Abstract
This study focused on the microencapsulation of enterocin from Enterococcus durans (E. durans MF5) in whey powder (WP) using a spray-drying technique followed by the evaluation of how complexation can preserve the enterocin structure and antimicrobial activity against food-borne pathogens. Crude enterocin samples (1 and 5%) were microencapsulated in 10% WP. The antimicrobial activity of unencapsulated (crude) enterocin and microencapsulated enterocin was tested against the target bacteria Salmonella Typhimurium, Escherichia coli, Listeria monocytogenes, Listeria innocua, and Listeria ivanovi. The microencapsulation yields were 31.66% and 34.16% for concentrations of 1 and 5% enterocin, respectively. There was no significant difference between these concentrations. Microencapsulated enterocin was efficient for up to 12 h of cocultivation with Listeria sp., and the concentration required to inhibit the growth of target bacteria presented values of 6400 AU/mL (arbitrary unit). Microencapsulated enterocin demonstrated enhanced efficacy against Listeria species and E. coli when compared with crude enterocin (p < 0.05). Fourier transform-infrared spectroscopy and differential scanning calorimetry results confirmed the presence of enterocin in the microparticles. Scanning electron microscopy showed cell damage of the target bacteria. The results showed that complexation with WP preserved enterocin antimicrobial activity during spray-drying, indicating its potential use as a food preservative.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
None.
Code availability
All content presented in this article is approved by the authors.
Abbreviations
- AMPs:
-
Antimicrobial peptides
- WP:
-
Whey protein
- AU:
-
Arbitrary units
- SEM:
-
Scanning electron microscopy
- E10:
-
Concentrations of 1 wt%
- E50:
-
Concentrations of 5 wt
References
Abdel-Hamid MS, Anis A, Elbawab RH, Mohammed AAB, Orabi SH, Fathalla SI (2018) Distinctive antagonistic role of new Enterococcus faecium ER-3M strain and its bacteriocin effect against Staphylococcus aureus pneumonia. Rend Fis Acc Lincei 29:675–690. https://doi.org/10.1007/s12210-018-0722-7
Abid Y, Gharsallaoui A, Dumas E, Ghnimi S, Attia H, Azabou S (2019) Spray-drying microencapsulation of nisin by complexation with exopolysaccharides produced by probiotic Bacillus tequilensis-GM and Leuconostoc citreum-BMS. Colloids Surf B 181:25–30. https://doi.org/10.1016/j.colsurfb.2019.05.022
Acuña L, Corbalan NS, Fernandez-No IC, Morero RD, Barros-Velazquez J, Bellomio A (2015) Inhibitory effect of the hybrid bacteriocin Ent35-MccV on the growth of Escherichia coli and Listeria monocytogenes in model and food systems. Food Bioprocess Technol 8:1063–1075. https://doi.org/10.1007/s11947-015-1469-0
Aghbashlo M, Mobli H, Madadlou A, Rafiee S (2013) Influence of wall material and inlet drying air temperature on the microencapsulation of fish oil by spray drying. Food Bioprocess Technol 6:1561–1569. https://doi.org/10.1007/s11947-012-0796-7
Ben Amar C, Kim L, Oulahal N, Degraeve P, Gharsallaoui A (2017) Using complexation for the microencapsulation of nisin in biopolymer matrices by spray-drying. Food Chem 236:32–40. https://doi.org/10.1016/j.foodchem.2017.04.168
Beye M, Gouriet F, Michelle C, Casalta JP, Habib G, Raoult D, Fournier P-E (2016) Genome analysis of Listeria ivanovii strain G770 that caused a deadly aortic prosthesis infection. New Microbes New Infect 10:87–92. https://doi.org/10.1016/j.nmni.2016.01.005
