Acta Scientific Microbiology (ASMI) (ISSN: 2581-3226)

Research Article Volume 3 Issue 3

Investigation of the Physiology and Architecture of Salmonella enteritidis Biofilms Under Alkaline Conditions

Aikaterina Papakonstantinou1 and Georgios Efthimiou2*

1Strathclyde Institute of Pharmacy and Biomedical Sciences, University of Strathclyde, 161 Cathedral Street,G4 0RE, Glasgow, United Kingdom
2Department of Biomedical Sciences, University of Hull, Cottingham Road, HU6 7RX, Hull, United Kingdom

*Corresponding Author:Georgios Efthimiou, Department of Biomedical Sciences, University of Hull, Cottingham Road, HU6 7RX, Hull, United Kingdom. E-mail: g.efthimiou@hull.ac.uk

Received: January 27, 2020; Published: February 08, 2020

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Abstract

  Formation of bacterial biοfilms is an important survival strategy in multiple adverse envirοnments. It is often affected by the nature of the attachment surface, the bacterial strain and the surrοunding physicochemical conditions. The effect of low pH on biofilm formation has been well studied, in contrast to the alkaline range. The aim οf this prοject was tο study the effect οf alkaline stress on the fοrmatiοn οf biοfilm by Salmοnella enteritidis and to examine the biofilm architecture patterns under different conditions, by use of confocal microscopy. The optimal pH for Salmonella biofilm formation was found to be pH 7.0, while pH 10.0 (adjusted by use of sodium hydroxide) reduces it significantly (p¬-value = 0.015). Planktonic cell growth was hindered due to the alkaline pH, yet the number of viable cells remained high. In addition, the effect on biofilm formation was stronger when the alkaline stimulus was applied during stationary phase (9 h after inoculation). When the pH was adjusted to 10 by use of a commercial alkaline detergent (sodium carbonate or washing soda) similar results were observed. Finally, the biofilm architecture at pH 7.0 was characterized by small cell clusters, whereas at pH 10.0 a slightly thinner layer of individual cells was observed. These findings indicate that although most cells survive the alkaline stress, their ability to form biofilm is impaired at alkaline pH, potentially leading to new disinfectant strategies involving alkaline reagents.

