Pseudomonas fluorescens MFE01 delivers a putative type VI secretion amidase that confers biocontrol against the soft-rot pathogen Pectobacterium atrosepticum.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
11 2023
11 2023
Historique:
received:
14
12
2022
accepted:
15
08
2023
medline:
15
11
2023
pubmed:
25
8
2023
entrez:
25
8
2023
Statut:
ppublish
Résumé
The type VI secretion system (T6SS) is a contractile nanomachine widespread in Gram-negative bacteria. The T6SS injects effectors into target cells including eukaryotic hosts and competitor microbial cells and thus participates in pathogenesis and intermicrobial competition. Pseudomonas fluorescens MFE01 possesses a single T6SS gene cluster that confers biocontrol properties by protecting potato tubers against the phytopathogen Pectobacterium atrosepticum (Pca). Here, we demonstrate that a functional T6SS is essential to protect potato tuber by reducing the pectobacteria population. Fluorescence microscopy experiments showed that MFE01 displays an aggressive behaviour with an offensive T6SS characterized by continuous and intense T6SS firing activity. Interestingly, we observed that T6SS firing is correlated with rounding of Pectobacterium cells, suggesting delivery of a potent cell wall targeting effector. Mutagenesis coupled with functional assays then revealed that a putative T6SS secreted amidase, Tae3
Identifiants
pubmed: 37622480
doi: 10.1111/1462-2920.16492
doi:
Substances chimiques
Type VI Secretion Systems
0
Bacterial Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2564-2579Informations de copyright
© 2023 The Authors. Environmental Microbiology published by Applied Microbiology International and John Wiley & Sons Ltd.
Références
Alcoforado Diniz, J., Liu, Y.-C. & Coulthurst, S.J. (2015) Molecular weaponry: diverse effectors delivered by the type VI secretion system. Cellular Microbiology, 17, 1742-1751. Available from: https://doi.org/10.1111/cmi.12532
Allsopp, L.P., Bernal, P., Nolan, L.M. & Filloux, A. (2020) Causalities of war: the connection between type VI secretion system and microbiota. Cellular Microbiology, 22, e13153. Available from: https://doi.org/10.1111/cmi.13153
Aschtgen, M.S., Bernard, C.S., Bentzmann, S., Lloubès, R. & Cascales, E. (2008) SciN is an outer membrane lipoprotein required for type VI secretion in Enteroaggregative Escherichia coli. Journal of Bacteriology, 190, 7523-7531. Available from: https://doi.org/10.1128/JB.00945-08
Aschtgen, M.S., Gavioli, M., Dessen, A., Lloubès, R. & Cascales, E. (2010) The SciZ protein anchors the enteroaggregative Escherichia coli type VI secretion system to the cell wall. Molecular Microbiology, 75, 886-899. Available from: https://doi.org/10.1111/j.1365-2958.2009.07028.x
Barbey, C., Crépin, A., Bergeau, A., Ouchiha, A., Mijouin, L., Taupin, L. et al. (2013) In planta biocontrol of Pectobacterium atrosepticum by Rhodococcus erythropolis involves silencing of pathogen communication by the rhodococcal gamma-lactone catabolic pathway. PLoS One, 8, e66642. Available from: https://doi.org/10.1371/journal.pone.0066642
Barnard, A.M.L. & Salmond, G.P.C. (2007) Quorum sensing in Erwinia species. Analytical and Bioanalytical Chemistry, 387, 415-423. Available from: https://doi.org/10.1007/s00216-006-0701-1
Basler, M. (2015) Type VI secretion system: secretion by a contractile nanomachine. Philosophical Transactions of the Royal Society B: Biological Sciences, 370, 20150021. Available from: https://doi.org/10.1098/rstb.2015.0021
