Skip to main content
SpringerLink
Log in

Furanone and phytol influence metabolic phenotypes regulated by acyl-homoserine lactone in Salmonella

  • Food Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Salmonella is an important foodborne pathogen, and it is unable to produce the quorum sensing signaling molecules called acyl-homoserine lactones (AHLs). However, it synthesizes the SdiA protein, detecting AHL molecules, also known as autoinducer-1 (AI-1), in the external environment. Exogenous AHLs can regulate specific genes related to virulence and stress response in Salmonella. Thus, interfering with quorum sensing can be a strategy to reduce virulence and help elucidate the cell-to-cell communication role in the pathogens' response to extracellular signals. This study aimed to evaluate the influence of the quorum sensing inhibitors furanone and phytol on phenotypes regulated by N-dodecanoyl homoserine lactone (C12-HSL) in Salmonella enterica serovar Enteritidis. The furanone C30 at 50 nM and phytol at 2 mM canceled the alterations promoted by C12-HSL on glucose consumption and the levels of free cellular thiol in Salmonella Enteritidis PT4 578 under anaerobic conditions. In silico analysis suggests that these compounds can bind to the SdiA protein of Salmonella Enteritidis and accommodate in the AHL binding pocket. Thus, furanone C30 and phytol act as antagonists of AI-1 and are likely inhibitors of the quorum sensing mechanism mediated by AHL in Salmonella.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Zhao S, White DG, Friedman SL et al (2008) Antimicrobial resistance in Salmonella enterica serovar Heidelberg isolates from retail meats, including poultry, from 2002 to 2006. Appl Environ Microbiol 74:6656–6662. https://doi.org/10.1128/AEM.01249-08

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Santhi LP, Sunkoji S, Siddiram S et al (2012) Patent research in salmonellosis prevention. Food Res Int 45:809–818. https://doi.org/10.1016/j.foodres.2011.11.006

    Article  Google Scholar 

  3. Stanaway JD, Parisi A, Sarkar K et al (2019) The global burden of non-typhoidal Salmonella invasive disease: a systematic analysis for the global burden of disease study 2017. Lancet Infect Dis 19:1312–1324. https://doi.org/10.1016/S1473-3099(19)30418-9

    Article  Google Scholar 

  4. Balasubramanian R, Im J, Lee JS et al (2019) The global burden and epidemiology of invasive non-typhoidal Salmonella infections. Hum Vaccin Immunother 15:1421–1426. https://doi.org/10.1080/21645515.2018.1504717

    Article  PubMed  Google Scholar 

  5. Ong SY, Ng FL, Badai SS et al (2010) Analysis and construction of pathogenicity island regulatory pathways in Salmonella enterica serovar Typhi. J Integr Bioinform 7:145. https://doi.org/10.2390/biecoll-jib-2010-145

    Article  Google Scholar 

  6. Fookes M, Schroeder GN, Langridge GC et al (2011) Salmonella bongori provides insights into the evolution of the Salmonellae. PLoS Pathog 7:e1002191. https://doi.org/10.1371/journal.ppat.1002191

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Kaur J, Jain SK (2012) Role of antigens and virulence factors of Salmonella enterica serovar Typhi in its pathogenesis. Microbiol Res 167:199–210. https://doi.org/10.1016/j.micres.2011.08.001

    Article  PubMed  CAS  Google Scholar 

  8. Nieto PA, Pardo-Roa C, Salazar-Echegarai FJ et al (2016) New insights about excisable pathogenicity islands in Salmonella and their contribution to virulence. Microbes Infect 18:302–309. https://doi.org/10.1016/j.micinf.2016.02.001

    Article  PubMed  CAS  Google Scholar 

  9. Van TTH, Nguyen HNK, Smooker PM et al (2012) The antibiotic resistance characteristics of non-typhoidal Salmonella enterica isolated from food-producing animals, retail meat and humans in South East Asia. Int J Food Microbiol 154:98–106. https://doi.org/10.1016/j.ijfoodmicro.2011.12.032

