DOI QR코드

DOI QR Code

Comparative Analyses of Four Complete Genomes in Pseudomonas amygdali Revealed Differential Adaptation to Hostile Environments and Secretion Systems

  • Jung, Hyejung (Department of Integrated Biological Science, Pusan National University) ;
  • Kim, Hong-Seop (Korea Seed & Variety Service) ;
  • Han, Gil (Department of Integrated Biological Science, Pusan National University) ;
  • Park, Jungwook (Department of Integrated Biological Science, Pusan National University) ;
  • Seo, Young-Su (Department of Integrated Biological Science, Pusan National University)
  • Received : 2021.11.30
  • Accepted : 2022.03.10
  • Published : 2022.04.01

Abstract

Pseudomonas amygdali is a hemibiotrophic phytopathogen that causes disease in woody and herbaceous plants. Complete genomes of four P. amygdali pathovars were comparatively analyzed to decipher the impact of genomic diversity on host colonization. The pan-genome indicated that 3,928 core genes are conserved among pathovars, while 504-1,009 are unique to specific pathovars. The unique genome contained many mobile elements and exhibited a functional distribution different from the core genome. Genes involved in O-antigen biosynthesis and antimicrobial peptide resistance were significantly enriched for adaptation to hostile environments. While the type III secretion system was distributed in the core genome, unique genomes revealed a different organization of secretion systems as follows: type I in pv. tabaci, type II in pv. japonicus, type IV in pv. morsprunorum, and type VI in pv. lachrymans. These findings provide genetic insight into the dynamic interactions of the bacteria with plant hosts.

Keywords

Acknowledgement

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Education (2019R1A2C2006779) and by a grant from the Nakdonggang National Institute of Biological Resources (NNIBR), funded by the Ministry of Environment(MOE) of the Republic of Korea (NNIBR202202108).

