Resistance of Dickeya solani strain IPO 2222 to lytic bacteriophage ΦD5 results in fitness tradeoffs for the bacterium during infection
Campbell, A. The future of bacteriophage biology. Nat. Rev. Genet. 4, 471–477. https://doi.org/10.1038/nrg1089 (2003).
Google Scholar
Cheetham, B. F. & Katz, M. E. A role for bacteriophages in the evolution and transfer of bacterial virulence determinants. Mol. Microbiol. 18, 201–208. https://doi.org/10.1111/j.1365-2958.1995.mmi_18020201.x (1995).
Google Scholar
Mann, N. H. The third age of phage. PLoS Biol. 3, e182. https://doi.org/10.1371/journal.pbio.0030182 (2005).
Google Scholar
Thurber, R. V. Current insights into phage biodiversity and biogeography. Curr. Opin. Microbiol. 12, 582–587. https://doi.org/10.1016/j.mib.2009.08.008 (2009).
Google Scholar
Buckling, A. & Rainey, P. B. Antagonistic coevolution between a bacterium and a bacteriophage. Proc. Biol. Sci. 269, 931–936. https://doi.org/10.1098/rspb.2001.1945 (2002).
Google Scholar
Dennehy, J. J. What can phages tell us about host-pathogen coevolution?. Int. J. Evol. Biol. 2012, 396165. https://doi.org/10.1155/2012/396165 (2012).
Google Scholar
Forde, S. E., Thompson, J. N., Holt, R. D. & Bohannan, B. J. Coevolution drives temporal changes in fitness and diversity across environments in a bacteria-bacteriophage interaction. Evolution 62, 1830–1839. https://doi.org/10.1111/j.1558-5646.2008.00411.x (2008).
Google Scholar
Suttle, C. A. The significance of viruses to mortality in aquatic microbial communities. Microb. Ecol. 28, 237–243. https://doi.org/10.1007/BF00166813 (1994).
Google Scholar
Duffy, M. A. & Forde, S. E. Ecological feedbacks and the evolution of resistance. J. Anim. Ecol. 78, 1106–1112. https://doi.org/10.1111/j.1365-2656.2009.01568.x (2009).
Google Scholar
Koskella, B. & Brockhurst, M. A. Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol. Rev. 38, 916–931. https://doi.org/10.1111/1574-6976.12072 (2014).
Google Scholar
Chibani-Chennoufi, S., Bruttin, A., Dillmann, M. L. & Brussow, H. Phage-host interaction: an ecological perspective. J. Bacteriol. 186, 3677–3686. https://doi.org/10.1128/JB.186.12.3677-3686.2004 (2004).
Google Scholar
Waterbury, J. B. & Valois, F. W. Resistance to co-occurring phages enables marine synechococcus communities to coexist with cyanophages abundant in seawater. Appl. Environ. Microbiol. 59, 3393–3399. https://doi.org/10.1128/aem.59.10.3393-3399.1993 (1993).
Google Scholar
Koskella, B. & Parr, N. The evolution of bacterial resistance against bacteriophages in the horse chestnut phyllosphere is general across both space and time. Phil. Trans. R. Soc. B 370, 20140297 (2015).
Google Scholar
Hantula, J., Kurki, A., Vuoriranta, P. & Bamford, D. H. Ecology of bacteriophages infecting activated sludge bacteria. Appl. Environ. Microbiol. 57, 2147–2151. https://doi.org/10.1128/aem.57.8.2147-2151.1991 (1991).
Google Scholar
Fernandez, L., Gutierrez, D., Rodriguez, A. & Garcia, P. Application of bacteriophages in the agro-food sector: a long way toward approval. Front. Cell Infect. Microbiol. 8, 296. https://doi.org/10.3389/fcimb.2018.00296 (2018).
Google Scholar
Jones, J. B. et al. Bacteriophages for plant disease control. Annu Rev. Phytopathol. 45, 245–262. https://doi.org/10.1146/annurev.phyto.45.062806.094411 (2007).
Google Scholar
Bradde, S., Vucelja, M., Tesileanu, T. & Balasubramanian, V. Dynamics of adaptive immunity against phage in bacterial populations. PLoS Comput. Biol. 13, e1005486. https://doi.org/10.1371/journal.pcbi.1005486 (2017).
