1,196
Views
2
CrossRef citations to date
0
Altmetric
Research Paper

Recombinant production of a diffusible signal factor inhibits Salmonella invasion and animal carriage

, , &
Article: 2208498 | Received 28 Feb 2023, Accepted 21 Apr 2023, Published online: 09 May 2023

References

  • Galan JE, Curtiss R 3rd. Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci U S A. 1989;86:6383–15. doi:10.1073/pnas.86.16.6383.
  • Eade CR, Bogomolnaya L, Hung CC, Betteken MI, Adams LG, Andrews-Polymenis H, Altier C. Salmonella pathogenicity Island 1 is expressed in the chicken intestine and promotes bacterial proliferation. Infect Immun. 2018. doi:10.1128/IAI.00503-18.
  • Lawley TD, Bouley DM, Hoy YE, Gerke C, Relman DA, Monack DM. Host transmission of Salmonella enterica serovar Typhimurium is controlled by virulence factors and indigenous intestinal microbiota. Infect Immun. 2008;76:403–416. doi:10.1128/IAI.01189-07.
  • Lawhon SD, Khare S, Rossetti CA, Everts RE, Galindo CL, Luciano SA, Figueiredo JF, Nunes JES, Gull T, Davidson GS, et al. Role of SPI-1 secreted effectors in acute bovine response to Salmonella enterica Serovar Typhimurium: a systems biology analysis approach. PLoS One. 2011;6:e26869. doi:10.1371/journal.pone.0026869.
  • Barthel M, Hapfelmeier S, Quintanilla-Martinez L, Kremer M, Rohde M, Hogardt M, Pfeffer K, Rüssmann H, Hardt W-D. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun. 2003;71:2839–2858. doi:10.1128/IAI.71.5.2839-2858.2003.
  • Ellermeier CD, Ellermeier JR, Slauch JM. HilD, HilC and RtsA constitute a feed forward loop that controls expression of the SPI1 type three secretion system regulator hilA in Salmonella enterica serovar Typhimurium. Mol Microbiol. 2005;57:691–705. doi:10.1111/j.1365-2958.2005.04737.x.
  • Altier C. Genetic and environmental control of salmonella invasion. J Microbiol. 2005;43 Spec No:85–92.
  • Bajaj V, Lucas RL, Hwang C, Lee CA. Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol Microbiol. 1996;22:703–714. doi:10.1046/j.1365-2958.1996.d01-1718.x.
  • Prouty AM, Gunn JS, DiRita VJ. Salmonella enterica serovar typhimurium invasion is repressed in the presence of bile. Infect Immun. 2000;68:6763–6769. doi:10.1128/IAI.68.12.6763-6769.2000.
  • Ellermeier JR, Slauch JM. Adaptation to the host environment: regulation of the SPI1 type III secretion system in Salmonella enterica serovar Typhimurium. Curr Opin Microbiol. 2007;10:24–29. doi:10.1016/j.mib.2006.12.002.
  • Golubeva YA, Ellermeier JR, Cott Chubiz JE, Slauch JM, Taylor RK. Intestinal long-chain fatty acids act as a direct signal to modulate expression of the salmonella pathogenicity Island 1 Type III secretion system. mBio. 2016;7: e02170-15. doi:10.1128/mBio.02170-15.
  • Hung CC, Garner CD, Slauch JM, Dwyer ZW, Lawhon SD, Frye JG, McClelland M, Ahmer BMM, Altier C. The intestinal fatty acid propionate inhibits salmonella invasion through the post-translational control of HilD. Mol Microbiol. 2013. doi:10.1111/mmi.12149.
  • Lawhon SD, Maurer R, Suyemoto M, Altier C. Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA. Mol Microbiol. 2002;46:1451–1464. doi:10.1046/j.1365-2958.2002.03268.x.
  • Zhou L, Zhang LH, Camara M, He YW. The DSF family of quorum sensing signals: diversity, biosynthesis, and turnover. Trends Microbiol. 2017;25:293–303. doi:10.1016/j.tim.2016.11.013.
  • Ionescu M, Yokota K, Antonova E, Garcia A, Beaulieu E, Hayes T, Iavarone AT, Lindow SE. Promiscuous diffusible signal factor production and responsiveness of the Xylella fastidiosa Rpf system. mBio. 2016;7. doi:10.1128/mBio.01054-16.