References

  1. Bender, C. L., Alarcon-Chaidez, F. and Gross, D. C. 1999. Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol. Mol. Biol. Rev. 63:266-292. https://doi.org/10.1128/mmbr.63.2.266-292.1999
  2. Bocsanczy, A. M., Huguet-Tapia, J. C. and Norman, D. J. 2017. Comparative genomics of Ralstonia solanacearum identifies candidate genes associated with cool virulence. Front. Plant Sci. 8:1565. https://doi.org/10.3389/fpls.2017.01565
  3. Cardan, L., Shafik, H., Belouin, S., Broch, R., Grimont, F. and Grimont, P. 1999. DNA relatedness among the pathovars of Pseudomonas syringae and description of Pseudomonas tremae sp. nov. and Pseudomonas cannabina sp. nov. (ex Sutic and Dowson 1959). Int. J. Syst. Bacteriol. 49:469-478. https://doi.org/10.1099/00207713-49-2-469
  4. Chang, J. H., Urbach, J. M., Law, T. F., Arnold, L. W., Hu, A., Gombar, S., Grant, S. R., Ausubel, F. M. and Dangl, J. L. 2005. A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae. Proc. Natl. Acad. Sci. U. S. A. 102:2549-2554. https://doi.org/10.1073/pnas.0409660102
  5. Cunnac, S., Lindeberg, M. and Collmer, A. 2009. Pseudomonas syringae type III secretion system effectors: repertoires in search of functions. Curr. Opin. Microbiol. 12:53-60. https://doi.org/10.1016/j.mib.2008.12.003
  6. Dudnik, A. and Dudler, R. 2014. Genomics-based exploration of virulence determinants and host-specific adaptations of Pseudomonas syringae strains isolated from grasses. Pathogens 3:121-148. https://doi.org/10.3390/pathogens3010121
  7. Goo, E., Kang, Y., Kim, H. and Hwang, I. 2010. Proteomic analysis of quorum sensing-dependent proteins in Burkholderia glumae. J. Proteome Res. 9:3184-3199. https://doi.org/10.1021/pr100045n
  8. Guttman, D. S., Vinatzer, B. A., Sarkar, S. F., Ranall, M. V., Kettler, G. and Greenberg, J. T. 2002. A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295:1722-1726. https://doi.org/10.1126/science.295.5560.1722
  9. Hersemann, L., Wibberg, D., Blom, J., Goesmann, A., Widmer, F., Vorholter, F.-J. and Kolliker, R. 2017. Comparative genomics of host adaptive traits in Xanthomonas translucens pv. graminis. BMC Genomics 18:35. https://doi.org/10.1186/s12864-016-3422-7
  10. Hulin, M. T., Mansfield, J. W., Brain, P., Xu, X., Jackson, R. W. and Harrison, R. J. 2018. Characterization of the pathogenicity of strains of Pseudomonas syringae towards cherry and plum. Plant Pathol. 67:1177-1193. https://doi.org/10.1111/ppa.12834
  11. Kapchina, V., Milanov, G., Zankov, A., Stefanov, D., Slavov, S., Goltsev, V. and Batchvarova, R. 2014. The changes in some photosynthetic characteristics of transgenic tobacco plants, resistant to bacteria Pseudomonas syringae pv. tabaci. Biotechnol. Biotechnol. Equip. 18:74-84.
  12. Koczan, J. M., Lenneman, B. R., McGrath, M. J. and Sundin, G. W. 2011. Cell surface attachment structures contribute to biofilm formation and xylem colonization by Erwinia amylovora. Appl. Environ. Microbiol. 77:7031-7039. https://doi.org/10.1128/AEM.05138-11
  13. Lawley, T. D., Klimke, W. A., Gubbins, M. J. and Frost, L. S. 2003. F factor conjugation is a true type IV secretion system. FEMS Microbiol. Lett. 224:1-15. https://doi.org/10.1016/S0378-1097(03)00430-0
  14. Lerouge, I. and Vanderleyden, J. 2002. O-antigen structural variation: mechanisms and possible roles in animal/plant-microbe interactions. FEMS Microbiol. Rev. 26:17-47. https://doi.org/10.1016/S0168-6445(01)00070-5
  15. Li, L., Yuan, L., Shi, Y., Xie, X., Chai, A., Wang, Q. and Li, B. 2019. Comparative genomic analysis of Pseudomonas amygdali pv. lachrymans NM002: insights into its potential virulence genes and putative invasion determinants. Genomics 111:1493-1503. https://doi.org/10.1016/j.ygeno.2018.10.004
  16. Lukjancenko, O. and Ussery, D. W. 2014. Vibrio chromosomespecific families. Front. Microbiol. 5:73. https://doi.org/10.3389/fmicb.2014.00073
