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Genomic overview of the phytopathogen Pectobacterium wasabiae strain RNS 08.42.1A suggests horizontal acquisition of quorum-sensing genes

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Abstract

The blackleg and soft-rot diseases caused by pectinolytic enterobacteria such as Pectobacterium and Dickeya are major causes of losses affecting potato crop in the field and upon storage. In this work, we report the isolation, characterization and genome analysis of the Pectobacterium wasabiae (formely identified as Pectobacterium carotovorum subsp. carotovorum) strain RNS 08.42.1A, that has been isolated from a Solanum tuberosum host plant in France. Comparative genomics with 3 other P. wasabiae strains isolated from potato plants in different areas in North America and Europe, highlighted both a strong similarity at the whole genome level (ANI > 99 %) and a conserved synteny of the virulence genes. In addition, our analyses evidenced a robust separation between these four P. wasabiae strains and the type strain P. wasabiae CFBP 3304T, isolated from horseradish in Japan. In P. wasabiae RNS 08.42.1A, the expI and expR nucleotidic sequences are more related to those of some Pectobacterium atrosepticum and P. carotovorum strains (90 % of identity) than to those of the other potato P. wasabiae strains (70 to 74 % of identity). This could suggest a recruitment of these genes in the P. wasabiae strain RNS 08.42.1A by an horizontal transfer between pathogens infecting the same potato host plant.

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References

  • Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M et al (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75. doi:10.1186/1471-2164-9-75

    Article  PubMed Central  PubMed  Google Scholar 

  • Baghaee-Ravari S, Rahimian H, Shams-Bakhsh M, Lopez-Solanilla E, Antúnez-Lamas M, Rodríguez-Palenzuela P (2011) Characterization of Pectobacterium species from Iran using biochemical and molecular methods. Eur J Plant Pathol 129:413–425. doi:10.1007/s10658-010-9704-z

    Article  Google Scholar 

  • Barras F, van Gijsegem F, Chatterjee AK (1994) Extracellular enzymes and pathogenesis of soft-rot Erwinia. Annu Rev Phytopathol 32:201–234. doi:10.1146/annurev.py.32.090194.001221

    Article  CAS  Google Scholar 

  • Bell KS, Sebaihia M, Pritchard L, Holden MTG, Hyman LJ, Holeva MC, Thomson NR, Bentley SD, Churcher LJC, Mungall K et al (2004) Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc Natl Acad Sci 101:11105–11110. doi:10.1073/pnas.0402424101

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Boughammoura A, Franza T, Dellagi A, Roux C, Matzanke-Markstein B, Expert D (2007) Ferritins, bacterial virulence and plant defence. Biometals 20:347–353. doi:10.1007/s10534-006-9069-0

    Article  CAS  PubMed  Google Scholar 

  • Budde PP, Davis BM, Yuan J, Waldor MK (2007) Characterization of a higBA toxin–antitoxin locus in Vibrio cholerae. J Bacteriol 189:491–500. doi:10.1128/JB.00909-06

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bukowski M, Rojowska A, Wladyka B (2011) Prokaryotic toxin–antitoxin systems—the role in bacterial physiology and application in molecular biology. Acta Biochim Pol 58:1–9

    CAS  PubMed  Google Scholar 

  • Charkowski AO (2006) The soft rot Erwinia. In: Gnanamanickam S (ed) Plant-associated bacteria. Springer, Netherlands, pp 423–505

  • Corbett M, Virtue S, Bell K, Birch P, Burr T, Hyman L, Lilley K, Poock S, Toth I, Salmond G (2005) Identification of a new quorum-sensing-controlled virulence factor in Erwinia carotovora subsp. atroseptica secreted via the type II targeting pathway. Mol Plant Microbe Interact 18:334–342

    Article  CAS  PubMed  Google Scholar 

  • Crépin A, Barbey C, Beury-Cirou A, Hélias V, Taupin L, Reverchon S, Nasser W, Faure D, Dufour A, Orange N et al (2012a) Quorum sensing signaling molecules produced by reference and emerging soft-rot bacteria (Dickeya and Pectobacterium spp.). PLoS ONE 7:e35176. doi:10.1371/journal.pone.0035176