    Article  PubMed  CAS  Google Scholar 

  10. Fabrega A, Vila J (2013) Salmonella enterica serovar Typhimurium skills to succeed in the host: virulence and regulation. Clin Microbiol Rev 26:308–341. https://doi.org/10.1128/CMR.00066-12

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Runkel S, Wells HC, Rowley G (2013) Chapter Three - Living with stress: a lesson from the enteric pathogen Salmonella enterica. Adv Appl Microbiol 83:87–144. https://doi.org/10.1016/B978-0-12-407678-5.00003-9

    Article  PubMed  CAS  Google Scholar 

  12. Dandekar T, Fieselmann A, Fischer E et al (2015) Salmonella - how a metabolic generalist adopts an intracellular lifestyle during infection. Front Cell Infect Microbiol 4:191. https://doi.org/10.3389/fcimb.2014.00191

    Article  PubMed  PubMed Central  Google Scholar 

  13. Rivera-Chávez F, Bäumler AJ (2015) The pyromaniac inside you: Salmonella metabolism in the host gut. Annu Rev Microbiol 69:31–48. https://doi.org/10.1146/annurev-micro-091014-104108

    Article  PubMed  CAS  Google Scholar 

  14. Herrero-Fresno A, Olsen JE (2018) Salmonella Typhimurium metabolism affects virulence in the host – A mini-review. Food Microbiol 71:98–110. https://doi.org/10.1016/j.fm.2017.04.016

    Article  PubMed  CAS  Google Scholar 

  15. Michael B, Smith JN, Swift S et al (2001) SdiA of Salmonella enterica is a LuxR homolog that detects mixed microbial communities. J Bacteriol 183:5733–5742. https://doi.org/10.1128/JB.183.19.5733-5742.2001

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Smith JN, Ahmer BMM (2003) Detection of other microbial species by Salmonella: expression of the SdiA regulon. J Bacteriol 185:1357–1366. https://doi.org/10.1128/JB.185.4.1357-1366.2003

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Sabag-Daigle A, Soares JA, Smith JN (2012) The acyl homoserine lactone receptor, SdiA, of Escherichia coli and Salmonella enterica serovar Typhimurium does not respond to indole. Appl Environ Microbiol 78:5424–5431. https://doi.org/10.1128/AEM.00046-12

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Abed N, Grépinet O, Canepa S et al (2014) Direct regulation of the pefI-srgC operon encoding the Rck invasin by the quorum-sensing regulator SdiA in Salmonella Typhimurium. Mol Microbiol 94:254–271. https://doi.org/10.1111/mmi.12738

    Article  PubMed  CAS  Google Scholar 

  19. Ahmer BMM (2004) Cell-to-cell signalling in Escherichia coli and Salmonella enterica. Mol Microbiol 52:933–945. https://doi.org/10.1111/j.1365-2958.2004.04054.x

    Article  PubMed  CAS  Google Scholar 

  20. Walters M, Sperandio V (2006) Quorum sensing in Escherichia coli and Salmonella. Int J Med Microbiol 296:125–131. https://doi.org/10.1016/j.ijmm.2006.01.041

    Article  PubMed  CAS  Google Scholar 

  21. Ahmer BMM, van Reeuwijk J, Timmers CD et al (1998) Salmonella Typhimurium encodes an SdiA homolog, a putative quorum sensor of the LuxR family, that regulates genes on the virulence plasmid. J Bacteriol 180:1185–1193. https://doi.org/10.1128/JB.180.5.1185-1193.1998

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Campos-Galvão MEM, Leite TDS, Ribon AOB et al (2015) A new repertoire of information about the quorum sensing system in Salmonella enterica serovar Enteritidis PT4. Genet Mol Res 14:4068–4084. https://doi.org/10.4238/2015.April.27.22

    Article  PubMed  CAS  Google Scholar 

  23. Campos-Galvão MEM, Ribon AOB, Araújo EF et al (2016) Changes in the Salmonella enterica Enteritidis phenotypes in presence of acyl-homoserine lactone quorum sensing signals. J Basic Microbiol 56:493–501. https://doi.org/10.1002/jobm.201500471

