Advertisement

Applied Microbiology and Biotechnology

, Volume 103, Issue 20, pp 8545–8557 | Cite as

Antibiofilm activity of coenzyme Q0 against Salmonella Typhimurium and its effect on adhesion–invasion and survival–replication

  • Yanpeng Yang
  • Jiahui Li
  • Yue Yin
  • Du Guo
  • Tong Jin
  • Ning Guan
  • Yiqi Shi
  • Yunfeng Xu
  • Sen Liang
  • Xiaodong Xia
  • Chao ShiEmail author
Applied microbial and cell physiology
  • 151 Downloads

Abstract

Salmonella Typhimurium, a common Gram-negative foodborne pathogen, threatens public health and hinders the development of the food industry. In this study, we evaluated the antibiofilm activity of coenzyme Q0 (CoQ0) against S. Typhimurium. Besides, the inhibition of the S. Typhimurium’s adhesion to and invasion of Caco-2 cells and its survival and replication in RAW 264.7 cells by CoQ0 were also explored. The minimum inhibitory concentrations and minimal bactericidal concentrations of CoQ0 against Salmonella were both 100–400 μg/mL. Salmonella Typhimurium biofilm formation was effectively inhibited by subinhibitory concentrations (SICs) of CoQ0. The CoQ0-affected biofilm morphology was observed with light microscopy and field-emission scanning electron microscopy. CoQ0 at SICs reduced the swimming motility and quorum sensing of S. Typhimurium and repressed the transcription of critical virulence-related genes. CoQ0 at SICs also clearly reduced the adhesion of S. Typhimurium to and its invasion of Caco-2 cells and reduced its survival and replication within RAW 264.7 macrophage cells. These findings suggest that CoQ0 has strong antibiofilm activity and can be used as an anti-infectious agent against Salmonella.

Keywords

Salmonella Typhimurium Coenzyme Q0 Antibiofilm Anti-infectious RAW264.7 Subinhibitory concentration 

Notes

Acknowledgments

We thank all the partners and laboratory members for their kind help.

Funding information

This work was financially supported by the Natural Science Foundation of China (31801659), the Fundamental Research Funds for the Central Universities (2452017228), and General Financial Grant from the China Postdoctoral Science Foundation (No. 2017M623256).

Compliance with ethical standards

Conflict of interest

The authors declare that there are no conflicts of interest.

Ethical statements

This paper is our original work. It has not been submitted elsewhere, and it is not under consideration in any other Journal. This article does not contain any studies with human participants or animals performed by any of the authors. All the authors have seen the manuscript and approved its submission to Applied Microbiology and Biotechnology.