Google Scholar
Naureen, Z. et al. Bacteriophages presence in nature and their role in the natural selection of bacterial populations. Acta Biomed. 91, e2020024. https://doi.org/10.23750/abm.v91i13-S.10819 (2020).
Google Scholar
Stern, A. & Sorek, R. The phage-host arms race: shaping the evolution of microbes. BioEssays 33, 43–51. https://doi.org/10.1002/bies.201000071 (2011).
Google Scholar
Burmeister, A. R. & Turner, P. E. Trading-off and trading-up in the world of bacteria-phage evolution. Curr. Biol. 30, R1120–R1124. https://doi.org/10.1016/j.cub.2020.07.036 (2020).
Google Scholar
Koderi Valappil, S. et al. Survival comes at a cost: a coevolution of phage and its host leads to phage resistance and antibiotic sensitivity of Pseudomonas aeruginosa multidrug resistant strains. Front. Microbiol. 12, 783722. https://doi.org/10.3389/fmicb.2021.783722 (2021).
Google Scholar
Labrie, S. J., Samson, J. E. & Moineau, S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8, 317–327. https://doi.org/10.1038/nrmicro2315 (2010).
Google Scholar
Lythgoe, K. A. & Chao, L. Mechanisms of coexistence of a bacteria and a bacteriophage in a spatially homogeneous environment. Ecol. Lett. 6, 326–334. https://doi.org/10.1046/j.1461-0248.2003.00433.x (2003).
Google Scholar
Mizoguchi, K. et al. Coevolution of bacteriophage PP01 and Escherichia coli O157:H7 in continuous culture. Appl. Environ. Microbiol. 69, 170–176. https://doi.org/10.1128/AEM.69.1.170-176.2003 (2003).
Google Scholar
Lennon, J. T., Khatana, S. A., Marston, M. F. & Martiny, J. B. Is there a cost of virus resistance in marine cyanobacteria?. ISME J. 1, 300–312. https://doi.org/10.1038/ismej.2007.37 (2007).
Google Scholar
Vale, P. F. et al. Costs of CRISPR-Cas-mediated resistance in Streptococcus thermophilus. Proc. Biol. Sci. 282, 20151270. https://doi.org/10.1098/rspb.2015.1270 (2015).
Google Scholar
Keen, E. C. Tradeoffs in bacteriophage life histories. Bacteriophage 4, e28365. https://doi.org/10.4161/bact.28365 (2014).
Google Scholar
Abedon, S. T. Bacterial ‘immunity’ against bacteriophages. Bacteriophage 2, 50–54 (2012).
Google Scholar
Charkowski, A. O. The changing face of bacterial soft-rot diseases. Annu. Rev. Phytopathol. 56, 269–288. https://doi.org/10.1146/annurev-phyto-080417-045906 (2018).
Google Scholar
Mansfield, J. et al. 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 (2012).
Google Scholar
Perombelon, M. C. M. 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.Shorttitle.doc.x (2002).
Google Scholar
Perombelon, M. C. M. & Kelman, A. Ecology of the soft rot Erwinias. Annu. Rev. Phytopathol. 18, 361–387 (1980).
Google Scholar
Rossmann, S., Dees, M. W., Perminow, J., Meadow, R. & Brurberg, M. B. Soft Rot Enterobacteriaceae are carried by a large range of insect species in potato fields. Appl. Environ. Microbiol. 84, 1. https://doi.org/10.1128/AEM.00281-18 (2018).
Google Scholar
Fikowicz-Krosko, J., Wszalek-Rozek, K., Smolarska, A. & Czajkowski, R. First report of isolation of soft rot Pectobacterium carotovorum subsp carotovorum from symptomless bittersweet nightshade occuing in rural area of Poland. J. Plant Pathol. 99, 1 (2017).
Batinovic, S. et al. Bacteriophages in natural and artificial environments. Pathogens 8, 100. https://doi.org/10.3390/pathogens8030100 (2019).
Google Scholar
Wright, R. C. T., Friman, V. P., Smith, M. C. M. & Brockhurst, M. A. Resistance evolution against phage combinations depends on the timing and order of exposure. mBio 10, e01652–01619, https://doi.org/10.1128/mBio.01652-19 (2019).
