Pseudomonas prosekii isolated in Antarctica inhibits plantpathogenic strains of Pseudomonas viridiflava and Pseudomonas fluorescens

Vol.11,No.2(2021)

Abstract

Pseudomonas-caused plant diseases are present worldwide and affect most of the major lineages of higher plants which, as a consequence, may result in significant economic losses. Despite the use of bacteriocins produced by rhizosphere and soil bacteria has been nowadays considered as novel crop protection approach, antagonistic interactions of cold-adapted isolates toward agriculturally important phytopathogenic bacteria have not been studied yet. In this study, we tested inhibition activity of Antarctic Pseudomonas spp. against phytopathogenic pseudomonads. Four Antarctic stains (P. prosekii CCM 8878, CCM 8879, and CCM 8881 and Pseudomonas sp. CCM 8880) inhibited several phytopathogenic strains of P. viridiflava and P. fluorescens. Based on inhibition zone character and previous genome research we suggest that L-pyocin activity was responsible for this effect against P. viridiflava strains and that tailocin inhibited P. fluorescens isolate.


Keywords:
pyocin; Pseudomonas; phytopathogen; tailocin; antimicrobial agents; James Ross Island
References

Barreteau, H., Tiouajni, M., Graille, M., Josseaume, N., Bouhss, A., Patin, D., Blanot, D., Fourgeaud, M., Mainardi, J.-L., Arthur, M., van Tilbeurgh, H., Mengin-Lecreulx, D. and Touzé, T. (2012): Functional and structural characterization of PaeM, a colicin M-like bacteriocin produced by Pseudomonas aeruginosa. The Journal of Biological Chemistry, 287(44): 37395-37405. https://doi.org/10.1074/jbc.M112.406439

Dorosky, R. J., Yu, J. M., Pierson, L. S. and Pierson, E. A. (2017): Pseudomonas chlororaphis produces two distinct R-tailocins that contribute to bacterial competition in biofilms and on roots. Applied and Environmental Microbiology, 83(15). https://doi.org/10.1128/AEM.00706-17

Fernandez, M., Godino, A., Príncipe, A., Morales, G. M. and Fischer, S. (2017): Effect of a Pseudomonas fluorescens tailocin against phytopathogenic Xanthomonas observed by atomic force microscopy. Journal of Biotechnology, 256: 13-20. https://doi.org/10.1016/j.jbiotec.2017.07.002

Flury, P., Aellen, N., Ruffner, B., Péchy-Tarr, M., Fataar, S., Metla, Z., Dominguez-Ferreras, A., Bloemberg, G., Frey, J., Goesmann, A., Raaijmakers, J. M., Duffy, B., Höfte, M., Blom, J., Smits, T. H. M., Keel, C. and Maurhofer, M. (2016): Insect pathogenicity in plant-beneficial pseudomonads: Phylogenetic distribution and comparative genomics. The ISME Journal, 10(10): 2527-2542. https://doi.org/10.1038/ismej.2016.5

Fyfe, J. A., Harris, G. and Govan, J. R. (1984): Revised pyocin typing method for Pseudomonas aeruginosa. Journal of Clinical Microbiology, 20(1): 47-50. https://doi.org/10.1128/jcm.20.1.47-50.1984

Ganeshan, G., Manoj Kumar, A. (2005): Pseudomonas fluorescens, a potential bacterial antagonist to control plant diseases. Journal of Plant Interactions, 1(3): 123-134. https://doi.org/10.1080/17429140600907043

Ghequire, M. G. K., De Mot, R. (2014): Ribosomally encoded antibacterial proteins and peptides from Pseudomonas. FEMS Microbiology Reviews, 38(4): 523-568. https://doi.org/10.1111/1574-6976.12079

Ghequire, M. G. K., Dillen, Y., Lambrichts, I., Proost, P., Wattiez, R. and De Mot, R. (2015): Different ancestries of R tailocins in rhizospheric Pseudomonas isolates. Genome Biology and Evolution, 7(10): 2810-2828. https://doi.org/10.1093/gbe/evv184

Ghequire, M. G. K., Öztürk, B. and De Mot, R. (2018): Lectin-like bacteriocins. Frontiers in Microbiology, 9: 2706. https://doi.org/10.3389/fmicb.2018.02706