    Article  PubMed Central  PubMed  Google Scholar 

  • Crépin A, Barbey C, Cirou A, Tannières M, Orange N, Feuilloley M, Dessaux Y, Burini J-F, Faure D, Latour X (2012b) Biological control of pathogen communication in the rhizosphere: a novel approach applied to potato soft rot due to Pectobacterium atrosepticum. Plant Soil 358:27–37. doi:10.1007/s11104-011-1030-5

    Article  Google Scholar 

  • Crépin A, Beury-Cirou A, Barbey C, Farmer C, Hélias V, Burini J-F, Faure D, Latour X (2012c) N-Acyl homoserine lactones in diverse Pectobacterium and Dickeya plant pathogens: diversity, abundance, and involvement in virulence. Sensors 12:3484–3497. doi:10.3390/s120303484

    Article  PubMed Central  PubMed  Google Scholar 

  • Czajkowski R, Pérombelon MCM, van Veen JA, van der Wolf JM (2011) Control of blackleg and tuber soft rot of potato caused by Pectobacterium and Dickeya species: a review: control of Dickeya and Pectobacterium species in potato. Plant Pathol 60:999–1013. doi:10.1111/j.1365-3059.2011.02470.x

    Article  Google Scholar 

  • Darling ACE (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403. doi:10.1101/gr.2289704

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Darrasse A, Priou S, Kotoujansky A, Bertheau Y (1994) PCR and restriction fragment length polymorphism of a pel gene as a tool to identify Erwinia carotovora in relation to potato diseases. Appl Environ Microbiol 60:1437–1443

    PubMed Central  CAS  PubMed  Google Scholar 

  • De Boer SH, Li X, Ward LJ (2012) Pectobacterium spp. associated with bacterial stem rot syndrome of potato in Canada. Phytopathology 102:937–947

    Article  PubMed  Google Scholar 

  • De la Cruz MA, Zhao W, Farenc C, Gimenez G, Raoult D, Cambillau C, Gorvel J-P, Méresse S (2013) A toxin–antitoxin module of Salmonella promotes virulence in mice. PLoS Pathog 9:e1003827. doi:10.1371/journal.ppat.1003827

    Article  PubMed Central  PubMed  Google Scholar 

  • Frechon D, Exbrayat P, Helias V, Hyman LJ, Jouan B, Llop P, Lopez MM, Payet N, Perombelon MCM, Toth IK (1998) Evaluation of a PCR kit for the detection of Erwinia carotovora subsp. atroseptica on potato tubers. Potato Res 41:163–173

    Article  Google Scholar 

  • Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR–LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gardan L, Gouy C, Richard C, Samson R (2003) Elevation of three subspecies of Pectobacterium carotovorum to species level: Pectobacterium atrosepticum sp. nov., Pectobacterium betavasculorum sp. nov. and Pectobacterium wasabiae sp. nov. Int J Syst Evol Microbiol 53:381–391. doi:10.1099/ijs.0.02423-0

    Article  CAS  PubMed  Google Scholar 

  • Gerdes K, Christensen SK, Løbner-Olesen A (2005) Prokaryotic toxin–antitoxin stress response loci. Nat Rev Microbiol 3:371–382. doi:10.1038/nrmicro1147

    Article  CAS  PubMed  Google Scholar 

  • Gogarten JP, Doolittle WF, Lawrence JG (2002) Prokaryotic evolution in light of gene transfer. Mol Biol Evol 19:2226–2238

    Article  CAS  PubMed  Google Scholar 

  • Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91. doi:10.1099/ijs.0.64483-0

    Article  CAS  PubMed  Google Scholar 

  • Goto M, Matsumoto K (1987) Erwinia carotovora subsp. wasabiae subsp. nov. Isolated from Diseased Rhizomes and Fibrous Roots of Japanese Horseradish (Eutrema wasabi Maxim.). Int J Syst Evol Microbiol 37(2):130–135. doi:10.1099/00207713-37-2-130

  • Gray KM, Garey JR (2001) The evolution of bacterial LuxI and LuxR quorum sensing regulators. Microbiology 147:2379–2387

