Acknowledgement
We are very grateful to Kyung Hye Lee and Hee Yeon Kim for their technical support and helpful comments. This research was supported by Basic Science Research Program through the National Research Foundation of Korea (Y.L: 2018R1D1A1A02085563) funded by the Ministry of Education, Republic of Korea, Korea University Grant (E.-H.C: K2021521 and K2106871), and the BK21 FOUR program (E.-H.C: 4299991014324).
References
- Abbott, D. W. and Boraston, A. B. 2008. Structural biology of pectin degradation by Enterobacteriaceae. Microbiol. Mol. Biol. Rev. 72:301-316. https://doi.org/10.1128/MMBR.00038-07
- Adeolu, M., Alnajar, S., Naushad, S. and Gupta, R. S. 2016. Genome-based phylogeny and taxonomy of the 'Enterobacteriales': proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int. J. Syst. Evol. Microbiol. 66:5575-5599. https://doi.org/10.1099/ijsem.0.001485
- Andersen, G. L., Beattie, G. A. and Lindow, S. E. 1998. Molecular characterization and sequence of a methionine biosynthetic locus from Pseudomonas syringae. J. Bacteriol. 180:4497-4507. https://doi.org/10.1128/jb.180.17.4497-4507.1998
- Barras, F., van Gijsegem, F. and Chatterjee, A. K. 1994. Extracellular enzymes and pathogenesis of soft-rot Erwinia. Annu. Rev. Phytopathol. 32:201-234. https://doi.org/10.1146/annurev.py.32.090194.001221
- Basavanna, S., Chimalapati, S., Maqbool, A., Rubbo, B., Yuste, J., Wilson, R. J., Hosie, A., Ogunniyi, A. D., Paton, J. C., Thomas, G. and Brown, J. S. 2013. The effects of methionine acquisition and synthesis on Streptococcus pneumoniae growth and virulence. PLoS ONE 8:e49638.
- Bell, K. S., Sebaihia, M., Pritchard, L., Holden, M. T. G., Hyman, L. J., Holeva, M. C., Thomson, N. R., Bentley, S. D., Churcher, L. J. C., Mungall, K., Atkin, R., Bason, N., Brooks, K., Chillingworth, T., Clark, K., Doggett, J., Fraser, A., Hance, Z., Hauser, H., Jagels, K., Moule, S., Norbertczak, H., Ormond, D., Price, C., Quail, M. A., Sanders, M., Walker, D., Whitehead, S., Salmond, G. P. C., Birch, P. R. J., Parkhill, J. and Toth, I. K. 2004. Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc. Natl. Acad. Sci. U. S. A. 101:11105-11110. https://doi.org/10.1073/pnas.0402424101
- Bellieny-Rabelo, D., Nkomo, N. P., Shyntum, D. Y. and Moleleki, L. N. 2020. Horizontally acquired quorum-sensing regulators recruited by the PhoP regulatory network expand the host adaptation repertoire in the phytopathogen Pectobacterium brasiliense. mSystems 5:e00650-19.
- Bennett, B. D., Kimball, E. H., Gao, M., Osterhout, R., Van Dien, S. J. and Rabinowitz, J. D. 2009. Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat. Chem. Biol. 5:593-599. https://doi.org/10.1038/nchembio.186
- Bernal, P., Llamas, M. A. and Filloux, A. 2018. Type VI secretion systems in plant-associated bacteria. Environ. Microbiol. 20:1-15. https://doi.org/10.1111/1462-2920.13956
- Bowden, G. and Li, Y. H. 1997. Nutritional influences on biofilm development. Adv. Dent. Res. 11:81-99. https://doi.org/10.1177/08959374970110012101
- Charkowski, A., Blanco, C., Condemine, G., Expert, D., Franza, T., Hayes, C., Hugouvieux-Cotte-Pattat, N., Lopez Solanilla, E., Low, D., Moleleki, L., Pirhonen, M., Pitman, A., Perna, N., Reverchon, S., Rodriguez Palenzuela, P., San Francisco, M., Toth, I., Tsuyumu, S., van der Waals, J., van der Wolf, J., van Gijsegem, F., Yang, C.-H. and Yedidia, I. 2012. The role of secretion systems and small molecules in soft-rot Enterobacteriaceae pathogenicity. Annu. Rev. Phytopathol. 50:425-449. https://doi.org/10.1146/annurev-phyto-081211-173013
- Charkowski, A. O. 2007. The soft rot Erwinia. In: Plant-associated bacteria, ed. by S. S. Gnanamanickam, pp. 423-505. Springer, Dordrecht, Germany.