Borin, J. M., Avrani, S., Barrick, J. E., Petrie, K. L. & Meyer, J. R. Coevolutionary phage training leads to greater bacterial suppression and delays the evolution of phage resistance. Proc. Natl. Acad. Sci. USA 118, e2104592118. https://doi.org/10.1073/pnas.2104592118 (2021).
Google Scholar
van der Wolf, J. M. et al. Dickeya solani sp. nov., a pectinolytic plant-pathogenic bacterium isolated from potato (Solanum tuberosum). Int J Syst Evol Microbiol 64, 768–774, https://doi.org/10.1099/ijs.0.052944-0 (2014).
Toth, I. K. et al. Dickeya species: an emerging problem for potato production in Europe. Plant. Pathol. 60, 385–399. https://doi.org/10.1111/j.1365-3059.2011.02427.x (2011).
Google Scholar
Czajkowski, R., van Veen, J. A. & van der Wolf, J. M. New biovar 3 Dickeya spp. strain (syn. Erwinia chrysanthemi) as a causative agent of blackleg in seed potato in Europe. Phytopathology 99, S27-S27 (2009).
Tsror Lahkim, L. et al. Characterization of Dickeya strains isolated from potato grown under hot-climate conditions. Plant Pathology 62, 1097–1105, doi:https://doi.org/10.1111/ppa.12030 (2013).
Tsror, L. et al. First report of potato blackleg caused by a biovar 3 Dickeya sp. in Georgia. New Disease Reports 23, 1 (2011).
Ozturk, M. & Aksoy, H. M. First report of Dickeya solani associated with potato blackleg and soft rot in Turkey. J. Plant Pathol. 99, 298 (2017).
Cardoza, Y. F., Duarte, V. & Lopes, C. A. First report of blackleg of potato caused by Dickeya solani in Brazil. Plant. Dis. 101, 243–243. https://doi.org/10.1094/pdis-07-16-1045-pdn (2017).
Google Scholar
Khayi, S., Blin, P., Chong, T. M., Chan, K. G. & Faure, D. Complete genome anatomy of the emerging potato pathogen Dickeya solani type strain IPO 2222(T). Stand. Genom. Sci. 11, 87. https://doi.org/10.1186/s40793-016-0208-0 (2016).
Google Scholar
Czajkowski, R., Ozymko, Z. & Lojkowska, E. Isolation and characterization of novel soilborne lytic bacteriophages infecting Dickeya spp. biovar 3 (‘D. solani’). Plant Pathol. 63, 758–772, doi:https://doi.org/10.1111/ppa.12157 (2014).
Czajkowski, R., Smolarska, A. & Ozymko, Z. The viability of lytic bacteriophage PhiD5 in potato-associated environments and its effect on Dickeya solani in potato (Solanum tuberosum L.) plants. PLoS ONE 12, e0183200, doi:https://doi.org/10.1371/journal.pone.0183200 (2017).
Adriaenssens, E. M. et al. A suggested new bacteriophage genus: “Viunalikevirus”. Arch Virol 157, 2035–2046. https://doi.org/10.1007/s00705-012-1360-5 (2012).
Google Scholar
Adriaenssens, E. M. et al. T4-related bacteriophage LIMEstone isolates for the control of soft rot on potato caused by “Dickeya solani”. PLoS ONE 7, e33227. https://doi.org/10.1371/journal.pone.0033227 (2012).
Google Scholar
Petrzik, K., Vacek, J., Brazdova, S., Sevcik, R. & Koloniuk, I. Diversity of limestone bacteriophages infecting Dickeya solani isolated in the Czech Republic. Arch Virol 166, 1171–1175. https://doi.org/10.1007/s00705-020-04926-7 (2021).
Google Scholar
Ranjan, M. et al. Genomic diversity and organization of complex polysaccharide biosynthesis clusters in the genus Dickeya. PLoS ONE 16, e0245727. https://doi.org/10.1371/journal.pone.0245727 (2021).
Google Scholar
Pedron, J., Chapelle, E., Alunni, B. & Van Gijsegem, F. Transcriptome analysis of the Dickeya dadantii PecS regulon during the early stages of interaction with Arabidopsis thaliana. Mol Plant Pathol 19, 647–663. https://doi.org/10.1111/mpp.12549 (2018).
