The importance of being regular: Caenorhabditis elegans and Pristionchus pacificus defecation mutants are hypersusceptible to bacterial pathogens

International Journal for Parasitology

Volumn 42, Issue 8, 2012, Pages 747-753

  Rae, Robbie ^a   Witte, Hanh ^a   Rödelsperger, Christian ^a   Sommer, Ralf J ^a  

^a MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

Bacillus species; Caenorhabditis elegans; Defecation; Innate immunity; Peristalsis; Pristionchus pacificus; Staphylococcus aureus

Indexed keywords

BACTERIUM; DEFECATION; IMMUNITY; NEMATODE; PATHOGEN; PATHOGENICITY; SURVIVAL; VIRULENCE;

ARTICLE; BACILLUS; BACTERIAL STRAIN; BACTERIUM ISOLATION; CAENORHABDITIS ELEGANS; DEFECATION; GENE FREQUENCY; GENE IDENTIFICATION; GENE MAPPING; HOST RESISTANCE; HOST SUSCEPTIBILITY; INTESTINE MOTILITY; MORTALITY; MUSCLE FUNCTION; NEMATODE; NONHUMAN; PATHOGENICITY; PRISTIONCHUS PACIFICUS; PROGENY; SIMPLE SEQUENCE REPEAT; SOIL ANALYSIS; STAPHYLOCOCCUS AUREUS; SURVIVAL RATE;

ANIMALS; BACILLUS; CAENORHABDITIS ELEGANS; HELMINTH PROTEINS; HOST-PATHOGEN INTERACTIONS; MOLECULAR SEQUENCE DATA; MUTATION; NEMATODA; SOIL MICROBIOLOGY; SPECIES SPECIFICITY; STAPHYLOCOCCUS AUREUS; VIRULENCE;

BACILLUS (BACTERIUM); BACILLUS SP.; BACTERIA (MICROORGANISMS); CAENORHABDITIS ELEGANS; HEXAPODA; NEMATODA; POSIBACTERIA; PRISTIONCHUS PACIFICUS; STAPHYLOCOCCUS AUREUS;

EID: 84863826292     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2012.05.005     Document Type: Article

References (62)