- Charkowski, A. O. 2018. The changing face of bacterial soft-rot diseases. Annu. Rev. Phytopathol. 56:269-288. https://doi.org/10.1146/annurev-phyto-080417-045906
- Chun, B. H., Han, D. M., Kim, K. H., Jeong, S. E., Park, D. and Jeon, C. O. 2019. Genomic and metabolic features of Tetragenococcus halophilus as revealed by pan-genome and transcriptome analyses. Food Microbiol. 83:36-47. https://doi.org/10.1016/j.fm.2019.04.009
- Coplin, D. L., Sequeira, L. and Hanson, R. S. 1974. Pseudomonas solanacearum: virulence of biochemical mutants. Can. J. Microbiol. 20:519-529. https://doi.org/10.1139/m74-080
- Cubitt, M. F., Hedley, P. E., Williamson, N. R., Morris, J. A., Campbell, E., Toth, I. K. and Salmond, G. P. C. 2013. A metabolic regulator modulates virulence and quorum sensing signal production in Pectobacterium atrosepticum. Mol. Plant-Microbe Interact. 26:356-366. https://doi.org/10.1094/MPMI-09-12-0210-R
- den Hengst, C. D., Groeneveld, M., Kuipers, O. P. and Kok, J. 2006. Identification and functional characterization of the Lactococcus lactis CodY-regulated branched-chain amino acid permease BcaP (CtrA). J. Bacteriol. 188:3280-3289. https://doi.org/10.1128/JB.188.9.3280-3289.2006
- Duarte, V., De Boer, S. H., Ward, L. J. and De Oliveira, A. M. R. 2004. Characterization of atypical Erwinia carotovora strains causing blackleg of potato in Brazil. J. Appl. Microbiol. 96:535-545. https://doi.org/10.1111/j.1365-2672.2004.02173.x
- Eisfeld, C., Schijven, J. F., van der Wolf, J. M., Medema, G., Kruisdijk, E. and van Breukelen, B. M. 2022. Removal of bacterial plant pathogens in columns filled with quartz and natural sediments under anoxic and oxygenated conditions. Water Res. 220:118724.
- Ejim, L. J., D'Costa, V. M., Elowe, N. H., Loredo-Osti, J. C., Malo, D. and Wright, G. D. 2004. Cystathionine beta-lyase is important for virulence of Salmonella enterica serovar Typhimurium. Infect. Immun. 72:3310-3314. https://doi.org/10.1128/IAI.72.6.3310-3314.2004
- Fatima, U. and Senthil-Kumar, M. 2015. Plant and pathogen nutrient acquisition strategies. Front. Plant Sci. 6:750.
- Ferla, M. P. and Patrick, W. M. 2014. Bacterial methionine biosynthesis. Microbiology (Reading) 160(Pt 8):1571-1584. https://doi.org/10.1099/mic.0.077826-0
- Holeva, M. C., Bell, K. S., Hyman, L. J., Avrova, A. O., Whisson, S. C., Birch, P. R. and Toth, I. K. 2004. Use of a pooled transposon mutation grid to demonstrate roles in disease development for Erwinia carotovora subsp. atroseptica putative type III secreted effector (DspE/A) and helper (HrpN) proteins. Mol. Plant-Microbe Interact. 17:943-950. https://doi.org/10.1094/MPMI.2004.17.9.943
- Hossain, M. M., Shibata, S., Aizawa, S.-I. and Tsuyumu, S. 2005. Motility is an important determinant for pathogenesis of Erwinia carotovora subsp. carotovora. Physiol. Mol. Plant Pathol. 66:134-143. https://doi.org/10.1016/j.pmpp.2005.06.001
- Hullo, M.-F., Auger, S., Dassa, E., Danchin, A. and Martin-Verstraete, I. 2004. The metNPQ operon of Bacillus subtilis encodes an ABC permease transporting methionine sulfoxide, D- and L-methionine. Res. Microbiol. 155:80-86. https://doi.org/10.1016/j.resmic.2003.11.008
- Husna, A. U., Wang, N., Cobbold, S. A., Newton, H. J., Hocking, D. M., Wilksch, J. J., Scott, T. A., Davies, M. R., Hinton, J. C., Tree, J. J., Lithgow, T., McConville, M. J. and Strugnell, R. A. 2018. Methionine biosynthesis and transport are functionally redundant for the growth and virulence of Salmonella Typhimurium. J. Biol. Chem. 293:9506-9519. https://doi.org/10.1074/jbc.RA118.002592
- Islam, R., Brown, S., Taheri, A. and Dumenyo, C. K. 2019. The gene encoding NAD-dependent epimerase/dehydratase, wcaG, affects cell surface properties, virulence, and extracellular enzyme production in the soft rot phytopathogen, Pectobacterium carotovorum. Microorganisms 7:172.
