The type VI secretion system of Stenotrophomonas rhizophila CFBP13503 limits the transmission of Xanthomonas campestris pv. campestris 8004 from radish seeds to seedlings.
Stenotrophomas rhizophila
Xanthomonas campestris pv. campestris
interbacterial competition
seed
seedling transmission
type VI secretion system
Journal
Molecular plant pathology
ISSN: 1364-3703
Titre abrégé: Mol Plant Pathol
Pays: England
ID NLM: 100954969
Informations de publication
Date de publication:
Jan 2024
Jan 2024
Historique:
revised:
20
10
2023
received:
20
07
2023
accepted:
27
11
2023
medline:
28
1
2024
pubmed:
28
1
2024
entrez:
27
1
2024
Statut:
ppublish
Résumé
Stenotrophomonas rhizophila CFBP13503 is a seedborne commensal bacterial strain, which is efficiently transmitted to seedlings and can outcompete the phytopathogenic bacterium Xanthomonas campestris pv. campestris (Xcc8004). The type VI secretion system (T6SS), an interference contact-dependent mechanism, is a critical component of interbacterial competition. The involvement of the T6SS of S. rhizophila CFBP13503 in the inhibition of Xcc8004 growth and seed-to-seedling transmission was assessed. The T6SS cluster of S. rhizophila CFBP13503 and nine putative effectors were identified. Deletion of two T6SS structural genes, hcp and tssB, abolished the competitive advantage of S. rhizophila against Xcc8004 in vitro. The population sizes of these two bacterial species were monitored in seedlings after inoculation of radish seeds with mixtures of Xcc8004 and either S. rhizophila wild-type (wt) strain or isogenic hcp mutant. A significant decrease in the population size of Xcc8004 was observed during confrontation with the S. rhizophila wt in comparison with T6SS-deletion mutants in germinated seeds and seedlings. We found that the T6SS distribution among 835 genomes of the Stenotrophomonas genus is scarce. In contrast, in all available S. rhizophila genomes, T6SS clusters are widespread and mainly belong to the T6SS group i4. In conclusion, the T6SS of S. rhizophila CFBP13503 is involved in the antibiosis against Xcc8004 and reduces seedling transmission of Xcc8004 in radish. The distribution of this T6SS cluster in the S. rhizophila complex could make it possible to exploit these strains as biocontrol agents against X. campestris pv. campestris.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13412Subventions
Organisme : Conseil Régional des Pays de la Loire
Organisme : Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement
Informations de copyright
© 2024 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd.
Références
Alanjary, M., Steinke, K. & Ziemert, N. (2019) AutoMLST: an automated web server for generating multi-locus species trees highlighting natural product potential. Nucleic Acids Research, 47, W276-W282.
Alavi, P., Starcher, M., Zachow, C., Mueller, H. & Berg, G. (2013) Root-microbe systems: the effect and mode of interaction of stress protecting agent (SPA) Stenotrophomonas rhizophila DSM14405T. Frontiers in Plant Science, 4, 141.
Baker, K.F. & Smith, S.H. (1966) Dynamics of seed transmission of plant pathogens. Annual Review of Phytopathology, 4, 311-332.
Barret, M., Guimbaud, J., Darrasse, A. & Jacques, M. (2016) Plant microbiota affects seed transmission of phytopathogenic microorganisms. Molecular Plant Pathology, 17, 791-795.
Bayer-Santos, E., de Moraes Ceseti, L., Farah, C.S. & Alvarez-Martinez, C.E. (2019) Distribution, function and regulation of type 6 secretion systems of Xanthomonadales. Frontiers in Microbiology, 10, 1635.
Berg, G. & Ballin, G. (1994) Bacterial antagonists to Verticillium dahliae Kleb. Journal of Phytopathology, 141, 99-110.
Berg, G., Marten, P. & Ballin, G. (1996) Stenotrophomonas maltophilia in the rhizosphere of oilseed rape-occurrence, characterization and interaction with phytopathogenic fungi. Microbiological Research, 151, 19-27.
Bernal, P., Allsopp, L.P., Filloux, A. & Llamas, M.A. (2017) The Pseudomonas putida T6SS is a plant warden against phytopathogens. The ISME Journal, 11, 972-987.
Bernal, P., Llamas, M.A. & Filloux, A. (2018) Type VI secretion systems in plant-associated bacteria. Environmental Microbiology, 20, 1-15.
Berni, B., Soscia, C., Djermoun, S., Ize, B. & Bleves, S. (2019) A type VI secretion system trans-kingdom effector is required for the delivery of a novel antibacterial toxin in Pseudomonas aeruginosa. Frontiers in Microbiology, 10, 1218.