  • Bi H, Christensen QH, Feng Y, Wang H, Cronan JE. The Burkholderia cenocepacia BDSF quorum sensing fatty acid is synthesized by a bifunctional crotonase homologue having both dehydratase and thioesterase activities. Mol Microbiol. 2012;83:840–855. doi:10.1111/j.1365-2958.2012.07968.x.
  • Ryan RP, An SQ, Allan JH, McCarthy Y, Dow JM, Dehio C. The DSF family of cell–cell signals: an expanding class of bacterial virulence regulators. PLoS Pathog. 2015;11:e1004986. doi:10.1371/journal.ppat.1004986.
  • Ryan RP, Dow JM. Communication with a growing family: diffusible signal factor (DSF) signaling in bacteria. Trends Microbiol. 2011;19:145–152. doi:10.1016/j.tim.2010.12.003.
  • Ryan RP, Fouhy Y, Garcia BF, Watt SA, Niehaus K, Yang L, Tolker-Nielsen T, Dow JM. Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Mol Microbiol. 2008;68:75–86. doi:10.1111/j.1365-2958.2008.06132.x.
  • Bosire EM, Eade CR, Schiltz CJ, Reid AJ, Troutman J, Chappie JS, Altier C. Diffusible signal factors act through AraC-type transcriptional regulators as chemical cues to repress virulence of enteric pathogens. Infect Immun. 2020;88. doi:10.1128/IAI.00226-20.
  • Chowdhury R, Pavinski Bitar PD, Keresztes I, Condo AM Jr., Altier C, Baumler AJ. A diffusible signal factor of the intestine dictates Salmonella invasion through its direct control of the virulence activator HilD. PLoS Pathog. 2021;17:e1009357. doi:10.1371/journal.ppat.1009357.
  • Chowdhury R, Pavinski Bitar PD, Adams MC, Chappie JS, Altier C. AraC-type regulators HilC and RtsA are directly controlled by an intestinal fatty acid to regulate Salmonella invasion. Mol Microbiol. 2021;116:1464–1475. doi:10.1111/mmi.14835.
  • Mutalik VK, Guimaraes JC, Cambray G, Lam C, Christoffersen MJ, Mai QA, Tran AB, Paull M, Keasling JD, Arkin AP, et al. Precise and reliable gene expression via standard transcription and translation initiation elements. Nat Methods. 2013;10:354–360. doi:10.1038/nmeth.2404.
  • Wassenaar TM. Insights from 100 years of research with probiotic E. Coli. Eur J Microbiol Immunol. 2016;6:147–161. doi:10.1556/1886.2016.00029.
  • Cukrowska B, LodInova-ZadnIkova R, Enders C, Sonnenborn U, Schulze J, Tlaskalova-Hogenova H. Specific proliferative and antibody responses of premature infants to intestinal colonization with nonpathogenic probiotic E. coli strain Nissle 1917. Scand J Immunol. 2002;55:204–209. doi:10.1046/j.1365-3083.2002.01005.x.
  • Deriu E, Liu JZ, Pezeshki M, Edwards RA, Ochoa RJ, Contreras H, Libby, SJ, Fang, FC, Raffatellu, M. Probiotic bacteria reduce salmonella typhimurium intestinal colonization by competing for iron. Cell Host & Microbe. 2013;14:26–37. doi:10.1016/j.chom.2013.06.007.
  • Lodinova-Zadnikova R, Sonnenborn U. Effect of preventive administration of a nonpathogenic Escherichia coli strain on the colonization of the intestine with microbial pathogens in newborn infants. Biol Neonate. 1997;71:224–232. doi:10.1159/000244421.
  • Litvak Y, Mon KKZ, Nguyen H, Chanthavixay G, Liou M, Velazquez EM, Kutter L, Alcantara MA, Byndloss MX, Tiffany CR, et al. Commensal Enterobacteriaceae protect against salmonella colonization through oxygen competition. Cell Host & Microbe. 2019;25:128–39 e5. doi:10.1016/j.chom.2018.12.003.
  • Diard M, Garcia V, Maier L, Remus-Emsermann MN, Regoes RR, Ackermann M, Hardt W-D. Stabilization of cooperative virulence by the expression of an avirulent phenotype. Nature. 2013;494:353–356. doi:10.1038/nature11913.