    Article  PubMed  CAS  Google Scholar 

  24. Nesse LL, Berg K, Vestby LK et al (2011) Salmonella Typhimurium invasion of HEp-2 epithelial cells in vitro is increased by N-acyl-homoserine lactone quorum sensing signals. Acta Vet Scand 53:44. https://doi.org/10.1186/1751-0147-53-44

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Liu Z, Que F, Liao L et al (2014) Study on the promotion of bacterial biofilm formation by a Salmonella conjugative plasmid and the underlying mechanism. PLoS One 9:e109808. https://doi.org/10.1371/journal.pone.0109808

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Almeida FA, Pimentel-Filho NJ, Pinto UM et al (2017) Acyl homoserine lactone-based quorum sensing stimulates biofilm formation by Salmonella Enteritidis in anaerobic conditions. Arch Microbiol 199:475–486. https://doi.org/10.1007/s00203-016-1313-6

    Article  PubMed  CAS  Google Scholar 

  27. Almeida FA, Pimentel-Filho NJ, Carrijo LC et al (2017) Acyl homoserine lactone changes the abundance of proteins and the levels of organic acids associated with stationary phase in Salmonella Enteritidis. Microb Pathog 102:148–159. https://doi.org/10.1016/j.micpath.2016.11.027

    Article  PubMed  CAS  Google Scholar 

  28. Almeida FA, Carneiro DG, Mendes TAO et al (2018) Vanetti, N-dodecanoyl-homoserine lactone influences the levels of thiol and proteins related to oxidation-reduction process in Salmonella. PLoS One 13:e0204673. https://doi.org/10.1371/journal.pone.0204673

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Carneiro DG, Almeida FA, Aguilar AP et al (2020) Salmonella enterica optimizes metabolism after addition of acyl-homoserine lactone under anaerobic conditions. Front Microbiol 11:1459. https://doi.org/10.3389/fmicb.2020.01459

    Article  PubMed  PubMed Central  Google Scholar 

  30. Landman C, Grill JP, Mallet JM et al (2018) Inter-kingdom effect on epithelial cells of the N-acyl homoserine lactone 3-oxo-C12:2, a major quorum-sensing molecule from gut microbiota. PLoS One 13:e0202587. https://doi.org/10.1371/journal.pone.0202587

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Galloway WRJD, Hodgkinson JT, Bowden S et al (2012) Applications of small molecule activators and inhibitors of quorum sensing in Gram-negative bacteria. Trends Microbiol 20:449–458. https://doi.org/10.1016/j.tim.2012.06.003

    Article  PubMed  CAS  Google Scholar 

  32. Defoirdt T, Brackman G, Coenye T (2013) Quorum sensing inhibitors: how strong is the evidence? Trends Microbiol 21:619–624. https://doi.org/10.1016/j.tim.2013.09.006

    Article  PubMed  CAS  Google Scholar 

  33. Kalia VC (2013) Quorum sensing inhibitors: an overview. Biotechnol Adv 31:224–245. https://doi.org/10.1016/j.biotechadv.2012.10.004

    Article  PubMed  CAS  Google Scholar 

  34. Quecán BXV, Rivera MLC, Pinto UM (2018) Bioactive phytochemicals targeting microbial activities mediated by quorum sensing. In: Kalia V (ed) Biotechnological applications of quorum sensing inhibitors. Springer Singapore, Singapore, pp 397–416. https://doi.org/10.1007/978-981-10-9026-4_19

  35. Rémy B, Mion S, Plener L et al (2018) Interference in bacterial quorum sensing: a biopharmaceutical perspective. Front Pharmacol 9:203. https://doi.org/10.3389/fphar.2018.00203

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. García-Contreras R, Wood TK, Tomás M (2019) Editorial: quorum network (sensing/quenching) in multidrug-resistant pathogens. Front Cell Infect Microbiol 9:80. https://doi.org/10.3389/fcimb.2019.00080

    Article  PubMed  PubMed Central  Google Scholar 

  37. Jiang Q, Chen J, Yang C et al (2019) Quorum sensing: a prospective therapeutic target for bacterial diseases. Biomed Res Int 2019:1–15. https://doi.org/10.1155/2019/2015978

