Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Infection and Immune Response in the Nematode Caenorhabditis elegans Elicited by the Phytopathogen Xanthomonas

  • Bai, Yanli (Gansu Key Laboratory of Biomonitoring and Bioremediation for Environmental Pollution, School of Life Sciences, Lanzhou University) ;
  • Zhi, Dejuan (School of Pharmacy, Lanzhou University) ;
  • Li, Chanhe (Gansu Key Laboratory of Biomonitoring and Bioremediation for Environmental Pollution, School of Life Sciences, Lanzhou University) ;
  • Liu, Dongling (Gansu Key Laboratory of Biomonitoring and Bioremediation for Environmental Pollution, School of Life Sciences, Lanzhou University) ;
  • Zhang, Juan (Gansu Key Laboratory of Biomonitoring and Bioremediation for Environmental Pollution, School of Life Sciences, Lanzhou University) ;
  • Tian, Jing (School of Pharmacy, Lanzhou University) ;
  • Wang, Xin (School of Pharmacy, Lanzhou University) ;
  • Ren, Hui (School of Pharmacy, Lanzhou University) ;
  • Li, Hongyu (Gansu Key Laboratory of Biomonitoring and Bioremediation for Environmental Pollution, School of Life Sciences, Lanzhou University)
  • Received : 2014.01.09
  • Accepted : 2014.05.18
  • Published : 2014.09.28
Download PDF
⟨ Previous Next ⟩

Abstract

Xanthomonas oryzae pv. oryzae (Xoo) strains are plant pathogenic bacteria that can cause serious blight of rice, and their virulence towards plant host is complex, making it difficult to be elucidated. Caenorhabditis elegans has been used as a powerful model organism to simplify the host and pathogen system. However, whether the C. elegans is feasible for studying plant pathogens such as Xoo has not been explored. In the present work, we report that Xoo strains PXO99 and JXOIII reduce the lifespan of worms not through acute toxicity, but in an infectious manner; pathogens proliferate and persist in the intestinal lumen to cause marked anterior intestine distension. In addition, Xoo triggers (i) the p38 MAPK signal pathway to upregulate its downstream C17H12.8 expression, and (ii) the DAF-2/DAF-16 pathway to upregulate its downstream gene expressions of mtl-1 and sod-3 under the condition of daf-2 mutation. Our findings suggest that C. elegans can be used as a model to evaluate the virulence of Xoo phytopathogens to host.