  17. Mardis, E., McPherson, J., Martienssen, R., Wilson, R. K. and Richard McCombie, W. 2002. What is finished, and why does it matter. Genome Res. 12:669-671. https://doi.org/10.1101/gr.032102
  18. Meng, X.-L., Xie, X.-W., Shi, Y.-X., Chai, A.-L., Ma, Z.-H. and Li, B.-J. 2017. Evaluation of a loop-mediated isothermal amplification assay based on hrpZ gene for rapid detection and identification of Pseudomonas syringae pv. lachrymans in cucumber leaves. J. Appl. Microbiol. 122:441-449. https://doi.org/10.1111/jam.13356
  19. Oliveira, P. H., Touchon, M. and Rocha, E. P. C. 2014. The interplay of restriction-modification systems with mobile genetic elements and their prokaryotic hosts. Nucleic Acids Res. 42:10618-10631. https://doi.org/10.1093/nar/gku734
  20. Pandin, C., Caroff, M. and Condemine, G. 2016. Antimicrobial peptide resistance genes in the plant pathogen Dickeya dadantii. Appl. Environ. Microbiol. 82:6423-6430. https://doi.org/10.1128/AEM.01757-16
  21. Rapicavoli, J., Ingel, B., Blanco-Ulate, B., Cantu, D. and Roper, C. 2018a. Xylella fastidiosa: an examination of a re-emerging plant pathogen. Mol. Plant Pathol. 19:786-800. https://doi.org/10.1111/mpp.12585
  22. Rapicavoli, J. N., Blanco-Ulate, B., Muszynski, A., Figueroa- Balderas, R., Morales-Cruz, A., Azadi, P., Dobruchowska, J. M., Castro, C., Cantu, D. and Roper, M. C. 2018b. Lipopolysaccharide O-antigen delays plant innate immune recognition of Xylella fastidiosa. Nat. Commun. 9:390. https://doi.org/10.1038/s41467-018-02861-5
  23. Satomi, Y., Arisawa, M., Nishino, H. and Iwashima, A. 1994. Antitumor-promoting activity of mallotojaponin, a major constituent of pericarps of Mallotus japonicus. Oncology 51:215-219. https://doi.org/10.1159/000227336
  24. Schmidtchen, A., Frick, I.-M., Andersson, E., Tapper, H. and Bjorck, L. 2002. Proteinases of common pathogenic bacteria degrade and inactivate the antibacterial peptide LL-37. Mol. Microbiol. 46:157-168. https://doi.org/10.1046/j.1365-2958.2002.03146.x
  25. Taguchi, F. and Ichinose, Y. 2011. Role of type IV pili in virulence of Pseudomonas syringae pv. tabaci 6605: correlation of motility, multidrug resistance, and HR-inducing activity on a nonhost plant. Mol. Plant.-Microbe. Interact. 24:1001-1011. https://doi.org/10.1094/MPMI-02-11-0026
  26. Taguchi, F., Suzuki, T., Inagaki, Y., Toyoda, K., Shiraishi, T. and Ichinose, Y. 2010. The siderophore pyoverdine of Pseudomonas syringae pv. tabaci 6605 is an intrinsic virulence factor in host tobacco infection. J. Bacteriol. 192:117-126. https://doi.org/10.1128/JB.00689-09
  27. Tettelin, H., Riley, D., Cattuto, C. and Medini, D. 2008. Comparative genomics: the bacterial pan-genome. Curr. Opin. Microbiol. 11:472-477. https://doi.org/10.1016/j.mib.2008.09.006
  28. Wu, H.-Y., Chung, P.-C., Shih, H.-W., Wen, S.-R. and Lai, E.-M. 2008. Secretome analysis uncovers an Hcp-family protein secreted via a type VI secretion system in Agrobacterium tumefaciens. J. Bacteriol. 190:2841-2850. https://doi.org/10.1128/JB.01775-07
  29. Yu, J., Penaloza-Vazquez, A., Chakrabarty, A. M. and Bender, C. L. 1999. Involvement of the exopolysaccharide alginate in the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae. Mol. Microbiol. 33:712-720. https://doi.org/10.1046/j.1365-2958.1999.01516.x
  30. Yuan, Z.-C., Liu, P., Saenkham, P., Kerr, K. and Nester, E. W. 2008. Transcriptome profiling and functional analysis of Agrobacterium tumefaciens reveals a general conserved response to acidic conditions (pH 5.5) and a complex acidmediated signaling involved in Agrobacterium-plant interactions. J. Bacteriol. 190:494-507. https://doi.org/10.1128/JB.01387-07
  31. Yun, H. Y. and Kim, H. 2021. First report of Pseudomonas amygdali causing bacterial leaf spot of Mallotus japonicus in South Korea. For. Pathol. 51:e12707.
  32. Zhang, Y., Fan, Q. and Loria, R. 2016. A re-evaluation of the taxonomy of phytopathogenic genera Dickeya and Pectobacterium using whole-genome sequencing data. Syst. Appl. Microbiol. 39:252-259. https://doi.org/10.1016/j.syapm.2016.04.001