Goumans, D. E., Chatzaki, A. K. (1998): Characterization and host range evaluation of Pseudomonas viridiflava from melon, blite, tomato, chrysanthemum and eggplant. European Journal of Plant Pathology, 104(2): 181-188. https://doi.org/10.1023/A:1008675704834

Grinter, R., Milner, J. and Walker, D. (2012): Bacteriocins active against plant pathogenic bacteria. Biochemical Society Transactions, 40(6): 1498-1502. https://doi.org/10.1042/BST20120206

Hockett, K. L., Renner, T. and Baltrus, D. A. (2015): Independent co-option of a tailed bacteriophage into a killing complex in Pseudomonas. mBio, 6(4): e00452. https://doi.org/10.1128/mBio.00452-15

Hu, J., Yang, T., Friman, V. P., Kowalchuk, G. A., Hautier, Y., Li, M., Wei, Z., Xu, Y., Shen, Q. and Jousset, A. (2021): Introduction of probiotic bacterial consortia promotes plant growth via impacts on the resident rhizosphere microbiome. Proceedings. Biological sciences, 288 (1960): 20211396. https://doi.org/10.1098/rspb.2021.1396

Lavermicocca, P., Lonigro, S. L., Valerio, F., Evidente, A. and Visconti, A. (2002): Reduction of olive knot disease by a bacteriocin from Pseudomonas syringae pv. Ciccaronei. Applied and Environmental Microbiology, 68(3): 1403-1407. https://doi.org/10.1128/AEM.68.3.1403-1407.2002

Loper, J. E., Hassan, K. A., Mavrodi, D. V., Davis, E. W., Lim, C. K., Shaffer, B. T., Elbourne, L. D. H., Stockwell, V. O., Hartney, S. L., Breakwell, K., Henkels, M. D., Tetu, S. G., Rangel, L. I., Kidarsa, T. A., Wilson, N. L., van de Mortel, J. E., Song, C., Blumhagen, R., Radune, D. and Paulsen, I. T. (2012): Comparative genomics of plant-associated Pseudomonas spp.: Insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genetics, 8(7): e1002784. https://doi.org/10.1371/journal.pgen.1002784

Majeed, H., Gillor, O., Kerr, B. and Riley, M. A. (2011): Competitive interactions in Escherichia coli populations: The role of bacteriocins. The ISME Journal, 5(1): 71-81. https://doi.org/10.1038/ismej.2010.90

McCaughey, L. C., Grinter, R., Josts, I., Roszak, A. W., Waløen, K. I., Cogdell, R. J., Milner, J., Evans, T., Kelly, S., Tucker, N. P., Byron, O., Smith, B. and Walker, D. (2014): Lectin-like bacteriocins from Pseudomonas spp. Utilise D-rhamnose containing lipopolysaccharide as a cellular receptor. PLoS Pathogens, 10(2): e1003898. https://doi.org/10.1371/journal.ppat.1003898

Metelev, M., Serebryakova, M., Ghilarov, D., Zhao, Y. and Severinov, K. (2013): Structure of microcin B-like compounds produced by Pseudomonas syringae and species specificity of their antibacterial action. Journal of Bacteriology, 195(18): 4129-4137. https://doi.org/10.1128/JB.00665-13

Micenková, L., Štaudová, B., Bosák, J., Mikalová, L., Littnerová, S., Vrba, M., Ševčíková, A., Woznicová, V. and Šmajs, D. (2014): Bacteriocin-encoding genes and ExPEC virulence determinants are associated in human fecal Escherichia coli strains. BMC Microbiology, 14: 109. https://doi.org/10.1186/1471-2180-14-109

Michel-Briand, Y., Baysse, C. (2002): The pyocins of Pseudomonas aeruginosa. Biochimie, 84(5–6): 499-510. https://doi.org/10.1016/S0300-9084(02)01422-0

Nakayama, K., Takashima, K., Ishihara, H., Shinomiya, T., Kageyama, M., Kanaya, S., Ohnishi, M., Murata, T., Mori, H. and Hayashi, T. (2000): The R-type pyocin of Pseudomonas aeruginosa is related to P2 phage, and the F-type is related to lambda phage. Molecular Microbiology, 38(2): 213-231. https://doi.org/10.1046/j.1365-2958.2000.02135.x

Oluyombo, O., Penfold, C. and Diggle, S. (2019): Competition in biofilms between cystic fibrosis isolates of Pseudomonas aeruginosa is shaped by R-Pyocins. mBio, 10: e01828-18. https://doi.org/10.1128/mBio.01828-18

Palleroni, N. J. (2015): Genus I. Pseudomonas. In Garrity, G. M., Brenner, D. J., Krieg, N. R., Staley, J. T. (eds.): Bergey’s manual of systematics of archaea and bacteria. Volume 2. Springer Verlag. New York. pp. 323–379.