Google Scholar
Czajkowski, R. Bacteriophages of Soft Rot Enterobacteriaceae-a minireview. FEMS Microbiol. Lett. 363, fnv230, doi:https://doi.org/10.1093/femsle/fnv230 (2016).
Toth, I. K. et al. in Plant Diseases Caused by Dickeya and Pectobacterium Species (eds Frédérique Van Gijsegem, Jan M. van der Wolf, & Ian K. Toth) Ch. Chapter 2, 13–37 (Springer International Publishing, 2021).
Holt, K. E., Lassalle, F., Wyres, K. L., Wick, R. & Mostowy, R. J. Diversity and evolution of surface polysaccharide synthesis loci in Enterobacteriales. ISME J. 14, 1713–1730. https://doi.org/10.1038/s41396-020-0628-0 (2020).
Google Scholar
Schnaitman, C. A. & Klena, J. D. Genetics of lipopolysaccharide biosynthesis in enteric bacteria. Microbiol. Rev. 57, 655–682. https://doi.org/10.1128/mr.57.3.655-682.1993 (1993).
Google Scholar
Mangalea, M. R. & Duerkop, B. A. Fitness trade-offs resulting from bacteriophage resistance potentiate synergistic antibacterial strategies. Infect. Immun. 88, e00926-e1919. https://doi.org/10.1128/IAI.00926-19 (2020).
Google Scholar
Bohannan, B. J. M. & Lenski, R. E. Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecol. Lett. 3, 362–377. https://doi.org/10.1046/j.1461-0248.2000.00161.x (2000).
Google Scholar
Bartnik, P., Jafra, S., Narajczyk, M., Czaplewska, P. & Czajkowski, R. Pectobacterium parmentieri SCC 3193 mutants with altered synthesis of cell surface polysaccharides are resistant to N4-like lytic bacteriophage phiA38 (vB_Ppp_A38) but express decreased virulence in potato (Solanum tuberosum L.) Plants. Int J Mol Sci 22, 7346, doi:https://doi.org/10.3390/ijms22147346 (2021).
Evans, T. J., Ind, A., Komitopoulou, E. & Salmond, G. P. C. Phage-selected lipopolysaccharide mutants of Pectobacterium atrosepticum exhibit different impacts on virulence. J. Appl. Microbiol. 109, 505–514. https://doi.org/10.1111/j.1365-2672.2010.04669.x (2010).
Google Scholar
Lukianova, A. A. et al. Morphologically Different Pectobacterium brasiliense bacteriophages PP99 and PP101: deacetylation of O-polysaccharide by the tail spike protein of phage PP99 accompanies the Infection. Front. Microbiol. 10, 3147. https://doi.org/10.3389/fmicb.2019.03147 (2019).
Google Scholar
Kim, H. et al. Colanic acid is a novel phage receptor of Pectobacterium carotovorum subsp. carotovorum phage POP72. Front. Microbiol. 10, 143, https://doi.org/10.3389/fmicb.2019.00143 (2019).
Costerton, J. W., Irvin, R. T. & Cheng, K. J. The role of bacterial surface structures in pathogenesis. Crit. Rev. Microbiol. 8, 303–338. https://doi.org/10.3109/10408418109085082 (1981).
Google Scholar
Beveridge, T. J. & Graham, L. L. Surface layers of bacteria. Microbiol. Rev. 55, 684–705. https://doi.org/10.1128/mr.55.4.684-705.1991 (1991).
Google Scholar
D’Haeze, W. & Holsters, M. Surface polysaccharides enable bacteria to evade plant immunity. Trends Microbiol. 12, 555–561. https://doi.org/10.1016/j.tim.2004.10.009 (2004).
Google Scholar
Li, J. & Wang, N. The gpsX gene encoding a glycosyltransferase is important for polysaccharide production and required for full virulence in Xanthomonas citri subsp. citri. BMC Microbiol. 12, 31 (2012).
Santaella, C., Schue, M., Berge, O., Heulin, T. & Achouak, W. The exopolysaccharide of Rhizobium sp. YAS34 is not necessary for biofilm formation on Arabidopsis thaliana and Brassica napus roots but contributes to root colonization. Environ. Microbiol. 10, 2150–2163, doi:https://doi.org/10.1111/j.1462-2920.2008.01650.x (2008).