References

  1. Bai JR, Zhong K, Wu YP, Elena G, Gao H (2019) Antibiofilm activity of shikimic acid against Staphylococcus aureus. Food Control 95:327–333.  https://doi.org/10.1016/j.foodcont.2018.08.020 CrossRefGoogle Scholar
  2. Bao KF, Yuan WY, Ma CB, Yu X, Wang L, Hong M, Xi XP, Zhou M, Chen TB (2018) Modification targeting the “Rana Box” motif of a novel nigrocin peptide from Hylarana latouchii enhances and broadens its potency against multiple bacteria. Front Microbiol 9:2846.  https://doi.org/10.3389/fmicb.2018.02846 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Baxter MA, Jones BD (2015) Two-component regulators control hilA expression by controlling fimZ and hilE expression within Salmonella enterica serovar Typhimurium. Infect Immun 83(3):978–985.  https://doi.org/10.1128/IAI.02506-14 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Birhanu BT, Park NH, Lee SJ, Hossain MA, Park SC (2018) Inhibition of Salmonella Typhimurium adhesion, invasion, and intracellular survival via treatment with methyl gallate alone and in combination with marbofloxacin. Vet Res 49(1):101.  https://doi.org/10.1186/s13567-018-0597-8 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bjarnsholt T, Buhlin K, Dufrene YF, Gomelsky M, Moroni A, Ramstedt M, Rumbaugh KP, Schulte T, Sun L, Akerlund B, Romling U (2018) Biofilm formation-what we can learn from recent developments. J Intern Med 284(4):332–345.  https://doi.org/10.1111/joim.12782 CrossRefPubMedGoogle Scholar
  6. Borges A, Serra S, Abreu AC, Saavedra MJ, Salgado A, Simoes M (2014) Evaluation of the effects of selected phytochemicals on quorum sensing inhibition and in vitro cytotoxicity. Biofouling 30(2):183–195.  https://doi.org/10.1080/08927014.2013.852542 CrossRefPubMedGoogle Scholar
  7. Cappitelli F, Polo A, Villa F (2014) Biofilm formation in food processing environments is still poorly understood and controlled. Food Eng Rev 6(1-2):29–42.  https://doi.org/10.1007/s12393-014-9077-8 CrossRefGoogle Scholar
  8. Chakroun I, Mahdhi A, Morcillo P, Cordero H, Cuesta A, Bakhrouf A, Mahdouani K, Esteban MÁ (2018) Motility, biofilm formation, apoptotic effect and virulence gene expression of atypical Salmonella Typhimurium outside and inside Caco-2 cells. Microb Pathog 114:153–162.  https://doi.org/10.1016/j.micpath.2017.11.010 CrossRefPubMedGoogle Scholar
  9. Choo JH, Rukayadi Y, Hwang JK (2006) Inhibition of bacterial quorum sensing by vanilla extract. Lett Appl Microbiol 42(6):637–641.  https://doi.org/10.1111/j.1472-765X.2006.01928.x CrossRefPubMedGoogle Scholar
  10. Chung CH, Yeh SC, Chen CJ, Lee KT (2014) Coenzyme Q0 from Antrodia cinnamomea in submerged cultures induces reactive oxygen species-mediated apoptosis in A549 human lung cancer cells. Evid Based Complement Alternat Med 2014(4):246748–246710.  https://doi.org/10.1155/2014/246748 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Clinical and Laboratory Standards Institute (2009) Clinical and Laboratory Standards Institute CLSI; CLSI Publishes 2009 Antimicrobial susceptibility testing standards. Atlanta, p 12Google Scholar
  12. Defoirdt T, Brackman G, Coenye T (2013) Quorum sensing inhibitors: how strong is the evidence? Trends Microbiol 21(12):619–624.  https://doi.org/10.1016/j.tim.2013.09.006 CrossRefPubMedGoogle Scholar
  13. DeGroote MA, Ochsner UA, Shiloh MU, Nathan C, McCord JM, Dinauer MC, Libby SJ, VazquezTorres A, Xu YS, Fang FC (1997) Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase. Proc Natl Acad Sci U S A 94(25):13997–14001.  https://doi.org/10.1073/pnas.94.25.13997 CrossRefGoogle Scholar
  14. Dhowlaghar N, Abeysundara PDA, Nannapaneni R, Schilling MW, Chang S, Cheng WH, Sharma CS (2018) Biofilm formation by Salmonella spp. in catfish mucus extract under industrial conditions. Food Microbiol:70.  https://doi.org/10.1016/j.fm.2017.09.016 CrossRefPubMedGoogle Scholar