  • Arnoldini M, Vizcarra IA, Pena-Miller R, Stocker N, Diard M, Vogel V, Beardmore RE, Hardt W-D, Ackermann M. Bistable expression of virulence genes in salmonella leads to the formation of an antibiotic-tolerant subpopulation. PLoS Biol. 2014;12:e1001928. doi:10.1371/journal.pbio.1001928.
  • Boyen F, Haesebrouck F, Vanparys A, Volf J, Mahu M, Van Immerseel F, Rychlik I, Dewulf J, Ducatelle R, Pasmans F. Coated fatty acids alter virulence properties of Salmonella Typhimurium and decrease intestinal colonization of pigs. Vet Microbiol. 2008;132:319–327. doi:10.1016/j.vetmic.2008.05.008.
  • Van Deun K, Haesebrouck F, Van Immerseel F, Ducatelle R, Pasmans F. Short-chain fatty acids and L-lactate as feed additives to control Campylobacter jejuni infections in broilers. Avian Pathol. 2008;37:379–383. doi:10.1080/03079450802216603.
  • Van Immerseel F, Boyen F, Gantois I, Timbermont L, Bohez L, Pasmans F, Haesebrouck F, Ducatelle R. Supplementation of coated butyric acid in the feed reduces colonization and shedding of Salmonella in poultry. Poult Sci. 2005;84:1851–1856. doi:10.1093/ps/84.12.1851.
  • Huang Y, Suyemoto M, Garner CD, Cicconi KM, Altier C. Formate acts as a diffusible signal to induce Salmonella invasion. J Bacteriol. 2008;190:4233–4241. doi:10.1128/JB.00205-08.
  • Cabre E, Hernandez-Perez JM, Fluvia L, Pastor C, Corominas A, Gassull MA. Absorption and transport of dietary long-chain fatty acids in cirrhosis: a stable-isotope-tracing study. Am J Clin Nutr. 2005;81:692–701. doi:10.1093/ajcn/81.3.692.
  • Thiennimitr P, Winter SE, Baumler AJ. Salmonella, the host and its microbiota. Curr Opin Microbiol. 2012;15:108–114. doi:10.1016/j.mib.2011.10.002.
  • Thiennimitr P, Winter SE, Winter MG, Xavier MN, Tolstikov V, Huseby DL, Sterzenbach T, Tsolis RM, Roth JR, Bäumler AJ. Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc Natl Acad Sci U S A. 2011;108:17480–17485. doi:10.1073/pnas.1107857108.
  • Winter SE, Thiennimitr P, Winter MG, Butler BP, Huseby DL, Crawford RW, Russell, JM, Bevins, CL, Adams, LG, Tsolis, RM, Roth, JR, Baumler, AJ. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature. 2010;467:426–429. doi:10.1038/nature09415.
  • Ackermann M, Stecher B, Freed NE, Songhet P, Hardt WD, Doebeli M. Self-destructive cooperation mediated by phenotypic noise. Nature. 2008;454:987–990. doi:10.1038/nature07067.
  • Cason JA, Hinton A Jr., Northcutt JK, Buhr RJ, Ingram KD, Smith DP, Cox NA. Partitioning of external and internal bacteria carried by broiler chickens before processing. J Food Prot. 2007;70:2056–2062. doi:10.4315/0362-028X-70.9.2056.
  • de Boer HA, Comstock LJ, Vasser M, de Boer HA. The tac promoter: a functional hybrid derived from the trp and lac promoters. Proc Natl Acad Sci U S A. 1983;80:21–25. doi:10.1073/pnas.80.1.21.
  • Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A. 2000;97:6640–6645. doi:10.1073/pnas.120163297.
  • Dole VP, Meinertz H. Microdetermination of long-chain fatty acids in plasma and tissues. J Biol Chem. 1960;235:2595–2599. doi:10.1016/S0021-9258(19)76920-8.
  • Miller JH. Experiments in molecular genetics. New York: Cold Spring Harbor; 1972.
  • Chowdhury R, Mandal RS, Ta A, Das S. An AIL family protein promotes type three secretion system-1-independent invasion and pathogenesis of Salmonella enterica serovar Typhi. Cell Microbiol. 2015;17:486–503. doi:10.1111/cmi.12379.