    Article  CAS  Google Scholar 

  38. Kalia VC, Patel SKS, Kang YC et al (2019) Quorum sensing inhibitors as antipathogens: biotechnological applications. Biotechnol Adv 37:68–90. https://doi.org/10.1016/j.biotechadv.2018.11.006

    Article  PubMed  CAS  Google Scholar 

  39. Saeki EK, Kobayashi RKT, Nakazato G (2020) Quorum sensing system: target to control the spread of bacterial infections. Microb Pathog 142:104068. https://doi.org/10.1016/j.micpath.2020.104068

    Article  PubMed  CAS  Google Scholar 

  40. Rasmussen TB, Manefield M, Andersen JB et al (2000) How Delisea pulchra furanones affect quorum sensing and swarming motility in Serratia liquefaciens MG1. Microbiology 146:3237–3244. https://doi.org/10.1099/00221287-146-12-3237

    Article  PubMed  CAS  Google Scholar 

  41. Hentzer M, Wu H, Andersen JB et al (2003) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22:3803–3815. https://doi.org/10.1093/emboj/cdg366

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Janssens JCA, Steenackers H, Robijns S et al (2008) Brominated furanones inhibit biofilm formation by Salmonella enterica serovar Typhimurium. Appl Environ Microbiol 74:6639–6648. https://doi.org/10.1128/AEM.01262-08

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Vestby LK, Lönn-Stensrud J, Møretrø T et al (2010) A synthetic furanone potentiates the effect of disinfectants on Salmonella in biofilm. J Appl Microbiol 108:771–778. https://doi.org/10.1111/j.1365-2672.2009.04495.x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Vestby LK, Johannesen KCS, Witsø IL (2014) Synthetic brominated furanone F202 prevents biofilm formation by potentially human pathogenic Escherichia coli O103:H2 and Salmonella ser. Agona on abiotic surfaces. J Appl Microbiol 116:258–268. https://doi.org/10.1111/jam.12355

    Article  PubMed  CAS  Google Scholar 

  45. Liu Z, Wang W, Zhu Y et al (2013) Antibiotics at subinhibitory concentrations improve the quorum sensing behavior of Chromobacterium violaceum. FEMS Microbiol Lett 341:37–44. https://doi.org/10.1111/1574-6968.12086

    Article  PubMed  CAS  Google Scholar 

  46. Pejin B, Ciric A, Glamoclija J et al (2014) In vitro anti-quorum sensing activity of phytol. Nat Prod Res 29:374–377. https://doi.org/10.1080/14786419.2014.945088

    Article  PubMed  CAS  Google Scholar 

  47. Srinivasan R, Devi KR, Kannappan A et al (2016) Piper betle and its bioactive metabolite phytol mitigates quorum sensing mediated virulence factors and biofilm of nosocomial pathogen Serratia marcescens in vitro. J Ethnopharmacol 193:592–603. https://doi.org/10.1016/j.jep.2016.10.017

    Article  PubMed  CAS  Google Scholar 

  48. Srinivasan R, Mohankumar R, Kannappan A et al (2017) Exploring the anti-quorum sensing and antibiofilm efficacy of phytol against Serratia marcescens associated acute pyelonephritis infection in Wistar rats. Front Cell Infect Microbiol 7:498. https://doi.org/10.3389/fcimb.2017.00498

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Almeida FA, Vargas ELG, Carneiro DG et al (2018) Virtual screening of plant compounds and nonsteroidal anti-inflammatory drugs for inhibition of quorum sensing and biofilm formation in Salmonella. Microb Pathog 121:369–388. https://doi.org/10.1016/j.micpath.2018.05.014

    Article  PubMed  CAS  Google Scholar 

  50. Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  51. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77. https://doi.org/10.1016/0003-9861(59)90090-6

    Article  PubMed  CAS  Google Scholar 

  52. Riddles PW, Blakeley RL, Zerner B (1979) Ellman’s reagent: 5,5′-dithiobis(2-nitrobenzoic acid) - a reexamination. Anal Biochem 94:75–81. https://doi.org/10.1016/0003-2697(79)90792-9