Morona, J. K., Miller, D. C., Morona, R. & Paton, J. C. The effect that mutations in the conserved capsular polysaccharide biosynthesis genes cpsA, cpsB, and cpsD have on virulence of Streptococcus pneumoniae. J. Infect. Dis. 189, 1905–1913. https://doi.org/10.1086/383352 (2004).
Google Scholar
Lawlor, M. S., Handley, S. A. & Miller, V. L. Comparison of the host responses to wild-type and cpsB mutant Klebsiella pneumoniae infections. Infect. Immun. 74, 5402–5407. https://doi.org/10.1128/IAI.00244-06 (2006).
Google Scholar
Geider, K. et al. in Advances in Molecular Genetics of Plant-Microbe Interactions Vol. 1 Current Plant Science and Biotechnology in Agriculture (eds Hauke Hennecke & Desh Pal S. Verma) Ch. Chapter 14, 90–93 (Springer Netherlands, 1991).
Mohamed, K. H. et al. Deciphering the dual effect of lipopolysaccharides from plant pathogenic Pectobacterium. Plant Signal Behav. 10, e1000160. https://doi.org/10.1080/15592324.2014.1000160 (2015).
Google Scholar
Katzen, F. et al. Xanthomonas campestris pv. campestris gum mutants: effects on xanthan biosynthesis and plant virulence. J. Bacteriol. 180, 1607–1617. https://doi.org/10.1128/JB.180.7.1607-1617.1998 (1998).
Google Scholar
Whitfield, C., Wear, S. S. & Sande, C. Assembly of bacterial capsular polysaccharides and exopolysaccharides. Annu. Rev. Microbiol. 74, 521–543. https://doi.org/10.1146/annurev-micro-011420-075607 (2020).
Google Scholar
Ormeno-Orrillo, E., Rosenblueth, M., Luyten, E., Vanderleyden, J. & Martinez-Romero, E. Mutations in lipopolysaccharide biosynthetic genes impair maize rhizosphere and root colonization of Rhizobium tropici CIAT899. Environ. Microbiol. 10, 1271–1284. https://doi.org/10.1111/j.1462-2920.2007.01541.x (2008).
Google Scholar
Touze, T., Goude, R., Georgeault, S., Blanco, C. & Bonnassie, S. Erwinia chrysanthemi O antigen is required for betaine osmoprotection in high-salt media. J. Bacteriol. 186, 5547–5550. https://doi.org/10.1128/JB.186.16.5547-5550.2004 (2004).
Google Scholar
Bowden, M. G. & Kaplan, H. B. The Myxococcus xanthus lipopolysaccharide O-antigen is required for social motility and multicellular development. Mol. Microbiol. 30, 275–284. https://doi.org/10.1046/j.1365-2958.1998.01060.x (1998).
Google Scholar
Andrianopoulos, K., Wang, L. & Reeves, P. R. Identification of the fucose synthetase gene in the colanic acid gene cluster of Escherichia coli K-12. J. Bacteriol. 180, 998–1001. https://doi.org/10.1128/JB.180.4.998-1001.1998 (1998).
Google Scholar
Islam, R., Brown, S., Taheri, A. & Dumenyo, C. K. 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. https://doi.org/10.3390/microorganisms7060172 (2019).
Google Scholar
Qimron, U., Marintcheva, B., Tabor, S. & Richardson, C. C. Genomewide screens for Escherichia coli genes affecting growth of T7 bacteriophage. Proc. Natl. Acad. Sci. USA 103, 19039–19044. https://doi.org/10.1073/pnas.0609428103 (2006).
Google Scholar
Pagnout, C. et al. Pleiotropic effects of rfa-gene mutations on Escherichia coli envelope properties. Sci. Rep. 9, 9696. https://doi.org/10.1038/s41598-019-46100-3 (2019).
Google Scholar
Montanaro, L. & Arciola, C. R. in Handbook of Bacterial Adhesion: Principles, Methods, and Applications (eds Yuehuei H. An & Richard J. Friedman) 331–343 (Humana Press, 2000).
Berne, C., Ellison, C. K., Ducret, A. & Brun, Y. V. Bacterial adhesion at the single-cell level. Nat. Rev. Microbiol. 16, 616–627. https://doi.org/10.1038/s41579-018-0057-5 (2018).