Basler, M., Pilhofer, M., Henderson, G.P., Jensen, G.J. & Mekalanos, J.J. (2012) Type VI secretion requires a dynamic contractile phage tail-like structure. Nature, 483, 182-186. Available from: https://doi.org/10.1038/nature10846
Bayer-Santos, E., Lima, L.D.P., Ceseti, L.M., Ratagami, C.Y., de Santana, E.S., da Silva, A.M. et al. (2018) Xanthomonas citri T6SS mediates resistance to Dictyostelium predation and is regulated by an ECF σ factor and cognate Ser/Thr kinase. Environmental Microbiology, 20, 1562-1575. Available from: https://doi.org/10.1111/1462-2920.14085
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. Available from: https://doi.org/10.1038/ismej.2016.169
Bernal, P., Llamas, M.A. & Filloux, A. (2018) Type VI secretion systems in plant-associated bacteria. Environmental Microbiology, 20, 1-15. Available from: https://doi.org/10.1111/1462-2920.13956
Bingle, L.E.H., Bailey, C.M. & Pallen, M.J. (2008) Type VI secretion: a beginner's guide. Current Opinion in Microbiology, 11, 3-8. Available from: https://doi.org/10.1016/j.mib.2008.01.006
Bogdanov, M. (2017) Mapping of membrane protein topology by substituted cysteine accessibility method (SCAMTM). In: Journet, L. & Cascales, E. (Eds.) Bacterial protein secretion systems. Methods in molecular biology, Vol. 1615. New York, NY: Springer New York, pp. 105-128. Available from: https://doi.org/10.1007/978-1-4939-7033-9_9
Bouteiller, M., Gallique, M., Bourigault, Y., Kosta, A., Hardouin, J., Massier, S. et al. (2020) Crosstalk between the type VI secretion system and the expression of class IV flagellar genes in the Pseudomonas fluorescens MFE01 strain. Microorganisms, 8, 622. Available from: https://doi.org/10.3390/microorganisms8050622
Boyer, F., Fichant, G., Berthod, J., Vandenbrouck, Y. & Attree, I. (2009) Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources? BMC Genomics, 10, 104. Available from: https://doi.org/10.1186/1471-2164-10-104
Brackmann, M., Nazarov, S., Wang, J. & Basler, M. (2017) Using force to punch holes: mechanics of contractile nanomachines. Trends in Cell Biology, 27, 623-632. Available from: https://doi.org/10.1016/j.tcb.2017.05.003
Brunet, Y.R., Espinosa, L., Harchouni, S., Mignot, T. & Cascales, E. (2013) Imaging type VI secretion-mediated bacterial killing. Cell Reports, 3, 36-41. Available from: https://doi.org/10.1016/j.celrep.2012.11.027
Cascales, E. (2008) The type VI secretion toolkit. EMBO Reports, 9, 735-741. Available from: https://doi.org/10.1038/embor.2008.131
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. Available from: https://doi.org/10.1111/1462-2920.15749
Ceseti, L.M., Santana, E.S., Ratagami, C.Y., Barreiros, Y., Lima, L.P., Dunger, G. et al. (2019) The Xanthomonas citri Pv. citri type VI secretion system is induced during epiphytic colonization of Citrus. Current Microbiology, 76, 1105-1111. Available from: https://doi.org/10.1007/s00284-019-01735-3
Chane, A., Barbey, C., Robert, M., Merieau, A., Ghiorghi, Y.K., Cirou, A.B. et al. (2019) Biocontrol of soft rot: confocal microscopy highlights virulent pectobacterial communication and its jamming by rhodococcal quorum-quenching. Molecular Plant-Microbe Interactions, 32, 802-812. Available from: https://doi.org/10.1094/MPMI-11-18-0314-R
Chassaing, B. & Cascales, E. (2018) Antibacterial weapons: targeted destruction in the microbiota. Trends in Microbiology, 26, 329-338. Available from: https://doi.org/10.1016/j.tim.2018.01.006
Chen, C., Yang, X. & Shen, X. (2019) Confirmed and potential roles of cacterial T6SSs in the intestinal ecosystem. Frontiers in Microbiology, 10, 1484. Available from: https://doi.org/10.3389/fmicb.2019.01484