- Islamov, B., Petrova, O., Mikshina, P., Kadyirov, A., Vorob'ev, V., Gogolev, Y. and Gorshkov, V. 2021. The role of Pectobacterium atrosepticum exopolysaccharides in plant-pathogen interactions. Int. J. Mol. Sci. 22:12781.
- Jee, S., Choi, J.-G., Lee, Y.-G., Kwon, M., Hwang, I. and Heu, S. 2020. Distribution of Pectobacterium species isolated in South Korea and comparison of temperature effects on pathogenicity. Plant Pathol. J. 36:346-354. https://doi.org/10.5423/PPJ.OA.09.2019.0235
- Jochim, A., Shi, T., Belikova, D., Schwarz, S., Peschel, A. and Heilbronner, S. 2019. Methionine limitation impairs pathogen expansion and biofilm formation capacity. Appl. Environ. Microbiol. 85:e00177-19.
- Kim, H., Kim, M., Jee, S.-N., Heu, S. and Ryu, S. 2022. Development of a bacteriophage cocktail against Pectobacterium carotovorum subsp. carotovorum and its effects on Pectobacterium virulence. Appl. Environ. Microbiol. 88:e0076122.
- Kovach, M. E., Elzer, P. H., Hill, D. S., Robertson, G. T., Farris, M. A., Roop, R. M. 2nd and Peterson, K. M. 1995. Four new derivatives of the broad-host-range cloning vector pB-BR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176. https://doi.org/10.1016/0378-1119(95)00584-1
- Lee, D. H., Kim, J.-B., Lim, J.-A., Han, S.-W. and Heu, S. 2014. Genetic diversity of Pectobacterium carotovorum subsp. brasiliensis isolated in Korea. Plant Pathol. J. 30:117-124. https://doi.org/10.5423/PPJ.OA.12.2013.0117
- 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 (Reading) 159(Pt 7):1487-1496. https://doi.org/10.1099/mic.0.067280-0
- Lee, S. M., Choi, Y. H., Kim, H., Kim, H. T. and Choi, G. J. 2020. Development of an efficient bioassay method for testing resistance to bacterial spot rot of Chinese cabbage. Res. Plant Dis. 26:159-169.
- Lee, Y., Kim, Y., Yeom, S., Kim, S., Park, S., Jeon, C. O. and Park, W. 2008. The role of disulfide bond isomerase A (DsbA) of Escherichia coli O157:H7 in biofilm formation and virulence. FEMS Microbiol. Lett. 278:213-222. https://doi.org/10.1111/j.1574-6968.2007.00993.x
- Lee, Y., Oh, S. and Park, W. 2009. Inactivation of the Pseudomonas putida KT2440 dsbA gene promotes extracellular matrix production and biofilm formation. FEMS Microbiol. Lett. 297:38-48. https://doi.org/10.1111/j.1574-6968.2009.01650.x
- Lee, Y., Seo, H., Yeom, J. and Park, W. 2011. Molecular characterization of the extracellular matrix in a Pseudomonas putida dsbA mutant: implications for acidic stress defense and plant growth promotion. Res. Microbiol. 162:302-310. https://doi.org/10.1016/j.resmic.2010.11.002
- Li, H. and Durbin, R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760. https://doi.org/10.1093/bioinformatics/btp324
- Liu, F., Hu, M., Zhang, Z., Xue, Y., Chen, S., Hu, A., Zhang, L.- H. and Zhou, J. 2022. Dickeya manipulates multiple quorum sensing systems to control virulence and collective behaviors. Front. Plant Sci. 13:838125.
- Liu, Q., Chen, N., Chen, H. and Huang, Y. 2020. RNA-Seq analysis of differentially expressed genes of Staphylococcus epidermidis isolated from postoperative endophthalmitis and the healthy conjunctiva. Sci. Rep. 10:14234.
