract

is one of the major model systems in biology based on advantageous properties such as short life span, transparency, genetic tractability and ease of culture using an diet. In its natural habitat, compost and rotting plant material, this nematode lives on bacteria. However, is a predator of bacteria, but can also be infected by nematopathogenic coryneform bacteria such and species, which display intriguing and diverse modes of pathogenicity. Depending on the nematode pathogen, aggregates of worms, termed worm-stars, can be formed, or severe rectal swelling, so-called Dar formation, can be induced. Using the human and animal pathogens and as well as the non-pathogenic species , we show that these coryneform bacteria can also induce star formation slowly in worms, as well as a severe tail-swelling phenotype. While had a significant, but minor influence on survival of , nematodes were killed after infection with and . The two pathogenic species were avoided by the nematodes and induced aversive learning in .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000201
2016-01-01
2020-01-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/162/1/84.html?itemId=/content/journal/micro/10.1099/mic.0.000201&mimeType=html&fmt=ahah

References

  1. Abe S., Takayama K., Kinoshita S.. 1967; Taxonomical studies on glutamic acid producing bacteria. J Gen Microbiol13:279–301 [CrossRef]
    [Google Scholar]
  2. Akimkina T., Yook K., Curnock S., Hodgkin J.. 2006; Genome characterization, analysis of virulence and transformation of Microbacterium nematophilum, a coryneform pathogen of the nematode Caenorhabditis elegans . FEMS Microbiol Lett264:145–151 [CrossRef][PubMed]
    [Google Scholar]
  3. Antunes C. A., Sanches dos Santos L., Hacker E., Köhler S., Bösl K., Ott L., de Luna M., Hirata R. Jr, Azevedo V. A., other authors. 2015; Characterization of DIP0733, a multi-functional virulence factor of Corynebacterium diphtheriae . Microbiology161:639–647 [CrossRef][PubMed]
    [Google Scholar]
  4. Becker J., Wittmann C.. 2012; Bio-based production of chemicals, materials and fuels - Corynebacterium glutamicum as versatile cell factory. Curr Opin Biotechnol23:631–640 [CrossRef][PubMed]
    [Google Scholar]
  5. Bernard K.. 2012; The genus Corynebacterium and other medically relevant coryneform-like bacteria. J Clin Microbiol50:3152–3158 [CrossRef][PubMed]
    [Google Scholar]
  6. Brenner S.. 1974; The genetics of Caenorhabditis elegans . Genetics77:71–94[PubMed]
    [Google Scholar]
  7. Broadway M. M., Rogers E. A., Chang C., Huang I. H., Dwivedi P., Yildirim S., Schmitt M. P., Das A., Ton-That H.. 2013; Pilus gene pool variation and the virulence of Corynebacterium diphtheriae clinical isolates during infection of a nematode. J Bacteriol195:3774–3783 [CrossRef][PubMed]
    [Google Scholar]
  8. Burkovski A.. 2013a; Diphtheria. In The Prokaryotes, 4th ed.vol 5 pp237–246 Edited by Rosenberg E., DeLong E. F., Thompson F., Lory S., Stackebrandt E.. New York: Springer;[CrossRef]
    [Google Scholar]
  9. Burkovski A.. 2013b; Cell envelope of corynebacteria: structure and influence on pathogenicity. ISRN Microbiol2013:935736 [CrossRef][PubMed]
    [Google Scholar]
  10. Burkovski A.. 2014; Diphtheria and its etiological agents. In Corynebacterium Diphtheriae and Related Toxigenic Species pp1–14 Edited by Burkovski A.. Dordrecht: [CrossRef] Springer;
    [Google Scholar]
  11. Burkovski A.. 2015; Corynebacterium Glutamicum: From Systems Biology to Biotechnological Applications Norfolk: Caister Academic Press;
    [Google Scholar]
  12. Chen J., Caswell-Chen E. P.. 2003; Why Caenorhabditis elegans adults sacrifice their bodies to progeny. Nematology5:641–645 [CrossRef]
    [Google Scholar]
  13. Clark L. C., Hodgkin J.. 2014; Commensals, probiotics and pathogens in the Caenorhabditis elegans model. Cell Microbiol16:27–38 [CrossRef][PubMed]
    [Google Scholar]
  14. de Bono M., Bargmann C. I.. 1998; Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans . Cell94:679–689 [CrossRef][PubMed]
    [Google Scholar]
  15. Gravato-Nobre M. J., Nicholas H. R., Nijland R., O'Rourke D., Whittington D. E., Yook K. J., Hodgkin J.. 2005; Multiple genes affect sensitivity of Caenorhabditis elegans to the bacterial pathogen Microbacterium nematophilum . Genetics171:1033–1045 [CrossRef][PubMed]
    [Google Scholar]
  16. Hodgkin J., Kuwabara P. E., Corneliussen B.. 2000; A novel bacterial pathogen, Microbacterium nematophilum, induces morphological change in the nematode C. elegans . Curr Biol10:1615–1618 [CrossRef][PubMed]
    [Google Scholar]
  17. Hodgkin J., Félix M. A., Clark L. C., Stroud D., Gravato-Nobre M. J.. 2013; Two Leucobacter strains exert complementary virulence on Caenorhabditis including death by worm-star formation. Curr Biol23:2157–2161 [CrossRef][PubMed]