Cherrak, Y., Flaugnatti, N., Durand, E., Journet, L. & Cascales, E. (2019) Structure and activity of the type VI secretion system. Microbiology Spectrum, 7, PSIB0031-2019. Available from: https://doi.org/10.1128/microbiospec.PSIB-0031-2019
Chou, S., Bui, N.K., Russell, A.B., Lexa, K.W., Gardiner, T.E., LeRoux, M. et al. (2012) Structure of a peptidoglycan amidase effector targeted to Gram-negative bacteria by the type VI secretion system. Cell Reports, 1, 656-664. Available from: https://doi.org/10.1016/j.celrep.2012.05.016
Cianfanelli, F.R., Monlezun, L. & Coulthurst, S.J. (2016) Aim, load, fire: the type VI secretion system, a bacterial nanoweapon. Trends in Microbiology, 24, 51-62. Available from: https://doi.org/10.1016/j.tim.2015.10.005
Coulthurst, S.J. (2019) The type VI secretion system: a versatile bacterial weapon. Microbiology, 165, 503-515. Available from: https://doi.org/10.1099/mic.0.000789
Crépin, A., Cirou, A.B., Barbey, B., Farmer, C., Hélias, V., Burini, J.F. et al. (2012) N-acyl homoserine lactones in diverse Pectobacterium and Dickeya plant pathogens: diversity, abundance, and involvement in virulence. Sensors, 12, 3484-3497. Available from: https://doi.org/10.3390/s120303484
Davey, M.E., Caiazza, N.C. & O'Toole, G.A. (2003) Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. Journal of Bacteriology, 185, 1027-1036. Available from: https://doi.org/10.1128/JB.185.3.1027-1036.2003
Decoin, V., Barbey, C., Bergeau, D., Latour, X., Feuilloley, M.G.J., Orange, N. et al. (2014) A type VI secretion system is involved in Pseudomonas fluorescens bacterial competition. PLoS One, 9, e89411. Available from: https://doi.org/10.1371/journal.pone.0089411
Decoin, V., Gallique, M., Barbey, C., Le Mauff, F., Duclairoir Poc, C., Feuilloley, M.G.J. et al. (2015) A Pseudomonas fluorescens type 6 secretion system is related to mucoidy, motility and bacterial competition. BMC Microbiology, 15, 72. Available from: https://doi.org/10.1186/s12866-015-0405-9
Deghelt, M., Cho, S.-H., Govers, S.K., Janssens, A., Dachsbeck, A., Remaut, H.K. et al. (2023) The outer membrane and peptidoglycan layer form a single mechanical device balancing turgor. BioRxiv. Available from: https://doi.org/10.1101/2023.04.29.538579
Diallo, S., Crépin, A., Barbey, C., Orange, N., Burini, J.F. & Latour, X. (2011) Mechanisms and recent advances in biological control mediated through the potato rhizosphere. FEMS Microbiology Ecology, 75, 351-364. Available from: 10.1111/j.1574-6941.2010.01023.x
Dupuis, B., Nkuriyingoma, P. & Van Gijsegem, F. (2021) Economic impact of Pectobacterium and Dickeya species on potato crops: a review and case study. In: Van Gijsegem, F., van der Wolf, J.M. & Toth, I.K. (Eds.) Plant diseases caused by Dickeya and Pectobacterium species. Springer Nature. Available from: https://doi.org/10.1007/978-3-030-61459-1_8
Durán, D., Bernal, P., Vazquez-Arias, D., Blanco-Romero, E., Garrido-Sanz, D., Redondo-Nieto, M. et al. (2021) Pseudomonas fluorescens F113 type VI secretion systems mediate bacterial killing and adaption to the rhizosphere microbiome. Scientific Reports, 11, 5772. Available from: https://doi.org/10.1038/s41598-021-85218-1
Durand, E., Cambillau, C., Cascales, E. & Journet, L. (2014) VgrG, Tae, Tle, and beyond: the versatile arsenal of type VI secretion effectors. Trends in Microbiology, 22, 498-507. Available from: https://doi.org/10.1016/j.tim.2014.06.004
El-Sayed, A.K., Hothersall, J. & Thomas, C.M. (2001) Quorum-sensing-dependent regulation of biosynthesis of the polyketide antibiotic mupirocin in Pseudomonas fluorescens NCIMB 10586. Microbiology, 147, 2127-2139.