- Lopez-Solanilla, E., Garcia-Olmedo, F. and Rodriguez-Palenzuela, P. 1998. Inactivation of the sapA to sapF locus of Erwinia chrysanthemi reveals common features in plant and animal bacterial pathogenesis. Plant Cell 10:917-924. https://doi.org/10.2307/3870678
- Ma, B., Hibbing, M. E., Kim, H.-S., Reedy, R. M., Yedidia, I., Breuer, J., Breuer, J., Glasner, J. D., Perna, N. T., Kelman, A. and Charkowski, A. O. 2007. Host range and molecular phylogenies of the soft rot enterobacterial genera Pectobacterium and Dickeya. Phytopathology 97:1150-1163. https://doi.org/10.1094/PHYTO-97-9-1150
- Malko, A., Frantsuzov, P., Nikitin, M., Statsyuk, N., Dzhavakhiya, V. and Golikov, A. 2019. Potato pathogens in Russia's regions: an instrumental survey with the use of real-time PCR/RT-PCR in matrix format. Pathogens 8:18.
- Mansfield, J., Genin, S., Magori, S., Citovsky, V., Sriariyanum, M., Ronald, P., Dow, M., Verdier, V., Beer, S. V., Machado, M. A., Toth, I., Salmond, G. and Foster, G. D. 2012. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol. Plant Pathol. 13:614-629. https://doi.org/10.1111/j.1364-3703.2012.00804.x
- Markovic, S., Stankovic, S., Jelusic, A., Ilicic, R., Kosovac, A., Postic, D. and Popovic, T. 2021. Occurrence and identification of Pectobacterium carotovorum subsp. brasiliensis and Dickeya dianthicola causing blackleg in some potato fields in Serbia. Plant Dis. 105:1080-1090. https://doi.org/10.1094/PDIS-05-20-1076-RE
- Mattinen, L., Nissinen, R., Riipi, T., Kalkkinen, N. and Pirhonen, M. 2007. Host-extract induced changes in the secretome of the plant pathogenic bacterium Pectobacterium atrosepticum. Proteomics 7:3527-3537. https://doi.org/10.1002/pmic.200600759
- Mattinen, L., Somervuo, P., Nykyri, J., Nissinen, R., Kouvonen, P., Corthals, G., Auvinen, P., Aittamaa, M., Valkonen, J. P. T. and Pirhonen, M. 2008. Microarray profiling of host-extract-induced genes and characterization of the type VI secretion cluster in the potato pathogen Pectobacterium atrosepticum. Microbiology (Reading) 154(Pt 8):2387-2396. https://doi.org/10.1099/mic.0.2008/017582-0
- Merlin, C., Gardiner, G., Durand, S. and Masters, M. 2002. The Escherichia coli metD locus encodes an ABC transporter which includes Abc (MetN), YaeE (MetI), and YaeC (MetQ). J. Bacteriol. 184:5513-5517. https://doi.org/10.1128/JB.184.19.5513-5517.2002
- Mole, B. M., Baltrus, D. A., Dangl, J. L. and Grant, S. R. 2007. Global virulence regulation networks in phytopathogenic bacteria. Trends Microbiol. 15:363-371. https://doi.org/10.1016/j.tim.2007.06.005
- Monson, R., Burr, T., Carlton, T., Liu, H., Hedley, P., Toth, I. and Salmond, G. P. C. 2013. Identification of genes in the VirR regulon of Pectobacterium atrosepticum and characterization of their roles in quorum sensing-dependent virulence. Environ. Microbiol. 15:687-701. https://doi.org/10.1111/j.1462-2920.2012.02822.x
- Mulholland, V., Hinton, J. C., Sidebotham, J., Toth, I. K., Hyman, L. J., Perombelon, M. C., Reeves, P. J. and Salmond, G. P. C. 1993. A pleiotropic reduced virulence (Rvi-) mutant of Erwinia carotovora subspecies atroseptica is defective in flagella assembly proteins that are conserved in plant and animal bacterial pathogens. Mol. Microbiol. 9:343-356. https://doi.org/10.1111/j.1365-2958.1993.tb01695.x
- Muturi, P., Yu, J., Li, J., Jiang, M., Maina, A. N., Kariuki, S., Mwaura, F. B. and Wei, H. 2018. Isolation and characterization of pectolytic bacterial pathogens infecting potatoes in Nakuru County, Kenya. J. Appl. Microbiol. 124:1580-1588. https://doi.org/10.1111/jam.13730
- Park, T.-H., Choi, B.-S., Choi, A.-Y., Choi, I.-Y., Heu, S. and Park, B.-S. 2012. Genome sequence of Pectobacterium carotovorum subsp. carotovorum strain PCC21, a pathogen causing soft rot in Chinese cabbage. J. Bacteriol. 194:6345-6346. https://doi.org/10.1128/JB.01583-12
- Perombelon, M. C. M. 2002. Potato diseases caused by soft rot erwinias: an overview of pathogenesis. Plant Pathol. 51:1-12. https://doi.org/10.1046/j.0032-0862.2001.Short title.doc.x
- Perombelon, M. C. M. and Kelman, A. 1980. Ecology of the soft rot Erwinias. Annu. Rev. Phytopathol. 18:361-387. https://doi.org/10.1146/annurev.py.18.090180.002045
- Plener, L., Boistard, P., Gonzalez, A., Boucher, C. and Genin, S. 2012. Metabolic adaptation of Ralstonia solanacearum during plant infection: a methionine biosynthesis case study. PLoS ONE 7:e36877.