Briand, M., Bouzid, M., Hunault, G., Legeay, M., Fischer-Le Saux, M. & Barret, M. (2021) A rapid and simple method for assessing and representing genome sequence relatedness. Peer Community Journal, 1, e24.
Cassan, F.D., Coniglio, A., Amavizca, E., Maroniche, G., Cascales, E., Bashan, Y. et al. (2021) The Azospirillum brasilense type VI secretion system promotes cell aggregation, biocontrol protection against phytopathogens and attachment to the microalgae Chlorella sorokiniana. Environmental Microbiology, 23, 6257-6274.
Cerutti, A., Jauneau, A., Auriac, M.-C., Lauber, E., Martinez, Y., Chiarenza, S. et al. (2017) Immunity at cauliflower hydathodes controls systemic infection by Xanthomonas campestris pv. campestris. Plant Physiology, 174, 700-716.
Chen, W.-J., Kuo, T.-Y., Hsieh, F.-C., Chen, P.-Y., Wang, C.-S., Shih, Y.-L. et al. (2016) Involvement of type VI secretion system in secretion of iron chelator pyoverdine in Pseudomonas taiwanensis. Scientific Reports, 6, 32950.
Cherrak, Y., Flaugnatti, N., Durand, E., Journet, L. & Cascales, E. (2019) Structure and activity of the type VI secretion system. Microbiology Spectrum, 7. Available from: https://doi.org/10.1128/microbiolspec.PSIB-0031-2019
Chesneau, G., Laroche, B., Préveaux, A., Marais, C., Briand, M., Marolleau, B. et al. (2022) Single seed microbiota: assembly and transmission from parent plant to seedling. mBio, 13, e01648-22.
Choi, Y., Kim, N., Mannaa, M., Kim, H., Park, J., Jung, H. et al. (2020) Characterization of type VI secretion system in Xanthomonas oryzae pv. oryzae and its role in virulence to rice. The Plant Pathology Journal, 36, 289-296.
Cianfanelli, F.R., Diniz, J.A., Guo, M., Cesare, V.D., Trost, M. & Coulthurst, S.J. (2016) VgrG and PAAR proteins define distinct versions of a functional type VI secretion system. PLoS Pathogens, 12, e1005735.
Darrasse, A., Darsonval, A., Boureau, T., Brisset, M.-N., Durand, K. & Jacques, M.-A. (2010) Transmission of plant-pathogenic bacteria by nonhost seeds without induction of an associated defense reaction at emergence. Applied and Environmental Microbiology, 76, 6787-6796.
Decoin, V., Barbey, C., Bergeau, D., Latour, X., Feuilloley, M.G., Orange, N. et al. (2014) A type VI secretion system is involved in Pseudomonas fluorescens bacterial competition. PLoS One, 9, e89411.
Denancé, N. & Grimault, V. (2022) Seed pathway for pest dissemination: the ISTA reference pest list, a bibliographic resource in non-vegetable crops. EPPO Bulletin, 52, 434-445.
Egamberdieva, D., Kucharova, Z., Davranov, K., Berg, G., Makarova, N., Azarova, T. et al. (2011) Bacteria able to control foot and root rot and to promote growth of cucumber in salinated soils. Biology and Fertility of Soils, 47, 197-205.
Engering, A., Hogerwerf, L. & Slingenbergh, J. (2013) Pathogen-host-environment interplay and disease emergence. Emerging Microbes & Infections, 2, e5.
Fei, N., Ji, W., Yang, L., Yu, C., Qiao, P., Yan, J. et al. (2022) Hcp of the type VI secretion system (T6SS) in Acidovorax citrulli group II strain Aac5 has a dual role as a core structural protein and an effector protein in colonization, growth ability, competition, biofilm formation, and ferric iron absorption. International Journal of Molecular Sciences, 23, 9632.
Ferrières, L., Hémery, G., Nham, T., Guérout, A.-M., Mazel, D., Beloin, C. et al. (2010) Silent mischief: bacteriophage mu insertions contaminate products of Escherichia coli random mutagenesis performed using suicidal transposon delivery plasmids mobilized by broad-host-range RP4 conjugative machinery. Journal of Bacteriology, 192, 6418-6427.
Flaugnatti, N., Le, T.T.H., Canaan, S., Aschtgen, M.-S., Nguyen, V.S., Blangy, S. et al. (2016) A phospholipase A1 antibacterial type VI secretion effector interacts directly with the C-terminal domain of the VgrG spike protein for delivery. Molecular Microbiology, 99, 1099-1118.
