Galan, J. E. & Waksman, G. Protein-injection machines in bacteria. Cell 172, 1306–1318 (2018).
Deng, W. et al. Assembly, structure, function and regulation of type III secretion systems. Nat. Rev. Microbiol 15, 323–337 (2017).
Han J., et al. Infection biology of Salmonella enterica. EcoSal. Plus 12, eesp00012023 (2023).
Galán, J. E. & Curtiss, R. Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc. Natl. Acad. Sci. USA 86, 6383–6387 (1989).
Galán, J. E. Salmonella Typhimurium and inflammation: a pathogen-centric affair. Nat. Rev. Microbiol. 19, 716–725 (2021).
Fattinger, S. A., Sellin, M. E. & Hardt, W. D. Salmonella effector driven invasion of the gut epithelium: breaking in and setting the house on fire. Curr. Opin. Microbiol 64, 9–18 (2021).
Shea, J. E., Hensel, M., Gleeson, C. & Holden, D. W. Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 93, 2593–2597 (1996).
Hensel, M. et al. Simultaneous identification of bacterial virulence genes by negative selection. Science 269, 400–403 (1995).
Maier, L. et al. Granulocytes impose a tight bottleneck upon the gut luminal pathogen population during Salmonella typhimurium colitis. PLoS Pathog. 10, e1004557 (2014).
Hapfelmeier, S. et al. The Salmonella pathogenicity island (SPI)-2 and SPI-1 type III secretion systems allow Salmonella serovar typhimurium to trigger colitis via MyD88-dependent and MyD88-independent mechanisms. J. Immunol. 174, 1675–1685 (2005).
LaRock, D. L., Chaudhary, A. & Miller, S. I. Salmonellae interactions with host processes. Nat. Rev. Microbiol 13, 191–205 (2015).
Pillay T. D., et al. Speaking the host language: how Salmonella effector proteins manipulate the host. Microbiology (Reading) 169, 001342 (2023).
Jennings, E., Thurston, T. L. M. & Holden, D. W. Salmonella SPI-2 type III secretion system effectors: molecular mechanisms and physiological consequences. Cell Host Microbe 22, 217–231 (2017).
Haraga, A., Ohlson, M. B. & Miller, S. I. Salmonellae interplay with host cells. Nat. Rev. Microbiol 6, 53–66 (2008).
Chen, D. et al. Systematic reconstruction of an effector-gene network reveals determinants of Salmonella cellular and tissue tropism. Cell Host Microbe 29, 1531–1544.e9 (2021).
Bayer-Santos, E. et al. The Salmonella effector SteD mediates MARCH8-dependent ubiquitination of MHC II molecules and inhibits T cell activation. Cell Host Microbe 20, 584–595 (2016).
Stapels, D. A. C. et al. Salmonella persisters undermine host immune defenses during antibiotic treatment. Science 362, 1156–1160 (2018).
Buckner, M. M. C., Croxen, M., Arena, E. T. & Finlay, B. B. A comprehensive study of the contribution of Salmonella enterica serovar Typhimurium SPI2 effectors to bacterial colonization, survival, and replication in typhoid fever, macrophage, and epithelial cell infection models. Virulence 2, 208–216 (2011).
Figueira R., Watson K. G., Holden D. W., Helaine S. Identification of Salmonella pathogenicity island-2 type iii secretion system effectors involved in intramacrophage replication of S. enterica serovar typhimurium: implications for rational vaccine design. mBio. https://doi.org/10.1128/mbio.00065-13 (2013).
Knuff-Janzen, K., Tupin, A., Yurist-Doutsch, S., Rowland, J. L. & Finlay, B. B. Multiple Salmonella-pathogenicity island 2 effectors are required to facilitate bacterial establishment of its intracellular niche and virulence. PLOS ONE 15, e0235020 (2020).
Matsuda S., Haneda T., Saito H., Miki T., Okada N. Salmonella enterica effectors SifA, SpvB, SseF, SseJ, and SteA contribute to type III secretion system 1-independent inflammation in a streptomycin-pretreated mouse model of colitis. Infect. Immun. 87, e00872-18 (2019).
Datsenko, K. A. & Wanner, B. L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. 97, 6640–6645 (2000).
Porwollik, S. et al. Defined single-gene and multi-gene deletion mutant collections in Salmonella enterica sv Typhimurium. PLoS One 9, e99820 (2014).
Zinder, N. D. & Lederberg, J. Genetic exchange in Salmonella. J. Bacteriol. 64, 679–699 (1952).
Zinder, N. D. Bacterial transduction. J. Cell Physiol. Suppl. 45, 23–49 (1955).
Cherepanov, P. P. & Wackernagel, W. Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158, 9–14 (1995).
Shea, J. E., Beuzon, C. R., Gleeson, C., Mundy, R. & Holden, D. W. Influence of the Salmonella typhimurium pathogenicity island 2 type III secretion system on bacterial growth in the mouse. Infect. Immun. 67, 213–219 (1999).
Lawley, T. D. et al. Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog. 2, e11 (2006).
