Browse > Article
http://dx.doi.org/10.5423/PPJ.OA.12.2021.0190

Genome Wide Analysis of the Potato Soft Rot Pathogen Pectobacterium carotovorum Strain ICMP 5702 to Predict Novel Insights into Its Genetic Features  

Mallick, Tista (Department of Biotechnology, Rama Devi Women's University)
Mishra, Rukmini (School of Applied Sciences, Centurion University of Technology and Management)
Mohanty, Sasmita (Department of Biotechnology, Rama Devi Women's University)
Joshi, Raj Kumar (Department of Biotechnology, Rama Devi Women's University)
Publication Information
The Plant Pathology Journal / v.38, no.2, 2022 , pp. 102-114 More about this Journal
Abstract
Pectobacterium carotovorum subsp. carotovorum (Pcc) is a gram-negative, broad host range bacterial pathogen which causes soft rot disease in potatoes as well as other vegetables worldwide. While Pectobacterium infection relies on the production of major cell wall degrading enzymes, other virulence factors and the mechanism of genetic adaptation of this pathogen is not yet clear. In the present study, we have performed an in-depth genome-wide characterization of Pcc strain ICMP5702 isolated from potato and compared it with other pathogenic bacteria from the Pectobacterium genus to identify key virulent determinants. The draft genome of Pcc ICMP5702 contains 4,774,457 bp with a G + C content of 51.90% and 4,520 open reading frames. Genome annotation revealed prominent genes encoding key virulence factors such as plant cell wall degrading enzymes, flagella-based motility, phage proteins, cell membrane structures, and secretion systems. Whereas, a majority of determinants were conserved among the Pectobacterium strains, few notable genes encoding AvrE-family type III secretion system effectors, pectate lyase and metalloprotease in addition to the CRISPR-Cas based adaptive immune system were uniquely represented. Overall, the information generated through this study will contribute to decipher the mechanism of infection and adaptive immunity in Pcc.
Keywords
effectors; genomic analysis; host-pathogen interaction; pathogenicity; Pectobacterium carotovorum subsp. carotovorum;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Filloux, A. 2004. The underlying mechanisms of type II protein secretion. Biochim. Biophys. Acta 1694:163-179.   DOI
2 Gallique, M., Decoin, V., Barbey, C., Rosay, T., Feuilloley, M. G. J., Orange, N. and Merieau, A. 2017. Contribution of the Pseudomonas fluorescens MFE01 type VI secretion system to biofilm formation. PLoS ONE 12:e0170770.   DOI
3 Arndt, D., Grant, J. R., Marcu, A., Sajed, T., Pon, A., Liang, Y. and Wishart, D. S. 2016. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res. 44:W16-W21.   DOI
4 Auch, A. F., Klenk, H.-P. and Goker, M. 2010. Standard operating procedure for calculating genome-to-genome distances based on high-scoring segment pairs. Stand. Genomic Sci. 2:142-148.   DOI
5 Wang, Y., Coleman-Derr, D., Chen, G. and Gu, Y. Q. 2015. OrthoVenn: a web server for genome wide comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res. 43:W78-W84.   DOI
6 Kim, H.-S., Thammarat, P., Lommel, S. A., Hogan, C. S. and Charkowski, A. O. 2011. Pectobacterium carotovorum elicits plant cell death with DspE/F but the P. carotovorum DspE does not suppress callose or induce expression of plant genes early in plant-microbe interactions. Mol. Plant-Microbe Interact. 24:773-786.   DOI
7 Huerta-Cepas, J., Szklarczyk, D., Heller, D., Hernandez-Plaza, A., Forslund, S. K., Cook, H., Mende, D. R., Letunic, I., Rattei, T., Jensen, L. J., von Mering, C. and Bork, P. 2019. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res. 47:D309-D314.   DOI
8 Kim, H.-S., Ma, B., Perna, N. T. and Charkowski, A. O. 2009. Phylogeny and virulence of naturally occurring type III secretion system-deficient Pectobacterium strains. Appl. Environ. Microbiol. 75:4593-4549.