Calo-Mata P, Arlindo S, Boehme K, de Miguel T, Pascoal A, Barros-Velazquez J (2008) Current applications and future trends of lactic acid bacteria and their bacteriocins for the biopreservation of aquatic food products. Food Bioprocess Technol 1:43–63. https://doi.org/10.1007/s11947-007-0021-2
Chandralekha A, Tavanandi AH, Amrutha N, Hebbar HU, Raghavarao KSMS, Gadre R (2016) Encapsulation of yeast (Saccharomyces cereviciae) by spray drying for extension of shelf life. Dry Technol 34:1307–1318. https://doi.org/10.1080/07373937.2015.1112808
Chew YL, Mahadi AM, Wong KM, Goh JK (2018) Anti-methicillin-resistance Staphylococcus aureus (MRSA) compounds from Bauhinia kockiana Korth. And their mechanism of antibacterial activity. BMC Complement Altern Med 18:70. https://doi.org/10.1186/s12906-018-2137-5
Condurache NN, Aprodu I, Crăciunescu O, Talia R, Horincar G, Barbu V, Enachi E, Rapeanu G, Bahrim G, Oancea A, Stanciuc N (2019) Probing the functionality of bioactives from eggplant peel extracts through extraction and microencapsulation in different polymers and whey protein hydrolysates. Food Bioprocess Technol 12:1316–1329. https://doi.org/10.1007/s11947-019-02302-1
den Bakker HC, Cummings CA, Ferreira V, Vatta P, Orsi RH, Degoricija L, Barker M, Petrauskene O, Furtado MR, Wiedmann M (2010) Comparative genomics of the bacterial genus Listeria: genome evolution is characterized by limited gene acquisition and limited gene loss. BMC Genom 11:688. https://doi.org/10.1186/1471-2164-11-688
Furlaneto-Maia L, Ramalho R, Rocha KR, Furlaneto MC (2020) Antimicrobial activity of enterocins against Listeria sp. and other food spoilage bacteria. Biotechnol Lett. https://doi.org/10.1007/s10529-020-02810-7
García-Toledo JA, Torrestiana-Sánchez B, Martínez-Sánchez CE, Tejero-Andrade JM, Garcia-Bórguez A, Mendoza-Garcia PG (2019) Nanoencapsulation of a bacteriocin from Pediococcus acidilactici ITV26 by microfluidization. Food Bioprocess Technol 12:88–97. https://doi.org/10.1007/s11947-018-2184-4
Gharanjig H, Gharanjig K, Hosseinnezhad M, Jafari SM (2020) Differential scanning calorimetry (DSC) of nanoencapsulated food ingredients. Nanoencapsul Food Ind 4:295–346. https://doi.org/10.1016/B978-0-12-815667-4.00010-9
Ibach A, Kind M (2007) Crystallization kinetics of amorphous lactose, whey-permeate and whey powders. Carbohydr Res 342:1357–1365. https://doi.org/10.1016/J.CARRES.2007.03.002
Jaouani I, Abbassi M, Alessandria V, Bouraoui J, Ben Salem R, Kilani H, Mansouri R, Messadi L, Cocolin L (2014) High inhibition of Paenibacillus larvae and Listeria monocytogenes by Enterococcus isolated from different sources in Tunisia and identification of their bacteriocin genes. Lett Appl Microbiol 59:17–25. https://doi.org/10.1111/lam.12239
Jordan K, McAuliffe O (2018) Listeria monocytogenes in foods. Adv Food Nutr Res 86:181–213. https://doi.org/10.1016/bs.afnr.2018.02.006
Karrar E, Mahdi AA, Sheth S, Ahmed IAM, Manzoor MF, Wei W, Wang X (2021) Effect of maltodextrin combination with gum arabic and whey protein isolate on the microencapsulation of gurum seed oil using a spray-drying method. Int J Biol Macromol 171:208–216. https://doi.org/10.1016/j.ijbiomac.2020.12.045
Korma SA, Wei W, Ali AH, Abed SM, Zheng L, Jin Q, Wang X (2019) Spray-dried novel structured lipids enriched with medium-and long-chain triacylglycerols encapsulated with different wall materials: characterization and stability. Food Res Int 116:538–547. https://doi.org/10.1016/j.foodres.2018.08.071