  15. Dyszel JL, Smith JN, Lucas DE, Soares JA, Swearingen MC, Vross MA, Young GM, Ahmer BMM (2010) Salmonella enterica serovar Typhimurium can detect acyl homoserine lactone production by Yersinia enterocolitica in mice. J Bacteriol 192(1):29–37.  https://doi.org/10.1128/JB.01139-09 CrossRefPubMedGoogle Scholar
  16. European Food Safety Authority (2017) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016.  https://doi.org/10.2903/j.efsa.2017.5077
  17. Fàbrega A, Vila J (2013) Salmonella enterica serovar Typhimurium skills to succeed in the host: virulence and regulation. Clin Microbiol Rev 26(2):308–341.  https://doi.org/10.1128/CMR.00066-12 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Fan Q, Zhang Y, Yang H, Wu Q, Shi C, Zhang C, Xia X, Wang X (2018) Effect of coenzyme Q0 on biofilm formation and attachment-invasion efficiency of Listeria monocytogenes. Food Control 90:274–281.  https://doi.org/10.1016/j.foodcont.2018.02.047 CrossRefGoogle Scholar
  19. Fuentes DN, Calderon PF, Acuna LG, Rodas PI, Paredes-Sabja D, Fuentes JA, Gil F, Calderon IL (2015) Motility modulation by the small non-coding RNA SroC in Salmonella Typhimurium. FEMS Microbiol Lett 362(17):fnv135.  https://doi.org/10.1093/femsle/fnv135 CrossRefPubMedGoogle Scholar
  20. Gal-Mor O (2019) Persistent infection and long-term carriage of typhoidal and nontyphoidal Salmonellae. Clin Microbiol Rev 32:e00088–e00018.  https://doi.org/10.1128/CMR.00088-18 CrossRefPubMedGoogle Scholar
  21. Hautefort I, Thompson A, Eriksson-Ygberg S, Parker ML, Lucchini S, Danino V, Bongaerts RJM, Ahmad N, Rhen M, Hinton JCD (2008) During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems. Cell Microbiol 10(4):958–984.  https://doi.org/10.1111/j.1462-5822.2007.01099.x CrossRefPubMedPubMedCentralGoogle Scholar
  22. Horstmann JA, Zschieschang E, Truschel T, de Diego J, Lunelli M, Rohde M, May T, Strowig T, Stradal T, Kolbe M, Erhardt M (2017) Flagellin phase-dependent swimming on epithelial cell surfaces contributes to productive Salmonella gut colonisation. Cell Microbiol 19:e12739.  https://doi.org/10.1111/cmi.12739 CrossRefGoogle Scholar
  23. Jiang L, Feng L, Yang B, Zhang W, Wang P, Jiang X, Wang L (2017) Signal transduction pathway mediated by the novel regulator LoiA for low oxygen tension induced Salmonella Typhimurium invasion. PLoS Pathog 13(6):e1006429–e1006429.  https://doi.org/10.1371/journal.ppat.1006429 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kaur J, Jain SK (2012) Role of antigens and virulence factors of Salmonella enterica serovar Typhi in its pathogenesis. Microbiol Res 167(4):199–210.  https://doi.org/10.1016/j.micres.2011.08.001 CrossRefPubMedGoogle Scholar
  25. Lamas A, Regal P, Vazquez B, Miranda JM, Cepeda A, Franco CM (2018) Influence of milk, chicken residues and oxygen levels on biofilm formation on stainless steel, gene expression and small RNAs in Salmonella enterica. Food Control 90:1–9.  https://doi.org/10.1016/j.foodcont.2018.02.023 CrossRefGoogle Scholar
  26. LaRock DL, Chaudhary A, Miller SI (2015) Salmonellae interactions with host processes. Nat Rev Microbiol 13(4):191–205.  https://doi.org/10.1038/nrmicro3420 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Li GH, Yan CH, Xu YF, Feng YQ, Wu Q, Lv XY, Yang BW, Wang X, Xia XD (2014) Punicalagin inhibits Salmonella virulence factors and has anti-quorum-sensing potential. Appl Environ Microbiol 80(19):6204–6211.  https://doi.org/10.1128/AEM.01458-14 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Li BQ, Yue YY, Yuan ZL, Zhang FY, Li P, Song NN, Lin W, Liu Y, Yang YL, Li ZH, Gu LC (2017) Salmonella STM1697 coordinates flagella biogenesis and virulence by restricting flagellar master protein FlhD(4)C(2) from recruiting RNA polymerase. Nucleic Acids Res 45(17):9976–9989.  https://doi.org/10.1093/nar/gkx656 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Ma ZP, Song Y, Cai ZH, Lin ZJ, Lin GH, Wang Y, Zhou J (2018) Anti-quorum sensing activities of selected coral symbiotic bacterial extracts from the South China Sea. Front Cell Infect Microbiol 8:144.  https://doi.org/10.3389/fcimb.2018.00144 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Mathur R, Oh H, Zhang DK, Park SG, Seo J, Koblansky A, Hayden MS, Ghosh S (2012) A mouse model of Salmonella Typhi infection. Cell 151(3):590–602.  https://doi.org/10.1016/j.cell.2012.08.042 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Merino L, Procura F, Trejo FM, Bueno DJ, Golowczyc MA (2019) Biofilm formation by Salmonella sp. in the poultry industry: detection, control and eradication strategies. Food Res Int 119:530–540.  https://doi.org/10.1016/j.foodres.2017.11.024 CrossRefPubMedGoogle Scholar