9 Krogh, A., Larsson, B., von Heijne, G. and Sonnhammer, E. L. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:567-580.   DOI
10 Li, L., Yuan, L., Shi, Y., Xie, X., Chai, A., Wang, Q. and Li, B. 2019. Comparative genomic analysis of Pectobacterium carotovorum subsp. brasiliense SX309 provides novel insights into its genetic and phenotypic features. BMC Genomics 20:486.   DOI
11 Wick, R. R., Judd, L. M., Gorrie, C. L. and Holt, K. E. 2017. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput. Biol. 13:e1005595.   DOI
12 Garg, A. and Gupta, D. 2008. VirulentPred: a SVM based prediction method for virulent proteins in bacterial pathogens. BMC Bioinformatics 9:62.   DOI
13 Charkowski, A. O. 2018. The changing face of bacterial soft-rot diseases. Annu. Rev. Phytopathol. 56:269-288.   DOI
14 Couvin, D., Bernheim, A., Toffano-Nioche, C., Touchon, M., Michalik, J., Neron, B., Rocha, E. P. C., Vergnaud, G., Gautheret, D. and Pourcel, C. 2018. CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins. Nucleic Acids Res. 46:W246-W251.   DOI
15 Dees, M. W., Lysoe, E., Rossmann, S., Perminow, J. and Brurberg, M. B. 2017. Pectobacterium polaris sp. nov., isolated from potato (Solanum tuberosum). Int. J. Syst. Evol. Microbiol. 67:5222-5229.   DOI
16 Lee, D. H., Lim, J.-A., Lee, J., Roh, E., Jung, K., Choi, M., Oh, C., Ryu, S., Yun, J. and Heu, S. 2013. Characterization of genes required for the pathogenicity of Pectobacterium carotovorum subsp. carotovorum Pcc21 in Chinese cabbage. Microbiology 159:1487-1496.   DOI
17 Petrova, O., Gorshkov, V., Sergeeva, I., Daminova, A., Ageeva, M. and Gogolev, Y. 2016. Alternative scenarios of starvationinduced adaptation in Pectobacterium atrosepticum. Res. Microbiol. 167:254-261.   DOI
18 Li, X., Ma, Y., Liang, S., Tian, Y., Yin, S., Xie, S. and Xie, H. 2018. Comparative genomics of 84 Pectobacterium genomes reveals the variations related to a pathogenic lifestyle. BMC Genomics 19:889.   DOI
19 Hogan, C. S., Mole, B. M., Grant, S. R., Willis, D. K. and Charkowski, A. O. 2013. The type III secreted effector DspE is required early in Solanum tuberosum leaf infection by Pectobacterium carotovorum to cause cell death, and requires Wx(3-6)D/E motifs. PLoS ONE 8:e65534.   DOI
20 Aziz, R. K., Bartels, D., Best, A. A., DeJongh, M., Disz, T., Edwards, R. A., Formsma, K., Gerdes, S., Glass, E. M., Kubal, M., Meyer, F., Olsen, G. J., Olson, R., Osterman, A. L., Overbeek, R. A., McNeil, L. K., Paarmann, D., Paczian, T., Parrello, B., Pusch, G. D., Reich, C., Stevens, R., Vassieva, O., Vonstein, V., Wilke, A. and Zagnitko, O. 2008. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9:75.   DOI
21 Nivaskumar, M. and Francetic, O. 2014. Type II secretion system: a magic beanstalk or a protein escalator. Biochim. Biophys. Acta 1843:1568-1577.   DOI
22 Carattoli, A., Zankari, E., Garcia-Fernandez, A., Voldby Larsen, M., Lund, O., Villa, L., Moller Aarestrup, F. and Hasman, H. 2014. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob. Agents Chemother. 58:3895-3903.   DOI
23 Rodriguez, R, L. M. and Konstantinidis, K. T. 2016. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Prepr. 4:e1900v1.
24 Waleron, M., Misztak, A., Waleron, M., Franczuk, M., Wielgomas, B. and Waleron, K. 2018. Transfer of Pectobacterium carotovorum subsp. carotovorum strains isolated from potatoes grown at high altitudes to Pectobacterium peruviense sp. nov. Syst. Appl. Microbiol. 41:85-93.   DOI
25 Wang, J., Li, J., Hou, Y., Dai, W., Xie, R., Marquez-Lago, T. T., Leier, A., Zhou, T., Torres, V., Hay, I., Stubenrauch, C., Zhang, Y., Song, J. and Lithgow, T. 2021. BastionHub: a universal platform for integrating and analyzing substrates secreted by Gram-negative bacteria. Nucleic Acids Res. 49:D651-D659.   DOI
26 Zhang, H., Yohe, T., Huang, L., Entwistle, S., Wu, P., Yang, Z., Busk, P. K., Xu, Y. and Yin, Y. 2018. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 46:W95-W101.   DOI
27 Kanehisa, M., Goto, S., Kawashima, S., Okuno, Y. and Hattori, M. 2004. The KEGG resource for deciphering the genome. Nucleic Acids Res. 32:D277-D280.   DOI
28 Almagro Armenteros, J. J., Tsirigos, K. D., Sonderby, C. K., Petersen, T. N., Winther, O., Brunak, S., von Heijne, G. and Nielsen, H. 2019. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat. Biotechnol. 37:420-423.   DOI
29 Koiv, V., Andresen, L., Broberg, M., Frolova, J., Somervuo, P., Auvinen, P., Pirhonen, M., Tenson, T. and Mae, A. 2013. Lack of RsmA-mediated control results in constant hypervirulence, cell elongation, and hyperflagellation in Pectobacterium wasabiae. PLoS ONE 8:e54248.   DOI
30 Mole, B., Habibi, S., Dangl, J. L. and Grant, S. R. 2010. Gluconate metabolism is required for virulence of the soft-rot pathogen Pectobacterium carotovorum. Mol. Plant-Microbe Interact. 23:1335-1344.   DOI
31 Oh, C.-S. and Beer, S. V. 2005. Molecular genetics of Erwinia amylovora involved in the development of fire blight. FEMS Microbiol. Lett. 253:185-192.   DOI
32 Panda, P., Lu, A., Armstrong, K. F. and Pitman, A. R. 2015. Draft genome sequence for ICMP 5702, the type strain of Pectobacterium carotovorum subsp. carotovorum that causes soft rot disease on potato. Genome Announc. 3:e00875-15.