    CAS  PubMed  Google Scholar 

  • Hélias V, Hamon P, Huchet E, Wolf JVD, Andrivon D (2012) Two new effective semiselective crystal violet pectate media for isolation of Pectobacterium and Dickeya: isolating pectolytic bacteria on CVP. Plant Pathol 61:339–345. doi:10.1111/j.1365-3059.2011.02508.x

    Article  Google Scholar 

  • Hugouvieux-Cotte-Pattat N, Condemine G, Nasser W, Reverchon S (1996) Regulation of pectinolysis in Erwinia chrysanthemi. Annu Rev Microbiol 50:213–257

    Article  CAS  PubMed  Google Scholar 

  • Hurley JM, Woychik NA (2009) Bacterial toxin HigB associates with ribosomes and mediates translation-dependent mRNA cleavage at A-rich sites. J Biol Chem 284:18605–18613. doi:10.1074/jbc.M109.008763

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jones S, Yu B, Bainton NA, Birdsall M, Bycroft BW, Chhabra SR, Cox AJ, Golby P, Reeves PJ, Stephens S et al (1993) The Lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO J 12:2477

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kim H-S, Ma B, Perna NT, Charkowski AO (2009) Phylogeny and virulence of naturally occurring type III secretion system-deficient Pectobacterium strains. Appl Environ Microbiol 75:4539–4549. doi:10.1128/AEM.01336-08

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kim MH, Cho MS, Kim BK, Choi HJ, Hahn JH, Kim C, Kang MJ, Kim SH, Park DS (2012) Quantitative real-time polymerase chain reaction assay for detection of Pectobacterium wasabiae using YD repeat protein gene-based primers. Plant Dis 96:253–257

    Article  Google Scholar 

  • Koskinen JP, Laine P, Niemi O, Nykyri J, Harjunpaa H, Auvinen P, Paulin L, Pirhonen M, Palva T, Holm L (2012) Genome sequence of Pectobacterium sp. strain SCC3193. J Bacteriol 194:6004. doi:10.1128/JB.00681-12

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lang AS, Zhaxybayeva O, Beatty JT (2012) Gene transfer agents: phage-like elements of genetic exchange. Nat Rev Microbiol. doi:10.1038/nrmicro2802

    PubMed Central  PubMed  Google Scholar 

  • Lerat E, Moran NA (2004) The evolutionary history of quorum-sensing systems in bacteria. Mol Biol Evol 21:903–913. doi:10.1093/molbev/msh097

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Coulthurst SJ, Pritchard L, Hedley PE, Ravensdale M, Humphris S, Burr T, Takle G, Brurberg M-B, Birch PRJ et al (2008) Quorum sensing coordinates rrute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. PLoS Pathog 4:e1000093. doi:10.1371/journal.ppat.1000093

    Article  PubMed Central  PubMed  Google Scholar 

  • Ma B, Hibbing ME, Kim H-S, Reedy RM, Yedidia I, Breuer J, Breuer J, Glasner JD, Perna NT, Kelman A et al (2007) Host range and molecular phylogenies of the soft rot enterobacterial genera Pectobacterium and Dickeya. Phytopathology 97:1150–1163. doi:10.1094/PHYTO-97-9-1150

    Article  PubMed  Google Scholar 

  • Magnuson RD (2007) Hypothetical functions of toxin-antitoxin systems. J Bacteriol 189:6089–6092. doi:10.1128/JB.00958-07

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Moleleki LN, Onkendi EM, Mongae A, Kubheka GC (2013) Characterisation of pectobacterium wasabiae causing blackleg and soft rot diseases in South Africa. Eur J Plant Pathol 135:279–288. doi:10.1007/s10658-012-0084-4

    Article  Google Scholar 

  • Nabhan S, Wydra K, Linde M, Debener T (2012) The use of two complementary DNA assays, AFLP and MLSA, for epidemic and phylogenetic studies of pectolytic enterobacterial strains with focus on the heterogeneous species Pectobacterium carotovorum: phylogenetic focus on soft-rot plant pathogens. Plant Pathol 61:498–508. doi:10.1111/j.1365-3059.2011.02546.x