  32. Ng WL, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222.  https://doi.org/10.1146/annurev-genet-102108-134304 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Pacello F, Ceci P, Ammendola S, Pasquali P, Chiancone E, Battistoni A (2008) Periplasmic Cu, Zn superoxide dismutase and cytoplasmic Dps concur in protecting Salmonella enterica serovar Typhimurium from extracellular reactive oxygen species. Biochim Biophys Acta 1780(2):226–232.  https://doi.org/10.1016/j.bbagen.2007.12.001 CrossRefPubMedGoogle Scholar
  34. Pati NB, Vishwakarma V, Jaiswal S, Periaswamy B, Hardt WD, Suar M (2013) Deletion of invH gene in Salmonella enterica serovar Typhimurium limits the secretion of Sip effector proteins. Microbes Infect 15(1):66–73.  https://doi.org/10.1016/j.micinf.2012.10.014 CrossRefPubMedGoogle Scholar
  35. Roche SM, Holbert S, Trotereau J, Schaeffer S, Georgeault S, Virlogeux-Payant I, Velge P (2018) Salmonella Typhimurium invalidated for the three currently known invasion factors keeps its ability to invade several cell models. Front Cell Infect Microbiol 8:273.  https://doi.org/10.3389/fcimb.2018.00273 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Ros-Chumillas M, Garre A, Mate J, Palop A, Periago PM (2017) Nanoemulsified D-limonene reduces the heat resistance of Salmonella Senftenberg over 50 times. Nanomaterials (Basel) 7(3).  https://doi.org/10.3390/nano7030065 CrossRefPubMedCentralGoogle Scholar
  37. Ryan D, Mukherjee M, Suar M (2017) The expanding targetome of small RNAs in Salmonella Typhimurium. Biochimie 137:69–77.  https://doi.org/10.1016/j.biochi.2017.03.005 CrossRefPubMedGoogle Scholar
  38. Ryan D, Mukherjee M, Nayak R, Dutta R, Suar M (2018) Biological and regulatory roles of acid-induced small RNA RyeC in Salmonella Typhimurium. Biochimie 150:48–56.  https://doi.org/10.1016/j.biochi.2018.05.001 CrossRefPubMedGoogle Scholar
  39. Salaheen S, Jaiswal E, Joo J, Peng M, Ho R, Oconnor D, Adlerz K, Aranda-Espinoza JH, Biswas D (2016) Bioactive extracts from berry byproducts on the pathogenicity of Salmonella Typhimurium. Int J Food Microbiol 237:128–135.  https://doi.org/10.1016/j.ijfoodmicro.2016.08.027 CrossRefPubMedGoogle Scholar
  40. Shi X, Zhu X (2009) Biofilm formation and food safety in food industries. Trends Food Sci Technol 20(9):407–413.  https://doi.org/10.1016/j.tifs.2009.01.054 CrossRefGoogle Scholar
  41. Shi C, Yan CH, Sui Y, Sun Y, Guo D, Chen YF, Jin T, Peng XL, Ma LL, Xia XD (2017) Thymoquinone inhibits virulence related traits of Cronobacter sakazakii ATCC 29544 and has anti-biofilm formation potential. Front Microbiol 8:2220.  https://doi.org/10.3389/fmicb.2017.02220 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Silva LN, Zimmer KR, Macedo AJ, Trentin DS (2016) Plant natural products targeting bacterial virulence factors. Chem Rev 116(16):9162–9236.  https://doi.org/10.1021/acs.chemrev.6b00184 CrossRefPubMedGoogle Scholar
  43. Srey S, Jahid IK, Ha SD (2013) Biofilm formation in food industries: a food safety concern. Food Control 31(2):572–585.  https://doi.org/10.1016/j.foodcont.2012.12.001 CrossRefGoogle Scholar
  44. Steenackers H, Hermans K, Vanderleyden J, De Keersmaecker SCJ (2012) Salmonella biofilms: an overview on occurrence, structure, regulation and eradication. Food Res Int 45(2):502–531.  https://doi.org/10.1016/j.foodres.2011.01.038 CrossRefGoogle Scholar