Filip, C., Fletcher, G., Wulff, J.L. & Earhart, C.F. (1973) Solubilization of the cytoplasmic membrane of Escherichia coli by the ionic detergent sodium-lauryl sarcosinate. Journal of Bacteriology, 115, 717-722. Available from: https://doi.org/10.1128/jb.115.3.717-722.1973
Fu, Y., Waldor, M.K. & Mekalanos, J.J. (2013) Tn-Seq analysis of vibrio cholerae intestinal colonization reveals a role for T6SS-mediated antibacterial activity in the host. Cell Host & Microbe, 14, 652-663. Available from: https://doi.org/10.1016/j.chom.2013.11.001
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. Available from: https://doi.org/10.1093/femsre/fuab033
Gallique, M., Bouteiller, M. & Merieau, A. (2017) The type VI secretion system: a dynamic system for bacterial communication? Frontiers in Microbiology, 8, 1454. Available from: https://doi.org/10.3389/fmicb.2017.01454
Gallique, M., Decoin, V., Barbey, C., Rosay, T., Feuilloley, M.G.J., Orange, O. et al. (2017) Contribution of the Pseudomonas fluorescens MFE01 type VI secretion system to biofilm formation. PLoS One, 12, e0170770. Available from: https://doi.org/10.1371/journal.pone.0170770
Gerc, A.J., Diepold, A., Trunk, A., Porter, M., Rickman, C., Armitage, J.P. et al. (2015) Visualization of the Serratia type VI secretion system reveals unprovoked attacks and dynamic assembly. Cell Reports, 12, 2131-2142. Available from: https://doi.org/10.1016/j.celrep.2015.08.053
Haas, D. & Défago, G. (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nature Reviews Microbiology, 3, 307-319. Available from: https://doi.org/10.1038/nrmicro1129
Hernandez, R.E., Gallegos-Monterrosa, R. & Coulthurst, S.J. (2020) Type VI secretion system effector proteins: effective weapons for bacterial competitiveness. Cellular Microbiology, 22, e13241. Available from: https://doi.org/10.1111/cmi.13241
Ho, B.T., Dong, T.G. & Mekalanos, J.J. (2014) A view to a kill: the bacterial type VI secretion system. Cell Host & Microbe, 15, 9-21. Available from: https://doi.org/10.1016/j.chom.2013.11.008
Jurenas, D. & Journet, L. (2021) Activity, delivery, and diversity of type VI secretion effectors. Molecular Microbiology, 115, 383-394. Available from: https://doi.org/10.1111/mmi.14648
Kapitein, N. & Mogk, A. (2013) Deadly syringes: type VI secretion system activities in pathogenicity and interbacterial competition. Current Opinion in Microbiology, 16, 52-58. Available from: https://doi.org/10.1016/j.mib.2012.11.009
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. Available from: https://doi.org/10.1038/ncomms14888
Liu, H., Coulthurst, S.J., Pritchard, L., Hedley, P.E., Ravensdale, M., Humphris, S. et al. (2008) Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. PLoS Pathogens, 4, e1000093. Available from: https://doi.org/10.1371/journal.ppat.1000093
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. Available from: https://doi.org/10.1016/j.chom.2014.06.002
Mansfield, J., Genin, S., Magori, S., Citovsky, V., Sriariyanum, M., Ronald, P. et al. (2012) Top 10 plant pathogenic bacteria in molecular plant pathology. Molecular Plant Pathology, 13, 614-629. Available from: https://doi.org/10.1111/j.1364-3703.2012.00804.x
Marchi, M., Boutin, M., Gazengel, K., Rispe, C., Gauthier, J.P., Guillerm-Erckelboudt, A.Y. et al. (2013) Genomic analysis of the biocontrol strain Pseudomonas fluorescens Pf29Arp with evidence of T3SS and T6SS gene expression on plant roots. Environmental Microbiology Reports, 5, 393-403. Available from: https://doi.org/10.1111/1758-2229.12048
Maurhofer, M., Reimmann, C., Schmidli-Sacherer, P., Heeb, S., Haas, D. & Défago, G. (1998) Salicylic acid biosynthetic genes expressed in Pseudomonas fluorescens strain P3 improve the induction of systemic resistance in tobacco against tobacco necrosis virus. Phytopathology, 88, 678-684. Available from: https://doi.org/10.1094/PHYTO.1998.88.7.678