1. Aballay A., Ausubel F.M. Programmed cell death mediated by ced-3 and ced-4 protects Caenorhabditis elegans from Salmonella typhimurium-mediated killing. Proc. Natl. Acad. Sci. USA 2001, 98:2735-2739.
2. Alverdy J.C., Aoys E. The effect of dexamethasone and endotoxin administration on biliary IgA and bacterial adherence. J. Surg. Res. 1992, 53:450-454.
3. Avery L., Thomas J.H. Feeding and defecation. C. elegans 2 1997, 679-716. Cold Spring Harbor Laboratory Press, New York. D.L. Riddle, T. Blumenthal, B.J. Meyer, J.R. Priess (Eds.).
4. Begun J., Sifri C.D., Goldman S., Calderwood S.B., Ausubel F.M. Staphylococcus aureus virulence factors identified by using a high-throughput Caenorhabditis elegans killing model. Infect. Immun. 2005, 73:872-877.
5. Bellier A., Chen C.-S., Kao C.Y., Cinar H.N., Aroian R.V. Hypoxia and the hypoxic response pathway protect against pore-forming toxins in C. elegans. PLoS Pathog. 2009, 5. 12:e1000689. 10.1371/journal.ppat.1000689.
6. Benian G.M., Kiff J.E., Neckelmann N., Moerman D.G., Waterston R.H. Sequence of an unusually large protein implicated in regulation of myosin activity in C. elegans. Nature 1989, 342:45-50.
7. Boehnisch C., Wong D., Habig M., Isermann K., Michiels N.K., Roeder T., May R.C., Schulenburg H. Protist-type lysozymes of the nematode Caenorhabditis elegans contribute to resistance against pathogenic Bacillus thuringiensis. PLoS One 2011, 6(9):e24619. 10.1371/journal.pone.0024619.
8. Borchert N., Dieterich C., Krug K., Schütz W., Jung S., Nordheim A., Sommer R.J., Macek B. Proteogenomics of Pristionchus pacificus reveals distinct proteome structure of nematode models. Genome Res. 2010, 20:837-846.
9. Branicky R., Hekimi S. What keeps C. elegans regular: the genetics of defecation. Trends Genet. 2006, 22:571-579.
10. Brown F.D., D'Anna I., Sommer R.J. Host-finding behavior in the nematode Pristionchus pacificus. Proc. R. Soc. B. 2011, 278:3269-3290.
11. Chantanao A., Jensen H.J. Saprozoic nematodes as carriers and disseminators of plant pathogenic bacteria. J. Nematol. 1969, 1:216-218.
12. Dack G.M., Petran R. Bacterial activity in different levels of the intestine. J. Infect. Dis. 1934, 54:204-220.
13. Dieterich C., Clifton S.W., Schuster L., Chinwalla A., Delehaunty K., Dinklelacker I., Fulton L., Godfrey J., Minx P., Mitreva M., Roeseler W., Tian H., Witte H., Yang S.P., Wilson R.K., Sommer R.J. The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nat. Genet. 2008, 40:1193-1198.
14. Dixon J.M.S., Paulley J.W. Bacteriological and histological studies of the small intestine of rats treated with mecamylamine. Gut. 1963, 4:169-173.
15. Dixon J.M.S. The fate of bacteria in the small intestine. J. Pathol. Bacteriol. 1960, 79:131-140.
16. Engelmann I., Griffon A., Tichit L., Montanana-Sanchis F., Wang G., Reinke V., Waterston R.H., Hillier L.W., Ewbank J.J. A comprehensive analysis of gene expression changes provoked by bacterial and fungal infection in C. elegans. Plos One 2011, 6(5):e19055. 10.1371/journal.pone.0019055.
17. Erbil Y., Berber E., Seven R., Calis A., Eminoglu L., Kocak M., Bilgic L. The effect of intestinal transit time on bacterial translocation. Acta Chir. Belg. 1998, 6:245-249.
18. Felix M.A., Braendle C. The natural history of Caenorhabditis elegans. Curr. Biol. 2010, 20:R965-R969.
19. Forst S., Dowds B., Boemare N., Stackebrandt E. Xenorhabdus spp. and Photorhabdus spp.: bugs that kill bugs. Annu. Rev. Microbiol. 1997, 51:47-72.
20. Garsin D.A., Villanueva J.M., Begun J., Kim D.H., Sifri C.D., Calderwood S.B., Ruvkun G., Ausubel F.M. Long-lived C. elegans daf-2 mutants are resistant to bacterial pathogens. Science 2003, 300:1921.
21. Ghafouri S., McGhee J.D. Bacterial residence time in the intestine of Caenorhabditis elegans. Nematology 2007, 9:87-91.