    [Google Scholar]
  18. Kinoshita S., Udaka S., Shimono M.. 1957; Studies on the amino acid fermentation: I. Production of l-glutamic acid by various microorganism. J Gen Appl Microbiol3:193–205 [CrossRef]
    [Google Scholar]
  19. Mattos Guaraldi A. L., Hirata R. Jr, Azevedo V.A.C.. 2014; Corynebacterium diphtheriae, Corynebacterium ulcerans and Corynebacterium pseudotuberculosis-General Aspects. In Corynebacterium Diphtheriae and Related Toxigenic Species pp15–37 Edited by Burkovski A.. Dordrecht: [CrossRef] Springer;
    [Google Scholar]
  20. Mosser T., Matic I., Leroy M.. 2011; Bacterium-induced internal egg hatching frequency is predictive of life span in Caenorhabditis elegans populations. Appl Environ Microbiol77:8189–8192 [CrossRef][PubMed]
    [Google Scholar]
  21. Ott L., Höller M., Rheinlaender J., Schäffer T. E., Hensel M., Burkovski A.. 2010; Strain-specific differences in pili formation and the interaction of Corynebacterium diphtheriae with host cells. BMC Microbiol10:257 [CrossRef][PubMed]
    [Google Scholar]
  22. Ott L., McKenzie A., Baltazar M. T., Britting S., Bischof A., Burkovski A., Hoskisson P. A.. 2012; Evaluation of invertebrate infection models for pathogenic corynebacteria. FEMS Immunol Med Microbiol65:413–421 [CrossRef][PubMed]
    [Google Scholar]
  23. Sambrook J., Fritsch E. F., Maniatis T.. 1989; Molecular Cloning: a Laboratory Manual, 2nd edn.. Cold Sring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  24. Santos L. S., Antunes C. A., Santos C. S., Pereira J.A.A., Sabbadini P. S., Luna M., Azevedo V., Hirata Júnior R., Burkovski A., other authors. 2015; Corynebacterium diphtheriae putative tellurite-resistance protein (CDCE8392_0813) contributes to the intracellular survival in human epithelial cells and lethality of Caenorhabditis elegans . Mem Inst Oswaldo Cruz110:662–668 [CrossRef][PubMed]
    [Google Scholar]
  25. Tauch A., Burkovski A.. 2015; Molecular armory or niche factors: virulence determinants of Corynebacterium species. FEMS Microbiol Lett fnv185 [CrossRef][PubMed]
    [Google Scholar]
  26. Tropis M., Meniche X., Wolf A., Gebhardt H., Strelkov S., Chami M., Schomburg D., Krämer R., Morbach S., Daffé M.. 2005; The crucial role of trehalose and structurally related oligosaccharides in the biosynthesis and transfer of mycolic acids in Corynebacterineae . J Biol Chem280:26573–26585 [CrossRef][PubMed]
    [Google Scholar]
  27. Trost E., Al-Dilaimi A., Papavasiliou P., Schneider J., Viehoever P., Burkovski A., Soares S. C., Almeida S. S., Dorella F. A., other authors. 2011; Comparative analysis of two complete Corynebacterium ulcerans genomes and detection of candidate virulence factors. BMC Genomics12:383 [CrossRef][PubMed]
    [Google Scholar]
  28. Trost E., Blom J., Soares S. C., Huang I. H., Al-Dilaimi A., Schröder J., Jaenicke S., Dorella F. A., Rocha F. S., other authors. 2012; Pangenomic study of Corynebacterium diphtheriae that provides insights into the genomic diversity of pathogenic isolates from cases of classical diphtheria, endocarditis, and pneumonia. J Bacteriol194:3199–3215 [CrossRef][PubMed]
    [Google Scholar]
  29. Ventura M., Canchaya C., Tauch A., Chandra G., Fitzgerald G. F., Chater K. F., van Sinderen D.. 2007; Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol Mol Biol Rev71:495–548 [CrossRef][PubMed]
    [Google Scholar]
  30. Viguetti S. Z., Pacheco L. G., Santos L. S., Soares S. C., Bolt F., Baldwin A., Dowson C. G., Rosso M. L., Guiso N., other authors. 2012; Multilocus sequence types of invasive Corynebacterium diphtheriae isolated in the Rio de Janeiro urban area, Brazil. Epidemiol Infect140:617–620 [CrossRef][PubMed]
    [Google Scholar]
  31. Wolf A., Krämer R., Morbach S.. 2003; Three pathways for trehalose metabolism in Corynebacterium glutamicum ATCC13032 and their significance in response to osmotic stress. Mol Microbiol49:1119–1134 [CrossRef][PubMed]
    [Google Scholar]
  32. Yook K., Hodgkin J.. 2007; Mos1 mutagenesis reveals a diversity of mechanisms affecting response of Caenorhabditis elegans to the bacterial pathogen Microbacterium nematophilum . Genetics175:681–697 [CrossRef][PubMed]
    [Google Scholar]
  33. Zhang Y., Lu H., Bargmann C. I.. 2005; Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans . Nature438:179–184 [CrossRef][PubMed]
    [Google Scholar]
  34. Zhi X. Y., Li W. J., Stackebrandt E.. 2009; An update of the structure and 16S rRNA gene sequence-based definition of higher ranks of the class Actinobacteria, with the proposal of two new suborders and four new families and emended descriptions of the existing higher taxa. Int J Syst Evol Microbiol59:589–608 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000201
Loading
/content/journal/micro/10.1099/mic.0.000201
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error