Miller, J.F. (2013) Gaming the competition in microbial cell-cell interactions. EMBO Journal, 32, 778-780. Available from: https://doi.org/10.1038/emboj.2013.45
Murdoch, S.L., Trunk, K., English, G., Fritsch, M.J., Pourkarimi, E. & Coulthurst, S.J. (2011) The opportunistic pathogen Serratia marcescens utilizes type VI secretion to target bacterial competitors. Journal of Bacteriology, 193, 6057-6069. Available from: https://doi.org/10.1128/JB.05671-11
Newman, J.R. & Fuqua, C. (1999) Broad-host-range expression vectors that carry the L-arabinose-inducible Escherichia coli araBAD promoter and the araC regulator. Gene, 227, 197-203. Available from: https://doi.org/10.1016/s0378-1119(98)00601-5
Ostrowski, A., Cianfanelli, F.R., Porter, M., Mariano, G., Peltier, J., Wong, J.J. et al. (2018) Killing with proficiency: integrated post-translational regulation of an offensive type VI secretion system. PLoS Pathogens, 14, e1007230. Available from: https://doi.org/10.1371/journal.ppat.1007230
Pérombelon, M.C.M. (2002) Potato diseases caused by soft rot Erwinias: an overview of pathogenesis. Plant Pathology, 51, 1-12. Available from: https://doi.org/10.1046/j.0032-0862.2001
Radkov, A., Sapiro, A.L., Flores, S., Henderson, C., Saunders, H., Kim, R. et al. (2022) Antibacterial potency of type VI amidase effector toxins is dependent on substrate topology and cellular context. eLife, 11, e79796. Available from: https://doi.org/10.7554/eLife.79796
Russell, A.B., Hood, R.D., Bui, N.K., LeRoux, M., Vollmer, W. & Mougous, J.D. (2011) Type VI secretion delivers bacteriolytic effectors to target cells. Nature, 475, 343-347. Available from: https://doi.org/10.1038/nature10244
Russell, A.B., Peterson, S.B. & Mougous, J.D. (2014) Type VI secretion system effectors: poisons with a purpose. Nature Reviews Microbiology, 12, 137-148. Available from: https://doi.org/10.1038/nrmicro3185
Russell, A.B., Singh, P., Brittnacher, M., Bui, N.K., Hood, R.D., Carl, M.A. et al. (2012) A widespread bacterial type VI secretion effector superfamily identified using a heuristic approach. Cell Host & Microbe, 11, 538-549. Available from: https://doi.org/10.1016/j.chom.2012.04.007
Sana, T.G., Flaugnatti, N., Lugo, K.A., Lam, L.H., Jacobson, A., Baylot, V. et al. (2016) Salmonella Typhimurium utilizes a T6SS-mediated antibacterial weapon to establish in the host gut. Proceedings of the National Academy of Sciences of the United States of America, 113, E5044-E5051. Available from: https://doi.org/10.1073/pnas.1608858113
Santin, Y.G., Doan, T., Journet, L. & Cascales, E. (2019) Cell width dictates type VI secretion tail length. Current Biology, 29, 3707-3713.e3. Available from: https://doi.org/10.1016/j.cub.2019.08.058
Santin, Y.G., Doan, T., Lebrun, R., Espinosa, L., Journet, L. & Cascales, E. (2018) In vivo TssA proximity labelling during type VI secretion biogenesis reveals TagA as a protein that stops and holds the sheath. Nature Microbiology, 3, 1304-1313. Available from: https://doi.org/10.1038/s41564-018-0234-3
Schneider, C.A., Rasband, W.S. & Eliceiri, K.W. (2012) NIH image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671-675. Available from: https://doi.org/10.1038/nmeth.2089
Schneider, J.P., Nazarov, S., Adaixo, R., Liuzzo, M., Ringel, P.D., Stahlberg, H. et al. (2019) Diverse roles of TssA-like proteins in the assembly of bacterial type VI secretion systems. The EMBO Journal, 38, e100825. Available from: https://doi.org/10.15252/embj.2018100825
Simon, R., Priefer, U. & Pühler, A. (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Nature Biotechnology, 1, 784-791.