  45. Stepanović S, Cirković I, Ranin L, Svabić-Vlahović M (2004) Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Lett Appl Microbiol 38(5):428–432.  https://doi.org/10.1111/j.1472-765X.2004.01513.x CrossRefPubMedGoogle Scholar
  46. Thoendel M, Kavanaugh JS, Flack CE, Horswill AR (2011) Peptide signaling in the Staphylococci. Chem Rev 111(1):117–151.  https://doi.org/10.1021/cr100370n CrossRefPubMedGoogle Scholar
  47. Vinothkannan R, Tamizh MM, Raj CD, Princy SA (2018) Fructose furoic acid ester: an effective quorum sensing inhibitor against uropathogenic Escherichia coli. Bioorg Chem 79:310–318.  https://doi.org/10.1016/j.bioorg.2018.05.009 CrossRefPubMedGoogle Scholar
  48. Wu SC, Fu BD, Chu XL, Su JQ, Fu YX, Cui ZQ, Xu DX, Wu ZM (2016) Subinhibitory concentrations of phloretin repress the virulence of Salmonella Typhimurium and protect against Salmonella Typhimurium infection. Antonie Van Leeuwenhoek 109(11):1503–1512.  https://doi.org/10.1007/s10482-016-0752-z CrossRefGoogle Scholar
  49. Wu SC, Chu XL, Su JQ, Cui ZQ, Zhang LY, Yu ZJ, Wu ZM, Cai ML, Li HX, Zhang ZJ (2018) Baicalin protects mice against Salmonella Typhimurium infection via the modulation of both bacterial virulence and host response. Phytomedicine 48:21–31.  https://doi.org/10.1016/j.phymed.2018.04.063 CrossRefPubMedGoogle Scholar
  50. Yang HL, Korivi M, Lin MW, Chen SC, Chou CW, Hseu YC (2015) Anti-angiogenic properties of coenzyme Q0 through downregulation of MMP-9/NF-κB and upregulation of HO-1 signaling in TNF-α-activated human endothelial cells. Biochem Pharmacol 98(1):144–156.  https://doi.org/10.1016/j.bcp.2015.09.003 CrossRefPubMedGoogle Scholar
  51. Yang HL, Lin MW, Korivi M, Wu JJ, Liao CH, Chang CT, Liao JW, Hseu YC (2016) Coenzyme Q0 regulates NFκB/AP-1 activation and enhances Nrf2 stabilization in attenuation of LPS-induced inflammation and redox imbalance: evidence from in vitro and in vivo studies. Biochim Biophys Acta 1859(2):246–261.  https://doi.org/10.1016/j.bbagrm.2015.11.001 CrossRefPubMedGoogle Scholar
  52. Yang HL, Thiyagarajan V, Shen PC, Mathew DC, Lin KY, Liao JW, Hseu YC (2019) Anti-EMT properties of CoQ0 attributed to PI3K/AKT/NFKB/MMP-9 signaling pathway through ROS-mediated apoptosis. J Exp Clin Cancer Res 38(1):186.  https://doi.org/10.1186/s13046-019-1196-x CrossRefPubMedPubMedCentralGoogle Scholar
  53. Zeng H, Carlson AQ, Guo YW, Yu YM, Collier-Hyams LS, Madara JL, Gewirtz AT, Neish AS (2003) Flagellin is the major proinflammatory determinant of enteropathogenic Salmonella. J Immunol 171(7):3668–3674.  https://doi.org/10.4049/jimmunol.171.7.3668 CrossRefPubMedGoogle Scholar
  54. Zhao XC, Liu ZH, Li WL, Li X, Shi C, Meng RZ, Cheng W, Jin KQ, Yang ZQ, Shi XC, Guo N, Yu L (2014) In Vitro synergy of nisin and coenzyme Q0 against Staphylococcus aureus. Food Control 46:368–373.  https://doi.org/10.1016/j.foodcont.2014.05.051 CrossRefGoogle Scholar
  55. Zhao YY, Gorvel JP, Meresse S (2016) Effector proteins support the asymmetric apportioning of Salmonella during cytokinesis. Virulence 7(6):669–678.  https://doi.org/10.1080/21505594.2016.1173298 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Zhu MJ, Olsen SA, Sheng L, Xue Y, Yue W (2015) Antimicrobial efficacy of grape seed extract against Escherichia coli O157:H7 growth, motility and Shiga toxin production. Food Control 51:177–182.  https://doi.org/10.1016/j.foodcont.2014.11.024 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Yanpeng Yang
    • 1
  • Jiahui Li
    • 1
  • Yue Yin
    • 1
  • Du Guo
    • 1
  • Tong Jin
    • 1
  • Ning Guan
    • 1
  • Yiqi Shi
    • 1
  • Yunfeng Xu
    • 2
  • Sen Liang
    • 3
  • Xiaodong Xia
    • 1
  • Chao Shi
    • 1
    Email author
  1. 1.College of Food Science and EngineeringNorthwest A&F UniversityYanglingChina
  2. 2.College of Food and BioengineeringHenan University of Science and TechnologyLuoyangChina
  3. 3.Beijing Advanced Innovation Center for Food Nutrition and Human HealthBeijing Technology and Business UniversityBeijingChina

Personalised recommendations