Keywords: Salmοnella enteritidis; Biοfilm; Alkaline; Architecture; Detergents

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References

  1. Gal-Mor O., et al. “Same species, different diseases: how and why typhoidal and non-typhoidal Salmonella enterica serovars differ”. Frontiers in Microbiology 5 (2014): 1-10. 
  2. Trevejo RT., et al. “Epidemiology of Salmonellosis in California, 1990 - 1999: Morbidity, Mortality, and Hospitalization Costs”. American Journal of Epidemiology 157 (2003): 48-57. 
  3. EFSA and ECDC. “The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016”. EFSA Journal 15 (2017): 1-227. 
  4. MacKenzie KD., et al. “Bistable Expression of CsgD in Salmonella enterica Serovar Typhimurium Connects Virulence to Persistence”. Infection and Immunity 83 (2015): 2312-2326. 
  5. Wang H., et al. “In situ characterization and analysis of Salmonella biofilm formation under meat processing environments using a combined microscopic and spectroscopic approach”. International Journal of Food Microbiology 167 (2013): 293-302. 
  6. Hall-Stoodley L., et al. “Bacterial biofilms: From the natural environment to infectious diseases”. Nature Reviews Microbiology 2 (2004): 95-108. 
  7. Yang Y., et al. “Biofilm formation of Salmonella Enteritidis under food-related environmental stress conditions and its subsequent resitance to chlorine treatment”. Food Microbiology 54 (2016): 98-105. 
  8. Davies DG and Geesey GG. “Regulation of the alginate biosynthesis gene algC in Pseudomonas aeruginosa during biofilm development in continuous culture”. Applied and Environmental Microbiology 61 (1995): 860-867. 
  9. Costerton JW., et al. “Bacterial Biofilms: A Common Cause of Persistent Infections”. Science 284 (1999):1318-1322. 
  10. Dimakopoulou-Papazoglou D., et al. “Modelling biofilm formation of Salmonella enterica ser. Newport as a function of pH and water activity”. Food Microbiology 53 (2016): 76-81. 
  11. Annous BA., et al. “Quorum Sensing in Biofilms: Why Bacteria Behave the Way They Do”. Journal of Food Science 74 (2009): R24-R37. 
  12. Zulfakar SS., et al. “Effect of pH, salt and chemical rinses on bacterial attachment to extracellular matrix proteins”. Food Microbiology 34 (2013): 369-375. 
  13. Cirkovic I., et al. “Influence of organic and inorganic acids on biofilm formation by Salmonella spp”. International Journal of Antimicrobial Agents 29 (2007): 610-611.
  14. Chaveerach P., et al. “In vitro study on the effect of organic acids on Campylobacter jejuni/coli populations in mixtures of water and feed”. Poultry Science 81 (2002): 621-628. 
  15. Borges A., et al. “The activity of ferulic and gallic acids in biofilm prevention and control of pathogenic bacteria”. Biofouling 28 (2012): 755-767. 
  16. Kang J., et al. “The specific effect of gallic acid on Escherichia coli biofilm formation by regulating pgaABCD genes expression”. Applied Microbiology and Biotechnology 102 (2018): 1837-1846. 
  17. Singla R., et al. “Novel synergistic approach to exploit the bactericidal efficacy of commercial disinfectants on the biofilms of Salmonella enterica serovar Typhimurium”. Journal of Bioscience and Bioengineering 118 (2014): 34-40. 
  18. Joseph B., et al. “Biofilm formation by Salmonella spp. on food contact surfaces and their sensitivity to sanitizers”. International Journal of Food Microbiology 64 (2001): 367-372. 
  19. Scher K., et al. “Effect of Heat, Acidification, and Chlorination on Salmonella enterica Serovar Typhimurium Cells in a Biofilm Formed at the Air-Liquid Interface”. Applied and Environmental Microbiology 71 (2005): 1163-1168. 
  20. Lieleg O., et al. “Mechanical robustness of Pseudomonas aeruginosa biofilms”. Soft Matter 7 (2011): 3307-3314. 
  21. Ueda S and Kuwabara Y. “Susceptibility of Biofilm Escherichia coli, Salmonella Enteritidis and Staphylococcus aureus to Detergents and Sanitizers”. Biocontrol Science 12 (2007): 149-153. 
  22. Nostro A., et al. “Effect of alkaline pH on staphylococcal biofilm formation”. Acta Pathologica et Microbiologica Scandinavica 120 (2012): 733-742. 
  23. Speranza B., et al. “Approaches to Removal and Killing of Salmonella Spp. Biofilms”. Journal of Food Processing and Preservation 41 (2017): 1-9. 
  24. Lewis K. “Riddle of Biofilm Resistance”. Antimicrob Agents Chemother 45 (2001): 999-1007. 
  25. Bridier A., et al. “The biofilm architecture of sixty opportunistic pathogens deciphered using a high throughput CLSM method”. Journal of Microbiological Methods 82 (2010): 64-70. 
  26. Stewart PS. “Diffusion in Biofilms”. Journal of Bacteriology 185 (2003): 1485-1491. 