    Article  PubMed  CAS  Google Scholar 

  53. Ferreira DF (2011) Sisvar: a computer statistical analysis system. Ciênc Agrotec 35:1039–1042. https://doi.org/10.1590/S1413-70542011000600001

    Article  Google Scholar 

  54. Almeida FA, Pinto UM, Vanetti MCD (2016) Novel insights from molecular docking of SdiA from Salmonella Enteritidis and Escherichia coli with quorum sensing and quorum quenching molecules. Microb Pathog 99:178–190. https://doi.org/10.1016/j.micpath.2016.08.024

    Article  PubMed  CAS  Google Scholar 

  55. Quecán BXV, Santos JTC, Rivera MLC et al (2019) Effect of quercetin rich onion extracts on bacterial quorum sensing. Front Microbiol 10:867. https://doi.org/10.3389/fmicb.2019.00867

    Article  PubMed  PubMed Central  Google Scholar 

  56. Rajab MS, Cantrell CL, Franzblau SG et al (1998) Antimycobacterial activity of (E)-phytol and derivatives: a preliminary structure-activity study. Planta Med 64:2–4. https://doi.org/10.1055/s-2006-957354

    Article  PubMed  CAS  Google Scholar 

  57. Inoue Y, Hada T, Shiraishi A et al (2005) Biphasic effects of geranylgeraniol, teprenone, and phytol on the growth of Staphylococcus aureus. Antimicrob Agents Chemother 49:1770–1774. https://doi.org/10.1128/AAC.49.5.1770-1774.2005

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. Saikia D, Parihar S, Chanda D et al (2010) Antitubercular potential of some semisynthetic analogues of phytol. Bioorganic Med Chem Lett 20:508–512. https://doi.org/10.1016/j.bmcl.2009.11.107

    Article  CAS  Google Scholar 

  59. Pejin B, Savic A, Sokovic M et al (2014) Further in vitro evaluation of antiradical and antimicrobial activities of phytol. Nat Prod Res 28:372–376. https://doi.org/10.1080/14786419.2013.869692

    Article  PubMed  CAS  Google Scholar 

  60. Srinivasan R, Kannappan A, Sivasankar C et al (2018) Biofim inhibitory efficiency of phytol in combination with cefotaxime against nosocomial pathogen Acinetobacter baumannii. J Appl Microbiol 125:56–71. https://doi.org/10.1111/jam.13741

    Article  CAS  Google Scholar 

  61. Forman HJ, Zhang H, Rinna A (2009) Glutathione: overview of its protective roles, measurement, and biosynthesis. Mol Aspects Med 30:1–12. https://doi.org/10.1016/j.mam.2008.08.006

    Article  PubMed  CAS  Google Scholar 

  62. Ku JW, Gan YH (2019) Modulation of bacterial virulence and fitness by host glutathione. Curr Opin Microbiol 47:8–13. https://doi.org/10.1016/j.mib.2018.10.004

    Article  PubMed  CAS  Google Scholar 

  63. Kumawat M, Pesingi PK, Agarwal RK et al (2016) Contribution of protein isoaspartate methyl transferase (PIMT) in the survival of Salmonella Typhimurium under oxidative stress and virulence. Int J Med Microbiol 306:222–230. https://doi.org/10.1016/j.ijmm.2016.04.005

    Article  PubMed  CAS  Google Scholar 

  64. Bjur E, Eriksson-Ygberg S, Åslund F et al (2006) Thioredoxin 1 promotes intracellular replication and virulence of Salmonella enterica serovar Typhimurium. Infect Immun 74:5140–5151. https://doi.org/10.1128/IAI.00449-06

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Aussel L, Zhao W, Hébrard M et al (2011) Salmonella detoxifying enzymes are sufficient to cope with the host oxidative burst. Mol Microbiol 80:628–640. https://doi.org/10.1111/j.1365-2958.2011.07611.x

    Article  PubMed  CAS  Google Scholar 

  66. García-Contreras R, Nuñez-López L, Jasso-Chávez R et al (2015) Quorum sensing enhancement of the stress response promotes resistance to quorum quenching and prevents social cheating. ISME J 9:115–125. https://doi.org/10.1038/ismej.2014.98