Flaugnatti, N., Rapisarda, C., Rey, M., Beauvois, S.G., Nguyen, V.A., Canaan, S. et al. (2020) Structural basis for loading and inhibition of a bacterial T6SS phospholipase effector by the VgrG spike. The EMBO Journal, 39, e104129.
Gallegos-Monterrosa, R. & Coulthurst, S.J. (2021) The ecological impact of a bacterial weapon: microbial interactions and the type VI secretion system. FEMS Microbiology Reviews, 45, fuab033.
Gouy, M., Guindon, S. & Gascuel, O. (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution, 27, 221-224.
Granato, E.T., Meiller-Legrand, T.A. & Foster, K.R. (2019) The evolution and ecology of bacterial warfare. Current Biology, 29, R521-R537.
Gröschel, M.I., Meehan, C.J., Barilar, I., Diricks, M., Gonzaga, A., Steglich, M. et al. (2020) The phylogenetic landscape and nosocomial spread of the multidrug-resistant opportunist Stenotrophomonas maltophilia. Nature Communications, 11, 2044.
Hersch, S.J., Manera, K. & Dong, T.G. (2020) Defending against the type six secretion system: beyond immunity genes. Cell Reports, 33, 10-13.
Ho, B.T., Dong, T.G. & Mekalanos, J.J. (2014) A view to kill: the bacterial type VI secretion system. Cell, Host & Microbe, 15, 9-21.
Hoang, T.T., Karkhoff-Schweizer, R.R., Kutchma, A.J. & Schweizer, H.P. (1998) A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene, 212, 77-86.
Holm, L., Laiho, A., Törönen, P. & Salgado, M. (2023) DALI shines a light on remote homologs: one hundred discoveries. Protein Science, 32, e4519.
Hunt, M., Silva, N.D., Otto, T.D., Parkhill, J., Keane, J.A. & Harris, S.R. (2015) Circlator: automated circularization of genome assemblies using long sequencing reads. Genome Biology, 16, 294.
Jacques, M.-A., Arlat, M., Boulanger, A., Boureau, T., Carrère, S., Cesbron, S. et al. (2016) Using ecology, physiology, and genomics to understand host specificity in Xanthomonas. Annual Review of Phytopathology, 54, 163-187.
Jiang, F., Wang, X., Wang, B., Chen, L., Zhao, Z., Waterfield, N.R. et al. (2016) The Pseudomonas aeruginosa type VI secretion PGAP1-like effector induces host autophagy by activating endoplasmic reticulum stress. Cell Reports, 16, 1502-1509.
Jiang, F., Waterfield, N.R., Yang, J., Yang, G. & Jin, Q. (2014) A Pseudomonas aeruginosa type VI secretion phospholipase D effector targets both procaryotic and eukaryotic cells. Cell, Host & Microbe, 15, 600-610.
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O. et al. (2021) Highly accurate protein structure prediction with AlphaFold. Nature, 596, 583-589.
Jurėnas, D. & Journet, L. (2021) Activity, delivery, and diversity of type VI secretion effectors. Molecular Microbiology, 115, 383-394.
Kolmogorov, M., Yuan, J., Lin, Y. & Pevzner, P.A. (2019) Assembly of long, error-prone reads using repeat graphs. Nature Biotechnology, 37, 540-546.
LaCourse, K.D., Peterson, S.B., Kulasekara, H.D., Radey, M.C., Kim, J. & Mougous, J.D. (2018) Conditional toxicity and synergy drive diversity among antibacterial effectors. Nature Microbiology, 3, 440-446.
Lien, Y.-W. & Lai, E.-M. (2017) Type VI secretion effectors: methodologies and biology. Frontiers in Cellular and Infection Microbiology, 7, 254.
Lin, J., Zhang, W., Cheng, J., Yang, X., Zhu, K., Wang, Y. et al. (2017) A Pseudomonas T6SS effector recruits PQS-containing outer membrane vesicles for iron acquisition. Nature Communications, 8, 14888.
Lin, J.-S., Pissaridou, P., Wu, H.-H., Tsai, M.-D., Filloux, A. & Lai, E.-M. (2018) TagF-mediated repression of bacterial type VI secretion systems involves a direct interaction with the cytoplasmic protein Fha. Journal of Biological Chemistry, 293, 8829-8842.