  27. Caricate-Nero A and Bergantin LB. “Importance of fluorescence microscopy in the study of the dysfunctions of intracellular Ca2+ homeostasis invovled in pathogenesis of cardiovascular diseases”. Nuclear Medicine and Molecular Imaging 2 (2017): 1-7. 
  28. Plank M., et al. “Millisecond timescale slimfield imaging and automated quantification of single fluorescent protein molecules for use in probing complex biological processes”. Integrative Biology 1 (2009): 602-612. 
  29. Dige I., et al. “In situ identification of streptococci and other bacteria in initial dental biofilm by confocal laser scanning microscopy and fluorescence in situ hybridization”. European Journal of Oral Sciences 115 (2007): 459-467. 
  30. Quintas V., et al. “Analyzing the oral biofilm using fluorescence-based microscopy: what’s in a dye? Microscopy: Advances in scientific research and education”. Formatex Research Center, Editors: A. Méndez-Vilas (2014): 226-238. 
  31. Yang Y., et al. “Membrane lipid composition and stress/virulence related gene expression of Salmonella Enteritidis cells adapted to lactic acid and trisodium phosphate and their resistance to lethal heat and acid stress”. International Journal of Food Microbiology 191 (2014): 24-31. 
  32. Speranza B., et al. “Effects of nutritional and environmental conditions on Salmonella sp. biofilm formation”. Journal of Food Science 76 (2011): 12-16. 
  33. Karaca B., et al. “Biofilm-producing abilities of Salmonella strains isolated from Turkey”. Biologia 68 (2013): 1-10. 
  34. Lianou A and Koutsoumanis KP. “Strain variability of the biofilm-forming ability of Salmonella enterica under various environmental conditions”. International Journal of Food Microbiology 160 (2012): 171-178.
  35. Wang Η., et al. “Response of long-term acid stress to biofilm formation of meat-related Salmonella Enteritidis”. Food Control 69 (2016): 214-220. 
  36. Singh R., et al. “Biofilms: implications in bioremediation”. Trends in Microbiology 14 (2006): 389-397. 
  37. Jarvis GN., et al. “The mechanism of carbonate killing of Escherichia coli”. Letters in Applied Microbiology 33 (2001): 196-200. 
  38. Zhang L., et al. “Lighting up the interactions between bacteria and surfactants with aggregation-induced emission characteristics”. Materials Chemistry Frontiers 1 (2017): 1829-1835. 
  39. Sapers GM. “Disinfection of contaminated produce with conventional washing and sanitizing technology”. Chapter in: The Produce Contamination Problem. Second Edition. Academic Press, Elsevier, The Netherlands (2009).
  40. Castelijn GA., et al. “Diversity in biofilm formation and production of curli fimbriae and cellulose of Salmonella Typhimurium strains of different origin in high and low nutrient medium”. Biofouling 28 (2012): 51-63. 
  41. White AP., et al. “Aggregation via the red, dry, and rough morphotype is not a virulence adaptation in Salmonella enterica serovar typhimurium”. Infection and Immunity 76 (2008):1048-1058. 
  42. Neu T., et al. “Assessment of lectin- binding analysis for in situ detection of glycoconjugates in biofilm systems”. Microbiology 147 (2001): 299-313. 
  43. Pantanella F., et al. “BioTimer Assay, a new method for counting Staphylococcus spp. in biofilm without sample manipulation applied to evaluate antibiotic susceptibility of biofilm”. Journal of Microbiological Methods 75 (2008): 478-484. 
  44. Murga R., et al. “Quantitative analysis of biofilm thickness variability”. Biotechnology and Bioengineering 45 (1995): 503-510. 
  45. Torresi E., et al. “Biofilm thickness influences biodiversity in nitrifying MBBRs - Implications on micropollutant removal”. Environmental Science and Technology 50 (2016): 9279-9288. 
  46. Hu M., et al. “Determination of porosity and thickness of biofilm attached on irregular-shaped media”. Journal of Environmental Engineering 139 (2013): 923-931. 
  47. Ryu J and Beuchat LR. “Biofilm formation by Escherichia coli O157: H7 on stainless steel: Effect of exopolysaccharide and curli production on its resistance to chlorine”. Applied and Environmental Microbiology 71 (2005): 247-254. 
  48. Díez-García M., et al. “Influence of serotype on the growth kinetics and the ability to form biofilms of Salmonella isolates from poultry”. Food Microbiology 31 (2012): 173-180. 
  49. Van Houdt R and Michiels CW. “Biofilm formation and the food industry, a focus on the bacterial outer surface”. Journal of Applied Microbiology 109 (2010): 1117-1131.
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Citation

Citation: Aikaterina Papakonstantinou and Georgios Efthimiou. “Investigation of the Physiology and Architecture of Salmonella enteritidis Biofilms Under Alkaline Conditions". Acta Scientific Microbiology 3.3 (2020): 01-11.




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