33 Toth, I. K., Bell, K. S., Holeva, M. C. and Birch, P. R. J. 2003. Soft rot erwiniae: from genes to genomes. Mol. Plant Pathol. 4:17-30.   DOI
34 Alcock, B. P., Raphenya, A. R., Lau, T., Tsang, K. K., Bouchard, M., Edalatmand, A., Huynh, W., Nguyen, A. V., Cheng, A. A., Liu, S., Min, S. Y., Miroshnichenko, A., Tran, H. K., Werfalli, R. E., Nasir, J. A., Oloni, M., Speicher, D. J., Florescu, A., Singh, B., Faltyn, M., Hernandez-Koutoucheva, A., Sharma, A. N., Bordeleau, E., Pawlowski, A. C., Zubyk, H. L., Dooley, D., Griffiths, E., Maguire, F., Winsor, G. L., Beiko, R. G., Brinkman, F. S. L., Hsiao, W. W. L., Domselaar, G. V. and McArthur, A. G. 2020. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res. 48:D517-D525.
35 Benson, G. 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27:573-580.   DOI
36 Coburn, B., Sekirov, I. and Finlay, B. B. 2007. Type III secretion systems and disease. Clin. Microbiol. Rev. 20:535-549.   DOI
37 Crepin, A., Barbey, C., Beury-Cirou, A., Helias, V., Taupin, L., Reverchon, S., Nasser, W., Faure, D., Dufour, A., Orange, N., Feuilloley, M., Heurlier, K., Burini, J.-F. and Latour, X. 2012. Quorum sensing signaling molecules produced by reference and emerging soft-rot bacteria (Dickeya and Pectobacterium spp.). PLoS ONE 7:e35176.   DOI
38 Mashavha, M. L. 2013. Characterisation of Pectobacterium carotovorum subsp. brasiliense isolates causing blackleg and soft rot diseases of potato in South Africa. M.S. thesis. University of Pretoria, Pretoria, South Africa.
39 Nykyri, J., Niemi, O., Koskinen, P., Nokso-Koivisto, J., Pasanen, M., Broberg, M., Plyusnin, I., Toronen, P., Holm, L., Pirhonen, M. and Palva, E. T. 2012. Revised phylogeny and novel horizontally acquired virulence determinants of the model soft rot phytopathogen Pectobacterium wasabiae SCC3193. PLoS Pathog. 8:e1003013.   DOI
40 Salzberg, S. L. 2019. Next-generation genome annotation: we still struggle to get it right. Genome Biol. 20:92.   DOI
41 Vercoe, R. B., Chang, J. T., Dy, R. L., Taylor, C., Gristwood, T., Clulow, J. S., Richter, C., Przybilski, R., Pitman, A. R. and Fineran, P. C. 2013. Cytotoxic chromosomal targeting by CRISPR/Cas systems can reshape bacterial genomes and expel or remodel pathogenicity islands. PLoS Genet. 9:e1003454.   DOI
42 Davidsson, P. R., Kariola, T., Niemi, O. and Palva, E. T. 2013. Pathogenicity of and plant immunity to soft rot pectobacteria. Front. Plant Sci. 4:191.   DOI
43 Darling, A. C. E., Mau, B., Blattner, F. R. and Perna, N. T. 2004. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 14:1394-1403.   DOI
44 Portier, P., Pedron, J., Taghouti, G., Fischer-Le Saux, M., Caullireau, E., Bertrand, C., Laurent, A., Chawki, K., Oulgazi, S., Moumni, M., Andrivon, D., Dutrieux, C., Faure, D., Helias, V. and Barny, M.-A. 2019. Elevation of Pectobacterium carotovorum subsp. odoriferum to species level as Pectobacterium odoriferum sp. nov., proposal of Pectobacterium brasiliense sp. nov. and Pectobacterium actinidiae sp. nov., emended description of Pectobacterium carotovorum and description of Pectobacterium versatile sp. nov., isolated from streams and symptoms on diverse plants. Int. J. Syst. Evol. Microbiol. 69:3207-3216.   DOI
45 Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-1313.   DOI
46 Toronen, P., Medlar, A. and Holm, L. 2018. PANNZER2: a rapid functional annotation web server. Nucleic Acids Res. 46:W84-W88.   DOI