Newson, J. P. M. et al. Antibiotic-recalcitrant Salmonella exploits post-antibiotic microbiota disruption to achieve virulence-dependent transmission. Cell Rep. 44, 115969 (2025).
Meynell, G. G. & Stocker, B. A. D. Some hypotheses on the aetiology of fatal infections in partially resistant hosts and their application to mice challenged with Salmonella paratyphi-B or Salmonella typhimurium by Intraperitoneal injection. Microbiology 16, 38–58 (1957).
Bäumler, A. J., Tsolis, R. M., Valentine, P. J., Ficht, T. A. & Heffron, F. Synergistic effect of mutations in invA and lpfC on the ability of Salmonella typhimurium to cause murine typhoid. Infect. Immun. 65, 2254–2259 (1997).
Beuzón, C. R. et al. Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. The. EMBO J. 19, 3235–3249 (2000).
Daniel, B. B. J. et al. Assessing microbiome population dynamics using wild-type isogenic standardized hybrid (WISH)-tags. Nat. Microbiol 9, 1103–1116 (2024).
Sintsova A., et al. mBARq: a versatile and user-friendly framework for the analysis of DNA barcodes from transposon insertion libraries, knockout mutants, and isogenic strain populations. Bioinformatics 40, btae078 (2024).
Nguyen, A. T. & McSorley, S. J. Fighting the enemy within: systemic immune defense against mucosal Salmonella infection. Immunol. Lett. 270, 106930 (2024).
Coburn, B., Li, Y., Owen, D., Vallance, B. A. & Finlay, B. B. Salmonella enterica serovar Typhimurium pathogenicity island 2 is necessary for complete virulence in a mouse model of infectious enterocolitis. Infect. Immun. 73, 3219–3227 (2005).
Barthel, M. et al. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect. Immun. 71, 2839–2858 (2003). WD.
Stecher, B. et al. Comparison of Salmonella enterica serovar Typhimurium colitis in germfree mice and mice pretreated with streptomycin. Infect. Immun. 73, 3228–3241 (2005).
Kaniga, K., Bossio, J. C. & Galán, J. E. The Salmonella typhimurium invasion genes invF and invG encode homologues of the AraC and PulD family of proteins. Mol. Microbiol 13, 555–568 (1994).
Coombes, B. rianK. et al. Analysis of the contribution of Salmonella pathogenicity islands 1 and 2 to enteric disease progression using a novel bovine ileal loop model and a murine model of infectious enterocolitis. Infect. Immun. 73, 7161–7169 (2005).
Stecher, B. et al. Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol. 5, 2177–2189 (2007).
Diard, M. et al. Stabilization of cooperative virulence by the expression of an avirulent phenotype. Nature 494, 353–356 (2013).
Gül, E. et al. The microbiota conditions a gut milieu that selects for wild-type Salmonella Typhimurium virulence. PLoS Biol. 21, e3002253 (2023).
Spanò, S., Gao, X., Hannemann, S., Lara-Tejero, M. & Galán, J. E. A bacterial pathogen targets a host rab-family GTPase defense pathway with a GAP. Cell Host Microbe 19, 216–226 (2016).
Dolowschiak, T. et al. IFN-gamma hinders recovery from mucosal inflammation during antibiotic therapy for Salmonella gut infection. Cell Host Microbe 20, 238–249 (2016).
Fattinger, S. A. et al. Salmonella Typhimurium discreet-invasion of the murine gut absorptive epithelium. PLoS Pathog. 16, e1008503 (2020).
Ruano-Gallego D., et al. Type III secretion system effectors form robust and flexible intracellular virulence networks. Science 371, eabc9531 (2021).
Sanchez-Garrido, J., Alberdi, L., Chatterjee, S., Frankel, G. & Mullineaux-Sanders, C. Type III secretion system effector subnetworks elicit distinct host immune responses to infection. Curr. Opin. Microbiol 64, 19–26 (2021).
Sanchez-Garrido, J., Ruano-Gallego, D., Choudhary, J. S. & Frankel, G. The type III secretion system effector network hypothesis. Trends Microbiol 30, 524–533 (2022).
Wibawa R. R., Li P., McCaffrey K. & Hartland E. L. Using Genomic Deletion Mutants to Investigate Effector-Triggered Immunity During Legionella pneumophila Infection, p 23-41. In Kufer T. A., Kaparakis-Liaskos M. (ed), Effector-Triggered Immunity: Methods and Protocols, Springer (2022).
O’Connor, T. J., Boyd, D., Dorer, M. S. & Isberg, R. R. Aggravating genetic interactions allow a solution to redundancy in a bacterial pathogen. Science 338, 1440–1444 (2012).
Nguyen, B. D. et al. Import of Aspartate and Malate by DcuABC Drives H(2)/fumarate respiration to promote initial Salmonella gut-lumen colonization in mice. Cell Host Microbe 27, 922–936.e6 (2020).