22. Grewal P.S. Influence of bacteria and temperature on the reproduction of Caenorhabditis elegans (Nematoda: Rhabditidae) infesting mushrooms (Agaricus bisporus). Nematologica 1991, 37:72-82.
23. Hasshoff M., Böhnisch C., Tonn D., Hasert B., Schulenburg H. The role of Caenorhabditis elegans insulin-like signaling in the behavioral avoidance of pathogenic Bacillus thuringiensis. FASEB J. 2007, 21:1801-1812.
24. Herrmann M., Mayer W., Sommer R.J. Nematodes of the genus Pristionchus are closely related with scarab beetles and the Colorado potato beetle in western Europe. Zoology. 2006, 109:96-108.
25. Hong R.L., Sommer R.J. Chemoattraction in Pristionchus nematodes and implications for insect host recognition. Curr. Biol. 2006, 16:2359-2365.
26. Huffman D.L., Abrami L., Sasik R., Corbeil J., van der Goot F.G., Aroian R.V. Mitogen-activated protein kinase pathways defend against bacterial pore-forming toxins. Proc. Natl. Acad. Sci. USA 2004, 101:10995-11000.
27. Husebye E. The pathogenesis of gastrointestinal bacterial overgrowth. Chemotherapy 2005, 51:1-22.
28. Kalif I.L., Quigley E.M.M., Konovitch E.A., Maximova I.D. Alterations in the colonic flora and intestinal permeability and evidence of immune activation in chronic constipation. Dig. Liver. Dis. 2005, 37:838-849.
29. Kao C.Y., Los F.C., Huffman D.L., Wachi S., Kloft N., Husmann M., Karabrahimi V., Schwartz J.L., Bellier A., Ha C., Sagong Y., Fan H., Ghosh P., Hsieh M., Hsu C.S., Chen L., Aroian R.V. Global functional analyses of cellular responses to pore-forming toxins. PLoS Pathog. 2011, 7(3). e1001314. 10.1371/journal.ppat.1001314.
30. Kawli T., Tan M.W. Neuroendocrine signals modulate the innate immunity of Caenorhabditis elegans through insulin signaling. Nat. Immunol. 2008, 9:1415-1424.
31. Kim D.H., Feinbaum R., Alloing G., Emerson F.E., Garsin D.A., Inoue H., Tanaka-Hino M., Hisamoto N., Matsumoto K., Tan M.W., Ausubel F.M. A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 2002, 297:623-626.
32. Li H., Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760.
33. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R. The sequence alignment/map format and SAMtools. Bioinformatics 2009, 25:2078-2079.
34. Liu D.W.C., Thomas J.H. Regulation of a periodic motor program in C. elegans. J. Neurosci. 1994, 14:1953-1962.
35. Los F.C., Kao C.Y., Smitham J., McDonald K.L., Ha C., Peixoto C.A., Aroian R.V. RAB-5 and RAB-11 dependant vesicle-trafficking pathways are required for plasma membrane repair after attack by bacterial pore-forming toxin. Cell Host Microbe 2011, 9:147-157.
36. Mallo G., Kurz C.I., Couillault C., Pujol N., Granjeaud S., Kohara Y., Ewbank J.J. Inducible antibacterial defense system in C. elegans. Curr. Biol. 2002, 12:1209-1214.
37. Martin P.A., Travers R.S. Worldwide abundance and distribution of Bacillus thuringiensis isolates. Appl. Environ. Microbiol. 1989, 55:2437-2442.
38. Morgan K., McGaughran A., Witte H., Bartelmes G., Villate L., Herrmann M., Rochat J., Sommer R.J. Multi-locus analysis of Pristionchus pacificus on LaReunion island reveals an evolutionary history shaped by multiple introductions, constrained dispersal events, and rare out-crossing. Mol. Ecol. 2012, 21:250-266.
39. Nicholas H.R., Hodgkin J. The ERK MAP kinase cascade mediates tail swelling and a protective response to rectal infection in C. elegans. Curr. Biol. 2004, 14:1256-1261.
40. Nieuwenhuijs V.B., Verheem A., van Duijvenbode-Beumer H., Visser M.R., Verhoef J., Gooszen H.G., Akkermans L.M. The role of interdigestive small bowel motility, bacterial overgrowth, and bacterial translocation in rats. Ann. Surg. 1998, 228:188-193.
41. Nurrish S.J. An overview of C. elegans trafficking mutants. Traffic. 2002, 3:2-10.
42. Nussbaumer A.D., Bright M., Baranyi C., Beisser C.J., Ott J.A. Attachment mechanism in a highly specific association between ectosymbiotic bacteria and marine nematodes. Aquat. Microb. Ecol. 2004, 34:239-246.
