Ultrasound promoted the inactivation efficacy of lactic acid against calcium-mediated biofilm formation by Pseudomonas fluorescens
Hongchao Dai
School of Food Science and Engineering, Yangzhou University, Yangzhou, 225127 China
Contribution: Investigation, Validation, Methodology, Writing - original draft
Search for more papers by this authorYanhe Zhang
School of Food Science and Engineering, Yangzhou University, Yangzhou, 225127 China
Contribution: Investigation, Validation, Methodology
Search for more papers by this authorZhenbo Xu
School of Food Science and Engineering, Guangdong Province Key Laboratory for Green Processing of Natural Products and Product Safety, Engineering Research Center of Starch and Vegetable Protein Processing Ministry of Education, South China University of Technology, Guangzhou, 510640 China
Department of Biology, Massachusetts Institute of Technology, Cambridge, 02139 MA, USA
Home Economics Technology, Rajamangala University of Technology Phra Nakhon, Bangkok, 10300 Thailand
Contribution: Methodology, Data curation
Search for more papers by this authorThanapop Stoteyome
Home Economics Technology, Rajamangala University of Technology Phra Nakhon, Bangkok, 10300 Thailand
Contribution: Data curation, Writing - review & editing
Search for more papers by this authorCorresponding Author
Lei Yuan
School of Food Science and Engineering, Yangzhou University, Yangzhou, 225127 China
Author for correspondence. E-mail: [email protected]
Contribution: Funding acquisition, Writing - review & editing, Methodology
Search for more papers by this authorHongchao Dai
School of Food Science and Engineering, Yangzhou University, Yangzhou, 225127 China
Contribution: Investigation, Validation, Methodology, Writing - original draft
Search for more papers by this authorYanhe Zhang
School of Food Science and Engineering, Yangzhou University, Yangzhou, 225127 China
Contribution: Investigation, Validation, Methodology
Search for more papers by this authorZhenbo Xu
School of Food Science and Engineering, Guangdong Province Key Laboratory for Green Processing of Natural Products and Product Safety, Engineering Research Center of Starch and Vegetable Protein Processing Ministry of Education, South China University of Technology, Guangzhou, 510640 China
Department of Biology, Massachusetts Institute of Technology, Cambridge, 02139 MA, USA
Home Economics Technology, Rajamangala University of Technology Phra Nakhon, Bangkok, 10300 Thailand
Contribution: Methodology, Data curation
Search for more papers by this authorThanapop Stoteyome
Home Economics Technology, Rajamangala University of Technology Phra Nakhon, Bangkok, 10300 Thailand
Contribution: Data curation, Writing - review & editing
Search for more papers by this authorCorresponding Author
Lei Yuan
School of Food Science and Engineering, Yangzhou University, Yangzhou, 225127 China
Author for correspondence. E-mail: [email protected]
Contribution: Funding acquisition, Writing - review & editing, Methodology
Search for more papers by this authorAbstract
This study investigated the synergistic effects of lactic acid (0.5%, 1% and 2%) and ultrasound (400 W, 20 kHz) on the inactivation of Pseudomonas fluorescens. Combined ultrasound and 2% lactic acid for 5 min reduced the planktonic cell count below 1.40 log cfu/mL. Ultrasound promoted the inactivation of P. fluorescens biofilms by lactic acid and increased the release of ATP and nucleic acids from bacterial cells by 0.09–0.22 μmol/OD and 0.043–0.113 of OD260 values, respectively. Results indicated that combined ultrasound and lactic acid can serve as a potential technique to control P. fluorescens biofilms.
CONFLICT OF INTEREST
The authors have no conflict of interest.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
REFERENCES
- Aaliya B, Sunooj K V, Navaf M, Parambil Akhila P, Sudheesh C, Ahmad Mir S, Sabu S, Sasidharan A, Theingi Hlaing M and George J (2021) Recent trends in bacterial decontamination of food products by hurdle technology: A synergistic approach using thermal and non-thermal processing techniques. Food Research International 147 110514.
- Azi F, Li Z, Xu P and Dong M (2022) Transcriptomic analysis reveals the antibacterial mechanism of phenolic compounds from kefir fermented soy whey against Escherichia coli O157:H7 and Listeria monocytogenes. International Journal of Food Microbiology 383 109953.
- Bevilacqua A, Sinigaglia M, Petruzzi L, Speranza B, Campaniello D, Racioppo A, Altieri C and Corbo M R (2023) Effect of weak acids, combined with pH and temperature, on the growth or inactivation of Alicyclobacillus acidoterrestris. Food Bioscience 56 103146.
- Chen L, Liu Q, Zhao X, Zhang H, Pang X and Yang H (2022) Inactivation efficacies of lactic acid and mild heat treatments against Escherichia coli strains in organic broccoli sprouts. Food Control 133 108577.
- Concha-Meyer A, Eifert J D, Williams R C, Marcy J E and Welbaum G E (2017) Listeria monocytogenes survival in the presence of malic acid, lactic acid or blueberry extract. Journal of Berry Research 7 33–41.