Smadja, B., Latour, X., Faure, D., Chevalier, S., Dessaux, Y. & Orange, N. (2004) Involvement of N-acylhomoserine lactones throughout plant infection by Erwinia carotovora subsp. atroseptica (Pectobacterium atrosepticum). Molecular Plant-Microbe Interactions, 17, 1269-1278. Available from: https://doi.org/10.1094/MPMI.2004.17.11.1269
Taylor, N.M.I., van Raaij, M.J. & Leiman, P.G. (2018) Contractile injection systems of bacteriophages and related systems. Molecular Microbiology, 108, 6-15. Available from: https://doi.org/10.1111/mmi.13921
Tian, Y., Zhao, Y., Wu, X., Liu, F., Hu, B. & Walcott, R.R. (2015) The type VI protein secretion system contributes to biofilm formation and seed-to-seedling transmission of Acidovorax citrulli on melon. Molecular Plant Pathology, 16, 38-47. Available from: https://doi.org/10.1111/mpp.12159
Toth, I.K., Barny, M.A., Brurberg, M.B., Condemine, G., Czajkowski, R., Elphinstone, J.G. et al. (2021) Pectobacterium and Dickeya: environment to disease development. In: Van Gijsegem, F., van der Wolf, J.M. & Toth, I.K. (Eds.) Plant diseases caused by Dickeya and Pectobacterium species. Springer Nature. Available from: https://doi.org/10.1007/978-3-030-61459-1_3
Turner, T.R., James, E.K. & Poole, P.S. (2013) The plant microbiome. Genome Biology, 14, 209. Available from: https://doi.org/10.1186/gb-2013-14-6-209
Vacheron, J., Péchy-Tarr, M., Brochet, S., Heiman, C.M., Stojiljkovic, M., Maurhofer, M. et al. (2019) T6SS contributes to gut microbiome invasion and killing of an herbivorous pest insect by plant-beneficial Pseudomonas protegens. The ISME Journal, 13, 1318-1329. Available from: https://doi.org/10.1038/s41396-019-0353-8
van der Ent, F. & Löwe, J. (2006) RF cloning: a restriction-free method for inserting target genes into plasmids. Journal of Biochemical and Biophysical Methods, 67, 67-74. Available from: https://doi.org/10.1016/j.jbbm.2005.12.008
Van Gijsegem, F., Hugouvieux-Cotte-Pattat, N., Kraepiel, Y., Lojkowska, E., Moleleki, L.N., Gorshkov, V. et al. (2021) Molecular interactions of Pectobacterium and Dickeya with plants. In: Van Gijsegem, F., van der Wolf, J.M. & Toth, I.K. (Eds.) Plant diseases caused by Dickeya and Pectobacterium species. Springer Nature. Available from: https://doi.org/10.1007/978-3-030-61459-1_4
Wang, J., Brodmann, M. & Basler, M. (2019) Assembly and subcellular localization of bacterial type VI secretion systems. Annual Review of Microbiology, 73, 621-638. Available from: https://doi.org/10.1146/annurev-micro-020518-115420
Wang, T., Hu, Z., Du, X., Shi, Y., Dang, J., Lee, M. et al. (2020) A type VI secretion system delivers a cell wall amidase to target bacterial competitors. Molecular Microbiology, 114, 308-321. Available from: https://doi.org/10.1111/mmi.14513
Whitney, J.C., Chou, S., Russell, A.B., Biboy, J., Gardiner, T.E., Ferrin, M.A. et al. (2013) Identification, structure, and function of a novel type VI secretion peptidoglycan glycoside hydrolase effector-immunity pair. Journal of Biological Chemistry, 288, 26616-26624. Available from: https://doi.org/10.1074/jbc.M113.488320
Yang, X., Liu, H., Zhang, Y. & Shen, X. (2021) Roles of type VI secretion system in transport of metal ions. Frontiers in Microbiology, 12, 756136. Available from: https://doi.org/10.3389/fmicb.2021.756136
Zhang, L., Xu, J., Xu, J., Chen, K., He, L. & Feng, J. (2012) TssM is essential for virulence and required for type VI secretion in Ralstonia solanacearum. Journal of Plant Diseases and Protection, 119, 125-134. Available from: https://doi.org/10.1007/BF03356431