Google Scholar
Brown, M. R. & Williams, P. The influence of environment on envelope properties affecting survival of bacteria in infections. Annu. Rev. Microbiol. 39, 527–556. https://doi.org/10.1146/annurev.mi.39.100185.002523 (1985).
Google Scholar
Czajkowski, R. et al. Genome-Wide identification of Dickeya solani transcriptional units up-regulated in response to plant tissues from a crop-host Solanum tuberosum and a weed-host Solanum dulcamara. Front. Plant. Sci. 11, 580330. https://doi.org/10.3389/fpls.2020.580330 (2020).
Google Scholar
Meaden, S. & Koskella, B. Exploring the risks of phage application in the environment. Front. Microbiol. 4, 358. https://doi.org/10.3389/fmicb.2013.00358 (2013).
Google Scholar
Reverchon, S., Muskhelisvili, G. & Nasser, W. in Progress in Molecular Biology and Translational Science Vol. 142 (eds Michael San Francisco & Brian San Francisco) 51–92 (Academic Press, 2016).
Jiang, X. et al. Global transcriptional response of Dickeya dadantii to environmental stimuli relevant to the plant infection. Environ. Microbiol. 18, 3651–3672. https://doi.org/10.1111/1462-2920.13267 (2016).
Google Scholar
Li, Y. et al. LPS remodeling is an evolved survival strategy for bacteria. Proc. Natl. Acad. Sci. USA 109, 8716–8721. https://doi.org/10.1073/pnas.1202908109 (2012).
Google Scholar
Hendrick, C. A. & Sequeira, L. Lipopolysaccharide-defective mutants of the wilt pathogen Pseudomonas solanacearum. Appl. Environ. Microbiol. 48, 94–101. https://doi.org/10.1128/aem.48.1.94-101.1984 (1984).
Google Scholar
Berry, M. C., McGhee, G. C., Zhao, Y. & Sundin, G. W. Effect of a waaL mutation on lipopolysaccharide composition, oxidative stress survival, and virulence in Erwinia amylovora. FEMS Microbiol. Lett. 291, 80–87. https://doi.org/10.1111/j.1574-6968.2008.01438.x (2009).
Google Scholar
Czajkowski, R., Ozymko, Z., Zwirowski, S. & Lojkowska, E. Complete genome sequence of a broad-host-range lytic Dickeya spp. bacteriophage phiD5. Arch. Virol. 159, 3153–3155, doi:https://doi.org/10.1007/s00705-014-2170-8 (2014).
Lisicka, W. et al. Oxygen availability influences expression of Dickeya solani genes associated with virulence in potato (Solanum tuberosum L.) and chicory (Cichorium intybus L.). Front. Plant. Sci. 9, 374, doi:https://doi.org/10.3389/fpls.2018.00374 (2018).
Czajkowski, R., Marcisz, M. & Bartnik, P. Fast and reliable screening assay developed to preselect candidate Soft Rot Pectobacteriaceae Tn5 mutants showing resistance to bacteriophage infection. Eur. J. Plant Pathol. 155, 671–676. https://doi.org/10.1007/s10658-019-01786-z (2019).
Google Scholar
Aziz, R. K. et al. The RAST Server: rapid annotations using subsystems technology. BMC Genom. 9, 75. https://doi.org/10.1186/1471-2164-9-75 (2008).
Google Scholar
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410. https://doi.org/10.1016/S0022-2836(05)80360-2 (1990).
Google Scholar
Kurowski, M. A. & Bujnicki, J. M. GeneSilico protein structure prediction meta-server. Nucl. Acids Res. 31, 3305–3307. https://doi.org/10.1093/nar/gkg557 (2003).
Google Scholar
Altschul, S. F. & Koonin, E. V. Iterated profile searches with PSI-BLAST-a tool for discovery in protein databases. Trends Biochem. Sci. 23, 444–447. https://doi.org/10.1016/s0968-0004(98)01298-5 (1998).
Google Scholar
Kanehisa, M. & Goto, S. KEGG: kyoto encyclopedia of genes and genomes. Nucl. Acids Res. 28, 27–30. https://doi.org/10.1093/nar/28.1.27 (2000).
Google Scholar
Letunic, I., Yamada, T., Kanehisa, M. & Bork, P. iPath: interactive exploration of biochemical pathways and networks. Trends Biochem. Sci. 33, 101–103. https://doi.org/10.1016/j.tibs.2008.01.001 (2008).