    Article  Google Scholar 

  • Nassar A, Darrasse A, Lemattre M, Kotoujansky A, Dervin C, Vedel R, Bertheau Y (1996) Characterization of Erwinia chrysanthemi by pectinolytic isozyme polymorphism and restriction fragment length polymorphism analysis of PCR-amplified fragments of pel genes. Appl Environ Microbiol 62:2228–2235

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nasser W, Bouillant ML, Salmond G, Reverchon S (1998) Characterization of the Erwinia chrysanthemi expI–expR locus directing the synthesis of two N-acyl-homoserine lactone signal molecules. Mol Microbiol 29:1391–1405. doi:10.1046/j.1365-2958.1998.01022.x

    Article  CAS  PubMed  Google Scholar 

  • Nasser W, Dorel C, Wawrzyniak J, Van Gijsegem F, Groleau M-C, Déziel E, Reverchon S (2013) Vfm a new quorum sensing system controls the virulence of Dickeya dadantii: new quorum sensing signal in Dickeya. Environ Microbiol 15:865–880. doi:10.1111/1462-2920.12049

    Article  CAS  PubMed  Google Scholar 

  • Ngadze E, Brady CL, Coutinho TA, van der Waals JE (2012) Pectinolytic bacteria associated with potato soft rot and blackleg in South Africa and Zimbabwe. Eur J Plant Pathol 134:533–549. doi:10.1007/s10658-012-0036-z

    Article  CAS  Google Scholar 

  • Nykyri J, Niemi O, Koskinen P, Nokso-Koivisto J, Pasanen M, Broberg M, Plyusnin I, Törönen P, Holm L, Pirhonen M et al (2012) Revised phylogeny and novel horizontally acquired virulence determinants of the model soft rot phytopathogen Pectobacterium wasabiae SCC3193. PLoS Pathog 8:e1003013. doi:10.1371/journal.ppat.1003013

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pérombelon MCM (2002) Potato diseases caused by soft rot erwinias: an overview of pathogenesis. Plant Pathol 51:1–12

    Article  Google Scholar 

  • Pitman AR, Harrow SA, Visnovsky SB (2010) Genetic characterisation of Pectobacterium wasabiae causing soft rot disease of potato in New Zealand. Eur J Plant Pathol 126:423–435. doi:10.1007/s10658-009-9551-y

    Article  Google Scholar 

  • Reeves PP, Wang L (2002) Genomic organization of LPS-specific loci. In: Hacker J, Kaper JB (eds) Pathogenicity islands and the evolution of pathogenic microbes. Springer, Berlin, Heidelberg, pp 109–135

  • Samson R, Legendre JB, Richard C, Fischer-Le Saux M, Achouak W, Gardan L et al (2005) Transfer of Pectobacterium chrysanthemi (Burkholder, 1953) Brenner et al. 1973 and Brenneria paradisiaca to the genus Dickeya gen. nov. as Dickeya chrysanthemi comb. nov. and Dickeya paradisiaca comb. nov. and delineation of four novel species, Dickeya dadantii sp. nov., Dickeya dianthicola sp. nov., Dickeya dieffenbachiae sp. nov. and Dickeya zeae sp. nov. Int J Syst Evol Microbiol 55:1415–1427. doi:10.1099/ijs.0.02791-0

    Article  CAS  PubMed  Google Scholar 

  • Schureck MA, Maehigashi T, Miles SJ, Marquez J, Cho SE, Erdman R, Dunham CM (2014) Structure of the Proteus vulgaris HigB-(HigA)2-HigB toxin-antitoxin complex. J Biol Chem 289:1060–1070. doi:10.1074/jbc.M113.512095

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Smadja B, Latour X, Trigui S, Burini JF, Chevalier S, Orange N (2004) Thermodependence of growth and enzymatic activities implicated in pathogenicity of two Erwinia carotovora subspecies (Pectobacterium spp.). Can J Microbiol 50:19–27. doi:10.1139/w03-099

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Toth IK, Bell KS, Holeva MC, Birch PR (2003) Soft rot erwiniae: from genes to genomes. Mol Plant Pathol 4:17–30

    Article  CAS  PubMed  Google Scholar 

  • Toth IK, Pritchard L, Birch PR (2006) Comparative genomics reveals what makes an enterobacterial plant pathogen. Annu Rev Phytopathol 44:305–336