Laganenka, L. et al. Interplay between chemotaxis, quorum sensing, and metabolism regulates Escherichia coli-Salmonella Typhimurium interactions in vivo. PLoS Pathog. 21, e1013156 (2025).
Chau N. Y. E., et al. (p)ppGpp-dependent regulation of the nucleotide hydrolase ppnn confers complement resistance in Salmonella enterica serovar typhimurium. Infect. Immun. 89, e00639-20 (2021).
Geiser P., et al. Salmonella enterica serovar typhimurium exploits cycling through epithelial cells to colonize human and murine enteroids. mBio 12, e02684-20 (2021).
Powers, T. R. et al. Intracellular niche-specific profiling reveals transcriptional adaptations required for the cytosolic lifestyle of Salmonella enterica. PLoS Pathog. 17, e1009280 (2021).
Schubert, C. et al. Monosaccharides drive Salmonella gut colonization in a context-dependent or -independent manner. Nat. Commun. 16, 1735 (2025).
Spanò, S. & Galán, J. E. A Rab32-dependent pathway contributes to Salmonella typhi host restriction. Science 338, 960–963 (2012).
Gerondopoulos, A., Langemeyer, L., Liang, J.-R., Linford, A. & Barr, F. rancisA. BLOC-3 mutated in hermansky-pudlak syndrome Is a Rab32/38 guanine nucleotide exchange factor. Curr. Biol. 22, 2135–2139 (2012).
Chen, M. et al. Itaconate is an effector of a Rab GTPase cell-autonomous host defense pathway against Salmonella. Science 369, 450–455 (2020).
Lian, H. et al. Parkinson’s disease kinase LRRK2 coordinates a cell-intrinsic itaconate-dependent defence pathway against intracellular Salmonella. Nat. Microbiol 8, 1880–1895 (2023).
Michelucci, A. et al. Immune-responsive gene 1 protein links metabolism to immunity by catalyzing itaconic acid production. Proc. Natl. Acad. Sci. USA 110, 7820–7825 (2013).
Hiyoshi, H. et al. Virulence factors perforate the pathogen-containing vacuole to signal efferocytosis. Cell Host Microbe 30, 163–170.e6 (2022).
Knodler, L. A. et al. Dissemination of invasive Salmonella via bacterial-induced extrusion of mucosal epithelia. Proc. Natl. Acad. Sci. USA 107, 17733–17738 (2010).
Grant, A. J. et al. Attenuated Salmonella Typhimurium lacking the pathogenicity island-2 type 3 secretion system grow to high bacterial numbers inside phagocytes in mice. PLoS Pathog. 8, e1003070 (2012).
Roudier, C., Fierer, J. & Guiney, D. G. Characterization of translation termination mutations in the spv operon of the Salmonella virulence plasmid pSDL2. J. Bacteriol. 174, 6418–6423 (1992).
Guiney D. G., Fierer J. The role of the spv genes in Salmonella pathogenesis. Front. Microbiol. 2, 129 (2011).
Lesnick, M. L., Reiner, N. E., Fierer, J. & Guiney, D. G. The Salmonella spvB virulence gene encodes an enzyme that ADP-ribosylates actin and destabilizes the cytoskeleton of eukaryotic cells. Mol. Microbiol 39, 1464–1470 (2001).
Tezcan-Merdol, D. et al. Actin is ADP-ribosylated by the Salmonella enterica virulence-associated protein SpvB. Mol. Microbiol 39, 606–619 (2001).
Libby, S. J., Lesnick, M., Hasegawa, P., Weidenhammer, E. & Guiney, D. G. The Salmonella virulence plasmid spv genes are required for cytopathology in human monocyte-derived macrophages. Cell Microbiol 2, 49–58 (2000).
Mazurkiewicz, P. et al. SpvC is a Salmonella effector with phosphothreonine lyase activity on host mitogen-activated protein kinases. Mol. Microbiol 67, 1371–1383 (2008).
Haneda, T. et al. Salmonella type III effector SpvC, a phosphothreonine lyase, contributes to reduction in inflammatory response during intestinal phase of infection. Cell Microbiol 14, 485–499 (2012).
Zhu, Y. et al. Structural insights into the enzymatic mechanism of the pathogenic MAPK phosphothreonine lyase. Mol. Cell 28, 899–913 (2007).
Grabe, G. J. et al. The Salmonella effector SpvD is a cysteine hydrolase with a serovar-specific polymorphism influencing catalytic activity, suppression of immune responses, and bacterial virulence. J. Biol. Chem. 291, 25853–25863 (2016).
Rolhion, N. et al. Inhibition of nuclear transport of NF-ĸB p65 by the Salmonella type III secretion system effector SpvD. PLOS Pathog. 12, e1005653 (2016).
Hoiseth, S. K. & Stocker, B. A. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291, 238–239 (1981).
Deatherage, D. E. & Barrick, J. E. Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq. Methods Mol. Biol. 1151, 165–188 (2014).
Grant, A. J. et al. Modelling within-host spatiotemporal dynamics of invasive bacterial disease. PLoS Biol. 6, e74 (2008).