Parret, A. H. A., Schoofs, G., Proost, P. and De Mot, R. (2003): Plant lectin-like bacteriocin from a rhizosphere-colonizing Pseudomonas isolate. Journal of Bacteriology, 185(3): 897-908. https://doi.org/10.1128/JB.185.3.897-908.2003

Parret, A. H. A., Temmerman, K. and De Mot, R. (2005): Novel lectin-like bacteriocins of biocontrol strain Pseudomonas fluorescens Pf-5. Applied and Environmental Microbiology, 71(9): 5197-5207. https://doi.org/10.1128/AEM.71.9.5197-5207.2005

Passera, A., Compant, S., Casati, P., Maturo, M. G., Battelli, G., Quaglino, F., Antonielli, L., Salerno, D., Brasca, M., Toffolatti, S. L., Mantegazza, F., Delledonne, M. and Mitter, B. (2019): Not Just a Pathogen? Description of a plant-beneficial Pseudomonas syringae Strain. Frontiers in Microbiology, 10: 1409. https://doi.org/10.3389/fmicb.2019.01409

Príncipe, A., Fernandez, M., Torasso, M., Godino, A. and Fischer, S. (2018): Effectiveness of tailocins produced by Pseudomonas fluorescens SF4c in controlling the bacterial-spot disease in tomatoes caused by Xanthomonas vesicatoria. Microbiological Research, 212–213: 94-102. https://doi.org/10.1016/j.micres.2018.05.010

Sarris, P. F., Trantas, E. A., Mpalantinaki, E., Ververidis, F. and Goumas, D. E. (2012): Pseudomonas viridiflava, a Multi Host Plant Pathogen with Significant Genetic Variation at the Molecular Level. PLoS ONE, 7(4): e36090. https://doi.org/10.1371/journal.pone.0036090

Sharp, C., Bray, J., Housden, N. G., Maiden, M. C. J., Kleanthous, C. (2017): Diversity and distribution of nuclease bacteriocins in bacterial genomes revealed using Hidden Markov Models. PLOS Computational Biology, 13(7): e1005652. https://doi.org/10.1371/journal.pcbi.1005652

Schroth, M., Hildebrand, D. and Panopoulos, N. (2006): Phytopathogenic Pseudomonads and Related Plant-Associated Pseudomonads. In: M. Dworkin, S. Falkow, E. Rosenberg, K. H. Schleifer, E. Stackebrandt (eds.): The Prokaryotes, Volume 6, 3rd ed., Springer Verlag. New York. pp. 714–740. https://doi.org/10.1007/0-387-30746-X_23

Smith, I. M., Dunez, J., Phillips, D. H., Lelliott, R. A. and Archer, S. A. (eds.) (2009): European handbook of plant diseases. John Wiley & Sons. pp. 136–175.

Snopková, K., Dufková, K., Chamrád, I., Lenobel, R., Čejková, D., Kosina M., Hrala, M., Holá, V., Sedláček, I. and Šmajs, D. (2021, Online ahead of print.): Pyocin-mediated antagonistic interactions in Pseudomonas spp. Isolated in James Ross Island, Antarctica. Environmental Microbiology. https://doi.org/10.1111/1462-2920.15809

Snopková, K., Sedláček, I. and Šmajs, D. (2018): First evidence of high-molecular-weight bacteriocin (tailocin) produced by Antarctic Pseudomonas spp. Czech Polar Reports, 8(2): 178-185. https://doi.org/10.5817/CPR2018-2-14

Strange, R. N., Scott, P. R. (2005): Plant disease: A threat to global food security. Annual Review of Phytopathology, 43: 83-116. https://doi.org/10.1146/annurev.phyto.43.113004.133839

Terauds, A., Lee, J. R. (2016): Antarctic biogeography revisited: Updating the Antarctic Conservation Biogeographic Regions. Diversity and Distributions, 22(8): 836-840. https://doi.org/10.1111/ddi.12453

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