Google Scholar
Szklarczyk, D. et al. STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucl. Acids Res. 47, D607–D613. https://doi.org/10.1093/nar/gky1131 (2019).
Google Scholar
Czajkowski, R., Ozymko, Z. & Lojkowska, E. Isolation and characterization of novel soilborne lytic bacteriophages infecting Dickeya spp. biovar 3 (‘D. solani’). Plant Pathol. 63, 758–772, https://doi.org/10.1111/ppa.12157, (2014).
Shao, Y. & Wang, I. N. Bacteriophage adsorption rate and optimal lysis time. Genetics 180, 471–482. https://doi.org/10.1534/genetics.108.090100 (2008).
Google Scholar
Czajkowski, R., Kaczyńska, N., Jafra, S., Narajczyk, M. & Lojkowska, E. Temperature-responsive genetic loci in pectinolytic plant pathogenic Dickeya solani. Plant. Pathol. 66, 584–594. https://doi.org/10.1111/ppa.12618 (2017).
Google Scholar
Roth, V. Doubling time computing, application available from: http://www.doubling-time.com/compute.php, (2006).
Krzyzanowska, D. M. et al. Compatible mixture of bacterial antagonists developed to protect ootato tubers from soft rot caused by Pectobacterium spp. and Dickeya spp. Plant. Dis. 103, 1374–1382, doi:https://doi.org/10.1094/PDIS-10-18-1866-RE (2019).
Czajkowski, R., de Boer, W. J., van Veen, J. A. & van der Wolf, J. M. Characterization of bacterial isolates from rotting potato tuber tissue showing antagonism to Dickeya sp. biovar 3 in vitro and in planta. Plant Pathology 61, 169–182, https://doi.org/10.1111/j.1365-3059.2011.02486.x (2012).
Shao, X., Xie, Y., Zhang, Y. & Deng, X. Biofilm formation assay in Pseudomonas syringae. Biol. Protoc. 9, e3237. https://doi.org/10.21769/BioProtoc.3237 (2019).
Google Scholar
Dickey, R. S. Erwinia chrysanthemi: a comparative study of phenotypic properties of strains from several hosts and other Erwinia species. Phytopathol. 69, 324–329 (1979).
Google Scholar
Perombelon, M. C. M. & van Der Wolf, J. M. Methods for the detection and quantification of Erwinia carotovora subsp. atroseptica (Pectobacterium carotovorum subsp. atrosepticum) on potatoes: a laboratory manual. Scottish Crop Research Institute Annual Report 10 (2002).
Py, B., Bortoli-German, I., Haiech, J., Chippaux, M. & Barras, F. Cellulase EGZ of Erwinia chrysanthemi: structural organization and importance of His98 and Glu133 residues for catalysis. Prot. Eng. 4, 325–333. https://doi.org/10.1093/protein/4.3.325 (1991).
Google Scholar
Ji, J. W., Hugouvieux Cotte Pattat, N. & Robert Baudouy, J. Use of Mu-Lac insertions to study the secretion of pectate lyases by Erwinia chrysanthemi. J. Gen. Microbiol. 133, 793–802 (1987).
Schwyn, B. & Neilands, J. B. Universal chemical assay for the detection and determination of siderophores. Anal Biochem. 160, 47–56. https://doi.org/10.1016/0003-2697(87)90612-9 (1987).
Google Scholar
Fiolka, M. J. et al. Antimycobacterial action of a new glycolipid-peptide complex obtained from extracellular metabolites of Raoultella ornithinolytica. APMIS 123, 1069–1080. https://doi.org/10.1111/apm.12466 (2015).
Google Scholar
Sorroche, F. G., Rinaudi, L. V., Zorreguieta, A. & Giordano, W. EPS II-dependent autoaggregation of Sinorhizobium meliloti planktonic cells. Curr. Microbiol. 61, 465–470. https://doi.org/10.1007/s00284-010-9639-9 (2010).
Google Scholar
Dorken, G., Ferguson, G. P., French, C. E. & Poon, W. C. Aggregation by depletion attraction in cultures of bacteria producing exopolysaccharide. J. R. Soc. Interface 9, 3490–3502. https://doi.org/10.1098/rsif.2012.0498 (2012).