- Dong Y, Su H, Jiang H, Zheng H, du Y, Wu J and Li D (2017) Experimental study on the influence of low-frequency and low-intensity ultrasound on the permeability of the Mycobacterium smegmatis cytoderm and potentiation with levofloxacin. Ultrasonics Sonochemistry 37 1–8.
- Du B, Meng L, Liu H, Zheng N, Zhang Y, Zhao S, Li M and Wang J (2022) Diversity and proteolytic activity of Pseudomonas species isolated from raw cow milk samples across China. Science of the Total Environment 838 156382.
- Fan L, Dai H, Zhou W, Yuan L, Yang J, Yang Z and Jiao X A (2024) Unraveling the significance of calcium as a biofilm promotion signal for Bacillus licheniformis strains isolated from dairy products. Food Research International 182 114145.
- Ferrante S, Guerrero S and Alzamora S M (2007) Combined use of ultrasound and natural antimicrobials to inactivate Listeria monocytogenes in orange juice. Journal of Food Protection 70 1850–1856.
- Gopalakrishnan S, Gupta A, Makabenta J M V, Park J, Amante J J, Chattopadhyay A N, Matuwana D, Kearney C J and Rotello V M (2022) Ultrasound-enhanced antibacterial activity of polymeric nanoparticles for eradicating bacterial biofilms. Advanced Healthcare Materials 11 2201060.
- In Y W, Kim J J, Kim H J and Oh S-W (2013) Antimicrobial activities of acetic acid, citric acid and lactic acid against Shigella species. Journal of Food Safety 33 79–85.
- Ji Q, Wang W, Yan H, Qu H, Liu Y, Qian Y and Gu R (2023) The effect of different organic acids and their combination on the cell barrier and biofilm of Escherichia coli. Food 12 103676.
- Li L, Mu T and Zhang M (2021) Contribution of ultrasound and slightly acid electrolytic water combination on inactivating Rhizopus stolonifer in sweet potato. Ultrasonics Sonochemistry 73 105528.
- Li H, Zhang Y, Yuan X, Liu S, Fan L, Zheng X, Wang S, Yuan L and Jiao X (2023) Microbial biodiversity of raw milk collected from Yangzhou and the heterogeneous biofilm-forming ability of Pseudomonas. International Journal of Dairy Technology 76 51–62.
- Machado S G, da Silva F L, Bazzolli D M S, Heyndrickx M, Costa P M A and Vanetti M C D (2015) Pseudomonas spp. and Serratia liquefaciens as predominant spoilers in cold raw milk. Journal of Food Science 80 1842–1849.
- Mullan W M A (2017a) Calculator for determining the concentration of undissociated lactic acid in cheese and whether the cheese will support the growth of Listeria monocytogenes. [Internet document] URL https://www.dairyscience.info/newcalculators/la.asp. Accessed 12/05/2024.
- Mullan W M A (2017b) Functions of starters in dairy fermentations. The importance and effectiveness of their antimicrobial mechanisms. [Internet document] URL https://www.dairyscience.info/cheese-starters/225-role-of-starters.html. Accessed: 12/05/2024. Based on a technical article authored in 2005. Updated September 2018; February 2022.
- Ning Y, Fu Y, Hou L, Ma M, Wang Z, Li X and Jia Y (2021) iTRAQ-based quantitative proteomic analysis of synergistic antibacterial mechanism of phenyllactic acid and lactic acid against Bacillus cereus. Food Research International 139 109562.
- Pang X, Zhang H, Seck H L and Zhou W (2022) Inactivation effect of low-energy X-ray irradiation against planktonic and biofilm Pseudomonas fluorescens and its antibacterial mechanism. International Journal of Food Microbiology 374 109716.
- Park J S and Ha J W (2019) Ultrasound treatment combined with fumaric acid for inactivating food-borne pathogens in apple juice and its mechanisms. Food Microbiology 84 103277.
- Presser K A, Ratkowsky D A and Ross T (1997) Modelling the growth rate of Escherichia coli as a function of pH and lactic acid concentration. Applied and Environmental Microbiology 63 2355–2360.
- Presser K A, Ross T and Ratkowsky D A (1998) Modelling the growth limits (growth/no growth interface) of E. coli as a function of pH, lactic acid and temperature. Applied and Environmental Microbiology 64 1773–1779.
- Qin X, Cheng J, Qi X, Guan N, Chen Q, Pei X, Jiang Y, Yang X and Man C (2023) Effect of thermostable enzymes produced by psychrotrophic bacteria in raw milk on the quality of ultra-high temperature sterilized milk. Food 12 3752.
- Rediske A M, Hymas W C, Wilkinson R and Pitt W G (1998) Ultrasonic enhancement of antibiotic action on several species of bacteria. Journal of General and Applied Microbiology 44 283–288.
- Shao L, Dong Y, Chen X, Xu X and Wang H (2020) Modeling the elimination of mature biofilms formed by Staphylococcus aureus and Salmonella spp. using combined ultrasound and disinfectants. Ultrasonics Sonochemistry 69 105269.
- Shen Q, Sun J, Pan J, Zheng X, Zhong J-J and Zhou W-W (2024) Ultrasound-synergized gas in ensuring the sterilization and physicochemical quality of fruit and vegetables: A review. Postharvest Biology and Technology 209 112705.