Lin, L., Capozzoli, R., Ferrand, A., Plum, M., Vettiger, A. & Basler, M. (2022) Subcellular localization of type VI secretion system assembly in response to cell-cell contact. EMBO Journal, 41, e108595.
Liu, Y., Gao, J., Wang, N., Li, X., Fang, N. & Zhuang, X. (2022) Diffusible signal factor enhances the saline-alkaline resistance and rhizosphere colonization of Stenotrophomonas rhizophila by coordinating optimal metabolism. Science of the Total Environment, 834, 155403.
Liyanapathiranage, P., Jones, J.B. & Potnis, N. (2021) A mutation of a single core gene, tssM, of type VI secretion system of Xanthomonas perforans influences virulence, epiphytic survival and transmission during pathogenesis on tomato. Phytopathology, 112, 752-764.
Lopez, J., Le, N.H., Moon, K.H., Salomon, D., Bosis, E. & Feldman, M.F. (2021) Formylglycine-generating enzyme-like proteins constitute a novel family of widespread type VI secretion system immunity proteins. Journal of Bacteriology, 203, e00281-21.
Lottmann, J., Heuer, H., Smalla, K. & Berg, G. (1999) Influence of transgenic T4-lysozyme-producing potato plants on potentially beneficial plant-associated bacteria. FEMS Microbiology Ecology, 29, 365-377.
Luo, J., Chu, X., Jie, J., Sun, Y., Guan, Q., Li, D. et al. (2023) Acinetobacter baumannii kills fungi via a type VI DNase effector. mBio, 14, e03420-22.
Ma, L.-S., Hachani, A., Lin, J.-S., Filloux, A. & Lai, E.-M. (2014) Agrobacterium tumefaciens deploys a superfamily of type VI secretion DNase effectors as weapons for interbacterial competition in planta. Cell, Host & Microbe, 16, 94-104.
Minkwitz, A. & Berg, G. (2001) Comparison of antifungal activities and 16S ribosomal DNA sequences of clinical and environmental isolates of Stenotrophomonas maltophilia. Journal of Clinical Microbiology, 39, 139-145.
Miyata, S.T., Unterweger, D., Rudko, S.P. & Pukatzki, S. (2013) Dual expression profile of type VI secretion system immunity genes protects pandemic Vibrio cholerae. PLoS Pathogens, 9, e1003752.
Montenegro Benavides, N.A., Alvarez, B.A., Arrieta-Ortiz, M.L., Rodriguez-R, L.M., Botero, D., Tabima, J.F. et al. (2021) The type VI secretion system of Xanthomonas phaseoli pv. manihotis is involved in virulence and in vitro motility. BMC Microbiology, 21, 14.
Mosquito, S., Bertani, I., Licastro, D., Compant, S., Myers, M.P., Hinarejos, E. et al. (2019) In planta colonization and role of T6SS in two rice Kosakonia endophytes. Molecular Plant-Microbe Interactions, 33, 349-363.
Néron, B., Denise, R., Coluzzi, C., Touchon, M., Rocha, E.P.C. & Abby, S.S. (2023) MacSyFinder v2: improved modelling and search engine to identify molecular systems in genomes. Peer Community Journal, 3, e28.
Newcombe, G., Harding, A., Ridout, M. & Busby, P.E. (2018) A hypothetical bottleneck in the plant microbiome. Frontiers in Microbiology, 9, 1645.
Parks, D.H., Imelfort, M., Skennerton, C.T., Hugenholtz, P. & Tyson, G.W. (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Research, 25, 1043-1055.
Randhawa, P. (1984) Selective isolation of Xanthomonas campestris pv. campestris from crucifer seeds. Phytopathology, 74, 268-272.
Rezki, S., Campion, C., Iacomi-Vasilescu, B., Preveaux, A., Toualbia, Y., Bonneau, S. et al. (2016) Differences in stability of seed-associated microbial assemblages in response to invasion by phytopathogenic microorganisms. PeerJ, 4, e1923.
Rezki, S., Campion, C., Simoneau, P., Jacques, M.-A., Shade, A. & Barret, M. (2018) Assembly of seed-associated microbial communities within and across successive plant generations. Plant and Soil, 422, 67-79.
Russell, A.B., LeRoux, M., Hathazi, K., Agnello, D.M., Ishikawa, T., Wiggins, P.A. et al. (2013) Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature, 496, 508-512.
Sambrook, J. & Russell, D.W. (2006) The Inoue method for preparation and transformation of competent E. coli: “ultra-competent” cells. Cold Spring Harbor Protocols, 2006, pdb.prot3944.