43. Ogawa A., Bento G., Bartelmes G., Dieterich C., Sommer R.J. Pristionchus pacificus daf-16 is essential for dauer formation but dispensable for mouth form dimorphism. Development 2011, 138:1281-1284.
44. Pires da Silva, A., 2006. Wormbook, Pristionchus pacificus genetic protocols. http://www.wormbook.org.
45. Rae R., Riebesell M., Dinkelacker I., Wang Q., Herrmann M., Weller A.M., Dieterich C., Sommer R.J. Isolation of naturally associated bacteria of necromenic Pristionchus nematodes and fitness consequences. J. Exp. Biol. 2008, 211:1927-1936.
46. Rae R., Iatsenko I., Witte H., Sommer R.J. A subset of naturally isolated Bacillus strains show extreme virulence to the free-living nematodes Caenorhabditis elegans and Pristionchus pacificus. Environ. Microbiol. 2010, 12:3007-3021.
47. Schlager B., Wang X., Braach G., Sommer R.J. Molecular cloning of a dominant roller mutant and establishment of DNA-mediated transformation in the nematode Pristionchus pacificus. Genesis. 2009, 47:300-304.
48. Schnepf E., Crickmore N., Van Rie J., Lereclus D., Baum J., Feitelson J., Zeigler D.R., Dean D.H. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 1998, 62:775-806.
49. Scott L.D., Cahall D.L. Influence of the interdigestive myoelectric complex on enteric flora in the rat. Gastroenterology. 1982, 82:737-745.
50. Shapira M., Tan M.W. Genetic analysis of Caenorhabditis elegans innate immunity. Innate immunity 2008, 429-442. Springer, Heidelberg. J.J. Ewbank, E. Vivier (Eds.).
51. Sicard M., Hering S., Schulte R., Gaudriault S., Schulenburg H. The effect of Photorhabdus luminescens (Enterobacteriaceae) on the survival, development, reproduction and behavior of Caenorhabditis elegans (Nematoda: Rhabditidae). Environ. Microbiol. 2007, 9:12-25.
52. Siddiqui Z.A., Mahmood I. Role of bacteria in the management of plant parasitic nematodes: a review. Bioresour. Technol. 1999, 69:167-179.
53. Sinha, A., Sommer, R.J., Dieterich, C., in press. Divergent gene expression in the conserved dauer stage of the nematodes Pristionchus pacificus and Caenorhabditis elegans. BMC Genomics.
54. Sommer R.J., Carta L.K., Kim S.Y., Sternberg P.W. Morphological, genetic and molecular description of Pristionchus pacificus sp. n. (Nematoda: Neodiplogastridae). Fund. Appl. Nematol. 1996, 19:521-551.
55. Srinivasan J., Sinz W., Lanz C., Brand A., Nandakumar R., Raddatz G., Witte H., Keller H., Kipping I., Pires-daSilva A., Jesse T., Millare J., de Both M., Schuster S.C., Sommer R.J. A bacterial artificial chromosome-based genetic linkage map of the nematode Pristionchus pacificus. Genetics. 2002, 162:229-234.
56. Taylor M.J., Bandi C., Hoerauf A. Wolbachia bacterial endosymbionts of filarial nematodes. Adv. Parasitol. 2005, 60:245-282.
57. Thompson J.N. The co-evolutionary process 1994, The University Chicago Press, Chicago and London.
58. Thompson J.N. The geographic mosaic of coevolution (interspecific interactions) The University Chicago Press 2005, Chicago and London.
59. Wang, J., Nakad, R., Schulenburg, H., 2011. Activation of the Caenorhabditis elegans FOXO family transcription factor DAF-16 by pathogenic Bacillus thuringiensis. Dev. Comp. Immunol. http://dx.doi.org/10.1016/j.dci.2011.08.016.
60. Wei J.Z., Hale K., Carta L., Platzer E., Wong C., Fang S.C., Aroian R.V. Bacillus thuringiensis crystal proteins that target nematodes. Proc. Natl. Acad. Sci. USA 2003, 100:2760-2765.
61. Wong D., Bazopoulou D., Pujol N., Tavernarakis N., Ewbank J.J. Genome-wide investigation reveals pathogen specific and shared signatures in the response of Caenorhabditis elegans to infection. Genome Biol. 2007, 8:R194.
62. Woolhouse M.E., Webster J.P., Domingo E., Charlesworth B., Levin B.R. Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat. Genet. 2002, 32:569-577.