Google Scholar
Trunk, T., Khalil, H. S. & Leo, J. C. Bacterial autoaggregation. AIMS Microbiol. 4, 140–164. https://doi.org/10.3934/microbiol.2018.1.140 (2018).
Google Scholar
Przepiora, T. et al. The periplasmic oxidoreductase DsbA is required for virulence of the phytopathogen Dickeya solani. Int. J. Mol. Sci. 23, 697 (2022).
Google Scholar
Bauer, A. W., Kirby, W. M. M., Sherris, J. C. & Turck, M. Antibiotic susceptibility testing by a standardized single disk method. Am. J. Clin. Pathol. 45, 493–500 (1966).
Google Scholar
Sambrook, J., Fritsch, E. F. & Maniatis, T. Molecular cloning: a laboratory manual. (1989).
Tsai, C. M. & Frasch, C. E. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal. Biochem. 119, 115–119. https://doi.org/10.1016/0003-2697(82)90673-x (1982).
Google Scholar
Fikowicz-Krosko, J. & Czajkowski, R. Systemic colonization and expression of disease symptoms on bittersweet nightshade (Solanum dulcamara) infected with a GFP-tagged Dickeya solani IPO2222 (IPO2254). Plant. Dis. 102, 619–627. https://doi.org/10.1094/PDIS-08-17-1147-RE (2018).
Google Scholar
Miller, W. G., Leveau, J. H. & Lindow, S. E. Improved gfp and inaZ broad-host-range promoter-probe vectors. Mol. Plant. Microbe Interact 13, 1243–1250. https://doi.org/10.1094/MPMI.2000.13.11.1243 (2000).
Google Scholar
Bloemberg, G. V., Wijfjes, A. H., Lamers, G. E., Stuurman, N. & Lugtenberg, B. J. Simultaneous imaging of Pseudomonas fluorescens WCS365 populations expressing three different autofluorescent proteins in the rhizosphere: new perspectives for studying microbial communities. Mol. Plant. Microbe Interact 13, 1170–1176. https://doi.org/10.1094/MPMI.2000.13.11.1170 (2000).
Google Scholar
Czajkowski, R. et al. Virulence of ‘Dickeya solani’ and Dickeya dianthicola biovar-1 and -7 strains on potato (Solanum tuberosum). Plant. Pathol. 62, 597–610. https://doi.org/10.1111/j.1365-3059.2012.02664.x (2013).
Google Scholar
Czajkowski, R., de Boer, W. J., Velvis, H. & van der Wolf, J. M. Systemic colonization of potato plants by a soilborne, green fluorescent protein-tagged strain of Dickeya sp. biovar 3. Phytopathology 100, 134–142, doi:https://doi.org/10.1094/PHYTO-100-2-0134 (2010).
Czajkowski, R., Grabe, G. J. & van der Wolf, J. M. Distribution of Dickeya spp. and Pectobacterium carotovorum subsp. carotovorum in naturally infected seed potatoes. Eur. J. Plant Pathol. 125, 263–275, doi:https://doi.org/10.1007/s10658-009-9480-9 (2009).
Czajkowski, R., de Boer, W. J., van Veen, J. A. & van der Wolf, J. M. Studies on the interaction between the biocontrol agent, Serratia plymuthica A30, with blackleg causing Dickeya sp. (biovar 3) in potato (Solanum tuberosum). Plant Pathol. 61, 677–688 (2012).
Shapiro, S. S. & Wilk, M. B. An analysis of variance test for normality (complete samples). Biometrika 52, 591–600. https://doi.org/10.2307/2333709 (1965).
Google Scholar
Welch, B. L. The generalisation of student’s problems when several different population variances are involved. Biometrika 34, 28–35. https://doi.org/10.1093/biomet/34.1-2.28 (1947).
Google Scholar
Box, G. E. P. Non-normality and tests on variances. Biometrika 40, 318–335. https://doi.org/10.2307/2333350 (1953).
Google Scholar
Student. The probable error of a mean. Biometrika 6, 1–25, doi:https://doi.org/10.2307/2331554 (1908).
Shieh, G. & Jan, S. L. The effectiveness of randomized complete block design. Stat. Neerl. 58, 111–124 (2004).
Google Scholar
Comments are closed.