Keywords

References

  1. Aballay A, Drenkard E, Hilbun LR, Ausubel FM. 2003. Caenorhabditis elegans innate immune response triggered by Salmonella enterica requires intact LPS and is mediated by a MAPK signaling pathway. Curr. Biol. 13: 47-52. https://doi.org/10.1016/S0960-9822(02)01396-9
  2. Alegado RA, Campbell MC, Chen WC, Slutz SS, Tan MW. 2003. Characterization of mediators of microbial virulence and innate immunity using the Caenorhabditis elegans hostpathogen model. Cell Microbiol. 5: 435-444. https://doi.org/10.1046/j.1462-5822.2003.00287.x
  3. Antebi A. 2007. Genetics of aging in Caenorhabditis elegans. PLoS Genet. 3: e129. https://doi.org/10.1371/journal.pgen.0030129
  4. Baumeister R, Schaffitzel E, Hertweck M. 2006. Endocrine signaling in Caenorhabditis elegans controls stress response and longevity. J. Endocrinol. 190: 191-202. https://doi.org/10.1677/joe.1.06856
  5. Bojer MS, Jakobsen H, Struve C, Krogfelt KA, Løbner- Olesen A. 2012. Lack of the RNA chaperone hfq attenuates pathogenicity of several Escherichia coli pathotypes towards Caenorhabditis elegans. Microb. Infect. 14: 1034-1039. https://doi.org/10.1016/j.micinf.2012.06.002
  6. Bolz DD, Tenor JL, Aballay A. 2010. A conserved PMK-1/ p38 MAPK is required in Caenorhabditis elegans tissuespecific immune response to Yersinia pestis infection. J. Biol. Chem. 285: 10832-10840. https://doi.org/10.1074/jbc.M109.091629
  7. Choi Y, Kang HE, Lim HY, Shim H, Lee KS, Park BJ. 2010. A study for the virulence of Xanthomonas, a plant pathogenic bacteria using C. elegans as a tractable host-pathogen system. Proceedings of the 2010 Symposium and Annual Meeting of the Korean Society for Microbiology and Biotechnology.
  8. Couillault C, Ewbank JJ. 2002. Diverse bacteria are pathogens of Caenorhabditis elegans. Infect. Immun. 70: 4705-4707. https://doi.org/10.1128/IAI.70.8.4705-4707.2002
  9. Darby C. 2005. Interactions with microbial pathogens, pp. 1-15. Wormbook. The C. elegans Research Community. DOI: 10.1895/wormbook.1.21.1, http://www.wormbook.org.
  10. Dhakal BK, Lee W, Kim YR, Choy HE, Ahnn J, Rhee JH. 2006. Caenorhabditis elegans as a simple model host for Vibrio vulnificus infection. Biochem. Biophys. Res. Commun. 346: 751-757. https://doi.org/10.1016/j.bbrc.2006.05.168
  11. Evans EA, Kawli T , Tan M-W. 2008 . Pseudomonas aeruginosa suppresses host immunity by activating the DAF-2 insulin like signaling pathway in Caenorhabditis elegans. PLoS Pathog. 4: e1000175. https://doi.org/10.1371/journal.ppat.1000175
  12. Xie GL, Weng JP, Mew TW. 1989. Comparision of virulence of Xanthomonas campestris pv. oryzae in Zhejiang of China and the Philippines. Acta Agric. Zhejiangensis 1: 72-77.
  13. Garigan D, Hsu AL, Fraser AG, Kamath RS, Ahringer J, Kenyon C. 2002. Genetic analysis of tissue aging in Caenorhabditis elegans: a role for heat-shock factor and bacterial proliferation. Genetics 161: 1101-1112.
  14. Garsin DA, Sifri CD, Mylonakis E, Qin X, Singh KV, Murray BE, et al. 2001. A simple model host for identifying grampositive virulence factors. Proc. Natl. Acad. Sci. USA 98: 10892-10897. https://doi.org/10.1073/pnas.191378698
  15. Grad LI, Lemire BD. 2004. Mitochondrial complex I mutations in Caenorhabditis elegans produce cytochrome c oxidase deficiency, oxidative stress and vitamin-responsive lactic acidosis. Human Mol. Genet. 13: 303-314. https://doi.org/10.1093/hmg/ddh231
  16. Henderson ST, Johnson TE. 2001. daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr. Biol. 11: 1975-1980. https://doi.org/10.1016/S0960-9822(01)00594-2
  17. Hopkins C, White F, Choi S, Guo A, Leach J. 1992. Identification of a family of avirulence genes from Xanthomonas oryzae pv. oryzae. Mol. Plant Microbe Interact. 5: 451-459. https://doi.org/10.1094/MPMI-5-451
  18. Inoue H, Hisamoto N, An JH, Oliveira RP, Nishida E, Blackwell TK, Matsumoto K. 2005. The C. elegans p38 MAPK pathway regulates nuclear localization of the transcription factor SKN-1 in oxidative stress response. Gene Dev. 19: 2278-2283. https://doi.org/10.1101/gad.1324805
  19. Irazoqui JE, Troemel ER, Feinbaum RL, Luhachack LG, Cezairliyan BO, Ausubel FM. 2010. Distinct pathogenesis and host responses during infection of C. elegans by P. aeruginosa and S. aureus. PLoS Pathog. 6: e1000982. https://doi.org/10.1371/journal.ppat.1000982
  20. Kim DH, Ausubel FM. 2005. Evolutionary perspectives on innate immunity from the study of Caenorhabditis elegans. Curr. Opin. Immunol. 17: 4-10. https://doi.org/10.1016/j.coi.2004.11.007
  21. Kim DH, Feinbaum R, Alloing G, Emerson FE, Garsin DA, Inoue H, et al. 2002. A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 297: 623-626. https://doi.org/10.1126/science.1073759