Schmidt, C.S., Alavi, M., Cardinale, M., Müller, H. & Berg, G. (2012) Stenotrophomonas rhizophila DSM14405T promotes plant growth probably by altering fungal communities in the rhizosphere. Biology and Fertility of Soils, 48, 947-960.
Seemann, T. (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics, 30, 2068-2069.
Shyntum, D.Y., Theron, J., Venter, S.N., Moleleki, L.N., Toth, I.K. & Coutinho, T.A. (2015) Pantoea ananatis utilizes a type VI secretion system for pathogenesis and bacterial competition. Molecular Plant-Microbe Interactions, 28, 420-431.
Si, M., Zhao, C., Burkinshaw, B., Zhang, B., Wei, D., Wang, Y. et al. (2017) Manganese scavenging and oxidative stress response mediated by type VI secretion system in Burkholderia thailandensis. Proceedings of the National Academy of Sciences of the United States of America, 114, E2233-E2242.
Simonin, M., Briand, M., Chesneau, G., Rochefort, A., Marais, C., Sarniguet, A. et al. (2022) Seed microbiota revealed by a large-scale meta-analysis including 50 plant species. New Phytologist, 234, 1448-1463.
Simonin, M., Préveaux, A., Marais, C., Garin, T., Arnault, G., Sarniguet, A. et al. (2023) Transmission of synthetic seed bacterial communities to radish seedlings: impact on microbiota assembly and plant phenotype. Peer Community Journal, 3, e95.
Storey, D., McNally, A., Åstrand, M., Santos, J., sa-Pessoa Graca Santos, J., Rodriguez-Escudero, I. et al. (2020) Klebsiella pneumoniae type VI secretion system-mediated microbial competition is PhoPQ controlled and reactive oxygen species dependent. PLoS Pathogens, 16, e1007969.
Torres-Cortés, G., Garcia, B.J., Compant, S., Rezki, S., Jones, P., Préveaux, A. et al. (2019) Differences in resource use lead to coexistence of seed-transmitted microbial populations. Scientific Reports, 9, 6648.
Trunk, K., Peltier, J., Liu, Y.-C., Dill, B.D., Walker, L., Gow, N.A.R. et al. (2018) The type VI secretion system deploys antifungal effectors against microbial competitors. Nature Microbiology, 3, 920-931.
Unterweger, D., Kostiuk, B. & Pukatzki, S. (2017) Adaptor proteins of type VI secretion system effectors. Trends in Microbiology, 25, 8-10.
van der Wolf, J., Kastelein, P., da Silva Júnior, T.A., Lelis, F.V. & van der Zouwen, P. (2019) Colonization of siliques and seeds of rapid cycling Brassica oleracea plants by Xanthomonas campestris pv. campestris after spray-inoculation of flower clusters. European Journal of Plant Pathology, 154, 445-461.
van Kempen, M., Kim, S.S., Tumescheit, C., Mirdita, M., Lee, J., Gilchrist, C.L.M. et al. (2023) Fast and accurate protein structure search with Foldseek. Nature Biotechnology. Available from: https://doi.org/10.1038/s41587-023-01773-0
Vicente, J.G. & Holub, E.B. (2013) Xanthomonas campestris pv. campestris (cause of black rot of crucifers) in the genomic era is still a worldwide threat to brassica crops. Molecular Plant Pathology, 14, 2-18.
Walker, B.J., Abeel, T., Shea, T., Priest, M., Abouelliel, A., Sakthikumar, S. et al. (2014) Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One, 9, e112963.
Weber, B.S., Hennon, S.W., Wright, M.S., Scott, N.E., de Berardinis, V., Foster, L.J. et al. (2016) Genetic dissection of the type VI secretion system in Acinetobacter and identification of a novel peptidoglycan hydrolase, Tagx, required for its biogenesis. mBio, 7, e01253-16.
Wolf, A., Fritze, A., Hagemann, M. & Berg, G. (2002) Stenotrophomonas rhizophila sp. nov., a novel plant-associated bacterium with antifungal properties. International Journal of Systematic and Evolutionary Microbiology, 52, 1937-1944.
Xia, Y., Li, K., Li, J., Wang, T., Gu, L. & Xun, L. (2019) T5 exonuclease-dependent assembly offers a low-cost method for efficient cloning and site-directed mutagenesis. Nucleic Acids Research, 47, e15.
Zhang, J., Guan, J., Wang, M., Li, G., Djordjevic, M., Tai, C. et al. (2022) SecReT6 update: a comprehensive resource of bacterial type VI secretion systems. Science China Life Sciences, 66, 626-634.