- 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. https://doi.org/10.1099/ijsem.0.003611
- Rochex, A. and Lebeault, J.-M. 2007. Effects of nutrients on biofilm formation and detachment of a Pseudomonas putida strain isolated from a paper machine. Water Res. 41:2885-2892. https://doi.org/10.1016/j.watres.2007.03.041
- Rossmann, S., Dees, M. W., Perminow, J., Meadow, R. and Brurberg, M. B. 2018. Soft rot Enterobacteriaceae are carried by a large range of insect species in potato fields. Appl. Environ. Microbiol. 84:e00281-18.
- Ryu, C.-M. 2015. Against friend and foe: type 6 effectors in plant-associated bacteria. J. Microbiol. 53:201-208. https://doi.org/10.1007/s12275-015-5055-y
- Shyntum, D. Y., Nkomo, N. P., Shingange, N. L., Gricia, A. R., Bellieny-Rabelo, D. and Moleleki, L. N. 2019. The impact of type VI secretion system, bacteriocins and antibiotics on bacterial competition of Pectobacterium carotovorum subsp. brasiliense and the regulation of carbapenem biosynthesis by iron and the ferric-uptake regulator. Front. Microbiol. 10:2379.
- Tate, R., Riccio, A., Caputo, E., Iaccarino, M. and Patriarca, E. J. 1999. The Rhizobium etli metZ gene is essential for methionine biosynthesis and nodulation of Phaseolus vulgaris. Mol. Plant-Microbe Interact. 12:24-34. https://doi.org/10.1094/MPMI.1999.12.1.24
- Torres, M., Uroz, S., Salto, R., Fauchery, L., Quesada, E. and Llamas, I. 2017. HqiA, a novel quorum-quenching enzyme which expands the AHL lactonase family. Sci. Rep. 7:943.
- Toth, I. K., Bell, K. S., Holeva, M. C. and Birch, P. R. 2003. Soft rot erwiniae: from genes to genomes. Mol. Plant Pathol. 4:17-30. https://doi.org/10.1046/j.1364-3703.2003.00149.x
- Valecillos, A. M., Palenzuela, P. R. and Lopez-Solanilla, E. 2006. The role of several multidrug resistance systems in Erwinia chrysanthemi pathogenesis. Mol. Plant-Microbe Interact. 19:607-613. https://doi.org/10.1094/MPMI-19-0607
- van der Merwe, J. J., Coutinho, T. A., Korsten, L. and van der Waals, J. E. 2010. Pectobacterium carotovorum subsp. brasiliensis causing blackleg on potatoes in South Africa. Eur. J. Plant Pathol. 126:175-185. https://doi.org/10.1007/s10658-009-9531-2
- Wang, C., Pu, T., Lou, W., Wang, Y., Gao, Z., Hu, B. and Fan, J. 2018. Hfq, a RNA chaperone, contributes to virulence by regulating plant cell wall-degrading enzyme production, type VI secretion system expression, bacterial competition, and suppressing host defense response in Pectobacterium carotovorum. Mol. Plant-Microbe Interact. 31:1166-1178. https://doi.org/10.1094/MPMI-12-17-0303-R
- Weissbach, H. and Brot, N. 1991. Regulation of methionine synthesis in Escherichia coli. Mol. Microbiol. 5:1593-1597. https://doi.org/10.1111/j.1365-2958.1991.tb01905.x
- Yi, X., Yamazaki, A., Biddle, E., Zeng, Q. and Yang, C.-H. 2010. Genetic analysis of two phosphodiesterases reveals cyclic diguanylate regulation of virulence factors in Dickeya dadantii. Mol. Microbiol. 77:787-800. https://doi.org/10.1111/j.1365-2958.2010.07246.x