  22. Kurz CL, Tan MW. 2004. Regulation of aging and innate immunity in C. elegans. Aging Cell 3: 185-193. https://doi.org/10.1111/j.1474-9728.2004.00108.x
  23. Landis JN, Murphy CT. 2010. Integration of diverse inputs in the regulation of Caenorhabditis elegans DAF-16/FOXO. Dev. Dyn. 239: 1405-1412.
  24. Li X, Li H, Pang X, Feng H, Zhi D, Wen J, Wang J. 2007. Localization changes of endogenous hydrogen peroxide during cell division cycle of Xanthomonas. Mol. Cell Biochem. 300: 207-213. https://doi.org/10.1007/s11010-006-9385-2
  25. Libina N, Berman JR, Kenyon C. 2003. Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 115: 489-502. https://doi.org/10.1016/S0092-8674(03)00889-4
  26. Mahajan-Miklos S, Tan MW, Rahme LG, Ausubel FM. 1999. Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96: 47-56. https://doi.org/10.1016/S0092-8674(00)80958-7
  27. Marsh EK, May RC. 2012. Caenorhabditis elegans, a model organism for investigating immunity. Appl. Environ. Microbiol. 78: 2075-2081. https://doi.org/10.1128/AEM.07486-11
  28. McElwee J, Bubb K, Thomas JH. 2003. Transcriptional outputs of the Caenorhabditis elegans forkhead protein DAF-16. Aging Cell 2: 111-121. https://doi.org/10.1046/j.1474-9728.2003.00043.x
  29. Millet A, Ewbank JJ. 2004. Immunity in Caenorhabditis elegans. Curr. Opin. Immunol. 16: 4-9. https://doi.org/10.1016/j.coi.2003.11.005
  30. Moy TI, Ball AR, Anklesaria Z, Casadei G, Lewis K, Ausubel FM. 2006. Identification of novel antimicrobials using a live-animal infection model. Proc. Natl. Acad. Sci. 103: 10414-10419. https://doi.org/10.1073/pnas.0604055103
  31. Muir RE, Tan MW. 2008. Virulence of Leucobacter chromiireducens subsp. solipictus to Caenorhabditis elegans: characterization of a novel host-pathogen interaction. Appl. Environ. Microbiol. 74: 4185-4198. https://doi.org/10.1128/AEM.00381-08
  32. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, et al. 2003. Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424: 277-283. https://doi.org/10.1038/nature01789
  33. Nicholas HR, Hodgkin J. 2004. Responses to infection and possible recognition strategies in the innate immune system of Caenorhabditis elegans. Mol. Immunol. 41: 479-493. https://doi.org/10.1016/j.molimm.2004.03.037
  34. Onasanya A, Onasanya R, Ojo AA, Adewale B. 2013. Genetic analysis and molecular identification of virulence in Xanthomonas oryzae pv. oryzae isolates. ISRN Mol. Biol. 2013: 1-8.
  35. Reinke S, Hu X, Sykes B, Lemire B. 2010. Caenorhabditis elegans diet significantly affects metabolic profile, mitochondrial DNA levels, lifespan and brood size. Mol. Genet. Metab. 100: 274-282. https://doi.org/10.1016/j.ymgme.2010.03.013
  36. Shen Y, Ronald P. 2002. Molecular determinants of disease and resistance in interactions of Xanthomonas oryzae pv. oryzae and rice. Microbes Infect. 4: 1361-1367. https://doi.org/10.1016/S1286-4579(02)00004-7
  37. Shivers RP, Kooistra T, Chu SW, Pagano DJ, Kim DH. 2009. Tissue-specific activities of an immune signaling module regulate physiological responses to pathogenic and nutritional bacteria in C. elegans. Cell Host Microbe 6: 321-330. https://doi.org/10.1016/j.chom.2009.09.001
  38. Shivers RP, Youngman MJ, Kim DH. 2008. Transcriptional responses to pathogens in Caenorhabditis elegans. Curr. Opin. Microbiol. 11: 251-256. https://doi.org/10.1016/j.mib.2008.05.014
  39. Troemel ER, Chu SW, Reinke V, Lee SS, Ausubel FM, Kim DH. 2006. p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet. 2: e183. https://doi.org/10.1371/journal.pgen.0020183
  40. Youngman MJ, Rogers ZN, Kim DH. 2011. A decline in p38 MAPK signaling underlies immunosenescence in Caenorhabditis elegans. PLoS Genet. 7: e1002082. https://doi.org/10.1371/journal.pgen.1002082
  41. Zou HS, Zhao WX, Zhang XF, Han YC, Zou LF, Chen GY. 2010. Identification of an avirulence gene, avrxa5, from the rice pathogen Xanthomonas oryzae pv. oryzae. Sci. China Life Sci. 53: 1440-1449. https://doi.org/10.1007/s11427-010-4109-y

Cited by

  1. Regulation of Lysosomal Function by the DAF-16 Forkhead Transcription Factor Couples Reproduction to Aging in Caenorhabditis elegans vol.207, pp.1, 2014, https://doi.org/10.1534/genetics.117.204222
  2. Novel Nematode-Killing Protein-1 (Nkp-1) from a Marine Epiphytic Bacterium Pseudoalteromonas tunicata vol.9, pp.11, 2014, https://doi.org/10.3390/biomedicines9111586
  3. Streptococcus thermophilus extends lifespan through activation of DAF-16-mediated antioxidant pathway in Caenorhabditis elegans vol.70, pp.1, 2014, https://doi.org/10.3164/jcbn.21-56