    Article  PubMed  CAS  Google Scholar 

  67. Nguyen Y, Nguyen NX, Rogers JL et al (2015) Structural and mechanistic roles of novel chemical ligands on the SdiA quorum-sensing transcription regulator. MBio 6:e02429-e2514. https://doi.org/10.1128/mbio.02429-14

    Article  PubMed  PubMed Central  Google Scholar 

  68. Freitas LL, Silva FP, Fernandes KM et al (2021) The virulence of Salmonella Enteritidis in Galleria mellonella is improved by N-dodecanoyl-homoserine lactone. Microb Pathog 152:104730. https://doi.org/10.1016/j.micpath.2021.104730

    Article  CAS  Google Scholar 

  69. Freitas LL, Santos CIA, Carneiro DG et al (2020) Nisin and acid resistance in Salmonella is enhanced by N-dodecanoyl-homoserine lactone. Microb Pathog 147:104320. https://doi.org/10.1016/j.micpath.2020.104320

    Article  CAS  Google Scholar 

  70. Alvarez HM, Steinbüchel A (2002) Triacylglycerols in prokaryotic microorganisms. Appl Microbiol Biotechnol 60:367–376. https://doi.org/10.1007/s00253-002-1135-0

    Article  PubMed  CAS  Google Scholar 

  71. Liu Q, Siloto RMP, Lehner R et al (2012) Acyl-CoA: diacylglycerol acyltransferase: molecular biology, biochemistry and biotechnology. Prog Lipid Res 51:350–377. https://doi.org/10.1016/j.plipres.2012.06.001

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Erika Lorena Giraldo Vargas was supported by a fellowship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and this research has also been supported by CAPES. The authors acknowledge the CLC bio of the QIAGEN Company by the license of the CLC Drug Discovery Workbench 4.0 software.

Funding

This work was financially supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, code 001) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

Author information

Authors and Affiliations

  1. Department of Microbiology, Universidade Federal de Viçosa (UFV), Viçosa, MG, Brazil

    Erika Lorena Giraldo Vargas, Leonardo Luiz de Freitas & Maria Cristina Dantas Vanetti

  2. Department of Nutrition, Universidade Federal de Juiz de Fora (UFJF), Governador Valadares, MG, Brazil

    Felipe Alves de Almeida

  3. Food Research Center, Department of Food and Experimental Nutrition, Universidade de São Paulo (USP), São Paulo, SP, Brazil

    Uelinton Manoel Pinto

Authors
  1. Erika Lorena Giraldo Vargas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Felipe Alves de Almeida
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Leonardo Luiz de Freitas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Uelinton Manoel Pinto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maria Cristina Dantas Vanetti
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Erika Lorena Giraldo Vargas was responsible for conceptualization, methodology, investigation, writing, and preparing the original draft. Felipe Alves de Almeida was involved in conceptualization, investigation, writing, and reviewing. Leonardo Luiz de Freitas carried out investigation. Uelinton Manoel Pinto wrote and prepared the original draft and reviewed the manuscript. Maria Cristina Dantas Vanetti participated in conceptualization, supervision, project administration, writing-reviewing, and editing.

Corresponding author

Correspondence to Maria Cristina Dantas Vanetti.

Ethics declarations

Ethical approval

Not required.

Consent to participate

Not applicable.

Consent for publication

The authors Erika Lorena Giraldo Vargas, Felipe Alves de Almeida, Leonardo Luiz de Freitas, Uelinton Manoel Pinto, and Maria Cristina Dantas Vanetti are in accordance with the submission of this manuscript to the Brazilian Journal of Microbiology.

Competing interests

None to declare.

Additional information

Responsible Editor: Luiz Henrique Rosa

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vargas, E.L.G., Almeida, F.A., de Freitas, L.L. et al. Furanone and phytol influence metabolic phenotypes regulated by acyl-homoserine lactone in Salmonella. Braz J Microbiol 53, 2133–2144 (2022). https://doi.org/10.1007/s42770-022-00809-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-022-00809-y

Keywords

Search

Navigation