- Shi Y, Pu D, Zhou X and Zhang Y (2022) Recent progress in the study of taste characteristics and the nutrition and health properties of organic acids in foods. Foods 11 3408.
- Shu Q, Lou H, Wei T, Zhang X and Chen Q (2021) Synergistic antibacterial and antibiofilm effects of ultrasound and MEL-A against methicillin-resistant Staphylococcus aureus. Ultrasonics Sonochemistry 72 105452.
- Sun J, Wang D, Sun Z, Liu F, du L and Wang D (2021) The combination of ultrasound and chlorogenic acid to inactivate Staphylococcus aureus under planktonic, biofilm, and food systems. Ultrasonics Sonochemistry 80 105801.
- Sun J, Sun Z, Wang D, Liu F and Wang D (2022) Contribution of ultrasound in combination with chlorogenic acid against Salmonella enteritidis under biofilm and planktonic condition. Microbial Pathogenesis 165 105489.
- Teh K H, Flint S, Palmer J, Andrewes P, Bremer P and Lindsay D (2012) Proteolysis produced within biofilms of bacterial isolates from raw milk tankers. International Journal of Food Microbiology 157 28–34.
- Torlak E and Sert D (2013) Combined effect of benzalkonium chloride and ultrasound against listeria monocytogenes biofilm on plastic surface. Letters in Applied Microbiology 57 220–226.
- Tsukatani T and Sakata F (2022) Combined effects of fumaric, lactic, and ferulic acid against food-borne pathogenic biofilms. Food Control 138 109024.
- Unal Turhan E, Polat S, Erginkaya Z and Konuray G (2022) Investigation of synergistic antibacterial effect of organic acids and ultrasound against pathogen biofilms on lettuce. Food Bioscience 47 101643.
- Wang C, Chang T, Yang H and Cui M (2014) Surface physiological changes induced by lactic acid on pathogens in consideration of pKa and pH. Food Control 46 525–531.
- Wang N, Jin Y, He G and Yuan L (2021) Development of multi-species biofilm formed by thermophilic bacteria on stainless steel immerged in skimmed milk. Food Research International 150 110754.
- Yang H, Zhan X, Song L, Cheng S, Su R, Zhang Y, Guo D, Lü X, Xia X and Shi C (2023) Synergistic antibacterial and anti-biofilm mechanisms of ultrasound combined with citral nanoemulsion against Staphylococcus aureus 29213. International Journal of Food Microbiology 391-393 110150.
- Yu H, Chen S and Cao P (2012) Synergistic bactericidal effects and mechanisms of low intensity ultrasound and antibiotics against bacteria: A review. Ultrasonics Sonochemistry 19 377–382.
- Yu H, Liu Y, Yang F, Xie Y, Guo Y, Cheng Y and Yao W (2021) Combined an acoustic pressure simulation of ultrasonic radiation and experimental studies to evaluate control efficacy of high-intensity ultrasound against Staphylococcus aureus biofilm. Ultrasonics Sonochemistry 79 105764.
- Yuan L, Sadiq F A, Burmolle M, Liu T and He G (2018) Insights into bacterial milk spoilage with particular emphasis on the roles of heat-stable enzymes, biofilms, and quorum sensing. Journal of Food Protection 81 1651–1660.
- Yuan L, Sadiq F A, Wang N, Yang Z and He G (2021) Recent advances in understanding the control of disinfectant-resistant biofilms by hurdle technology in the food industry. Critical Reviews in Food Science and Nutrition 61 3876–3891.
- Yuan L, Fan L, Dai H, He G, Zheng X, Rao S, Yang Z and Jiao X A (2023) Multi-omics reveals the increased biofilm formation of Salmonella Typhimurium M3 by the induction of tetracycline at sub-inhibitory concentrations. Science of the Total Environment 899 165695.
- Yuan L, Zhang Y, Mi Z, Zheng X, Wang S, Li H and Yang Z (2024) Calcium-mediated modulation of Pseudomonas fluorescens biofilm formation. Journal of Dairy Science 107 1950–1966.
- Zarei M, Rahimi S, Saris P E J and Yousefvand A (2022) Pseudomonas fluorescens group bacterial strains interact differently with pathogens during dual-species biofilm formation on stainless steel surfaces in milk. Frontiers in Microbiology 13 104787.
- Zhang H, Wang S, Goon K, Gilbert A, Nguyen Huu C, Walsh M, Nitin N, Wrenn S and Tikekar R V (2020) Inactivation of foodborne pathogens based on synergistic effects of ultrasound and natural compounds during fresh produce washing. Ultrasonics Sonochemistry 64 104983.
- Zhang J, Wang D, Sun J, Sun Z, Liu F, du L and Wang D (2021) Synergistic antibiofilm effects of ultrasound and phenyllactic acid against Staphylococcus aureus and Salmonella enteritidis. Food 10 2171.
- Zou M and Liu D (2018) A systematic characterization of the distribution, biofilm-forming potential and the resistance of the biofilms to the CIP processes of the bacteria in a milk powder processing factory. Food Research International 113 316–326.