    Article  CAS  PubMed  Google Scholar 

  • Waleron M, Waleron K, Podhajska AJ, Lojkowska E (2002) Genotyping of bacteria belonging to the former Erwinia genus by PCR-RFLP analysis of a recA gene fragment. Microbiology 148:583–595

    CAS  PubMed  Google Scholar 

  • Waleron M, Waleron K, Lojkowska E (2013) Occurrence of Pectobacterium wasabiae in potato field samples. Eur J Plant Pathol 137:149–158. doi:10.1007/s10658-013-0227-2

    Article  Google Scholar 

  • Wen Y, Behiels E, Devreese B (2014) Toxin-Antitoxin systems: their role in persistence, biofilm formation, and pathogenicity. Pathog Dis 70:240–249. doi:10.1111/2049-632X.12145

    Article  CAS  PubMed  Google Scholar 

  • Whitehead NA, Byers JT, Commander P, Corbett MJ, Coulthurst SJ, Everson L, Harris AKP, Pemberton CL, Simpson NJL, Slater H et al (2002) The regulation of virulence in phytopathogenic Erwinia species: quorum sensing, antibiotics and ecological considerations. Antonie Van Leeuwenhoek 81:223–231

    Article  CAS  PubMed  Google Scholar 

  • Wilson K (1987) Preparation of genomic DNA from bacteria. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (eds) Protocols in molecular biology. Greene Publishing and Wiley- Interscience, New York, pp 2.4.1–2.4.5

  • Yamaguchi Y, Park J-H, Inouye M (2011) Toxin–antitoxin systems in bacteria and archaea. Annu Rev Genet 45:61–79. doi:10.1146/annurev-genet-110410-132412

    Article  CAS  PubMed  Google Scholar 

  • Yuan K, Adam Z, Tambong J, Levesque CA, Chen W, Lewis CT, De Boer SH, Li X (2014) Draft Genome sequence of Pectobacterium wasabiae strain CFIA1002. Genome Announc 2:e00214–14. doi:10.1128/genomeA.00214-14

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by a cooperative project between France and Morocco (PRAD 14-02, Campus France No. 30229 ZK), the excellence Grant (No. H011/007) awarded by the Ministry of Higher education of Morocco, and a collaborative project between Centre National de la Recherche Scientifique (CNRS, Gif sur Yvette) and Fédération Nationale des Producteurs de Plants de Pomme de Terre-Recherche Développement Promotion du Plants de Pomme de Terre (FN3PT-RD3PT, Paris).

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Authors and Affiliations

  1. Institut des Sciences du Végétal, UPR2355, Saclay Plant Sciences, Centre National de la Recherche Scientifique, 1, Avenue de la Terrasse, 91 198, Gif-sur-Yvette, France

    Slimane Khayi, Yannick Raoul des Essarts & Denis Faure

  2. Département de Biologie, Faculté des Sciences, Université Moulay Ismaïl, Meknes, Morocco

    Slimane Khayi & Mohieddine Moumni

  3. Fédération Nationale des Producteurs de Plants de Pomme de Terre-Recherche Développement Promotion du Plant de Pomme de Terre (FN3PT-RD3PT), 75008, Paris, France

    Yannick Raoul des Essarts, Angélique Quêtu-Laurent & Valérie Hélias

  4. UMR 1349 IGEPP INRA - Agrocampus Ouest Rennes, 35653, LeRheu, France

    Angélique Quêtu-Laurent & Valérie Hélias

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  1. Slimane Khayi
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  2. Yannick Raoul des Essarts
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  3. Angélique Quêtu-Laurent
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  4. Mohieddine Moumni
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  5. Valérie Hélias
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Correspondence to Valérie Hélias or Denis Faure.

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Khayi, S., Raoul des Essarts, Y., Quêtu-Laurent, A. et al. Genomic overview of the phytopathogen Pectobacterium wasabiae strain RNS 08.42.1A suggests horizontal acquisition of quorum-sensing genes. Genetica 143, 241–252 (2015). https://doi.org/10.1007/s10709-014-9793-2

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