Kumariya R, Garsa AK, Rajput YS, Sood SK, Akhtar N, Patel S (2019) Bacteriocins: classification, synthesis, mechanism of action and resistance development in food spoilage causing bacteria. Microb Pathog 128:171–177. https://doi.org/10.1016/j.micpath.2019.01.002
Lee G (2002) Spray-drying of proteins. In: Carpenter JF, Manning MC (eds) Rational design of stable protein formulations: theory and practice. Springer, Boston, pp 135–158
Lü X, Hu P, Dang Y, Liu B (2014) Purification and partial characterization of a novel bacteriocin produced by Lactobacillus casei TN-2 isolated from fermented camel milk (Shubat) of Xinjiang Uygur Autonomous region, China. Food Control 43:276–283. https://doi.org/10.1016/j.foodcont.2014.03.020
Luque-Sastre L, Arroyo C, Fox EM, McMahon BJ, Bai L, Li F, Fanning S (2018) Antimicrobial resistance in Listeria species. Microbiol Spectr. https://doi.org/10.1128/microbiolspec.ARBA-0031-2017
Masias E, Dupuy FG, Sanches PRS, Farizano JV, Cilli E, Bellomio A, Saavedra L, Minahk C (2017) Impairment of the class IIa bacteriocin receptor function and membrane structural changes are associated to enterocin CRL35 high resistance in Listeria monocytogenes. Biochim Et Biophys Acta (BBA) 1861:1770–1776. https://doi.org/10.1016/j.bbagen.2017.03.014
Morisset D, Berjeaud JM, Marion D, Lacombe C, Frère J (2004) Mutational analysis of mesentericin Y105, an anti-listeria bacteriocin, for determination of impact on bactericidal activity, in vitro secondary structure, and membrane interaction. Appl Environ Microbiol 70:4672–4680. https://doi.org/10.1128/AEM.70.8.4672-4680.2004
Moura A, Disson O, Lavina M, Thouvenot P, Huang L, Leclerq A, Fredriksson-Ahomaa M, Eshwar AK, Stephan R, Lecuit M (2019) Atypical haemolytic Listeria innocua isolates are virulent, albeit less than Listeria monocytogenes. Infect Immun 87(4):e00758-e818. https://doi.org/10.1128/IAI.00758-18
Nambiar RB, Sellamuthu PS, Perumal AB (2017) Microencapsulation of tender coconut water by spray drying: effect of moringa oleifera gum, maltodextrin concentrations, and inlet temperature on powder qualities. Food Bioprocess Technol 10:1668–1684. https://doi.org/10.1007/s11947-017-1934-z
Pui LP, Karim R, Yusof YA, Wong CW, Ghazali HM (2020) Optimization of spray-drying parameters for the production of ‘Cempedak’ (Artocarpus integer) fruit powder. J Food Meas Charact 14:3238–3249. https://doi.org/10.1007/s11694-020-00565-3
Puttarat N, Thangrongthong S, Kasemwong K, Kerdsup P, Taweechotipatr M (2021) Spray-drying microencapsulation using whey protein isolate and nano-crystalline starch for enhancing the survivability and stability of Lactobacillus reuteri TF-7. Food Sci Biotechnol 30:245–256. https://doi.org/10.1007/s10068-020-00870-z
Qiao X, Du R, Wang Y, Han Y, Zhou Z (2020) Purification, characterization 36 and mode of action of enterocin, a novel bacteriocin produced by Enterococcus faecium TJUQ1. Int J Biol Macromol 144:151–159. https://doi.org/10.1016/j.ijbiomac.2019.12.090
Ramos FM, Silveira Júnior V, Prata AS (2019) Assessing the vacuum spray drying effects on the properties of orange essential oil microparticles. Food Bioprocess Technol 12:1917–1927. https://doi.org/10.1007/s11947-019-02355-2
Rocha KR, Perini HF, de Souza CM, Schueler J, Tosoni NF, Furlaneto MC, Furlaneto-Maia L (2019) Inhibitory effect of bacteriocins from enterococci on developing and preformed biofilms of Listeria monocytogenes, Listeria ivanovii and Listeria innocua. World J Microbiol Biotechnol 35:96–107. https://doi.org/10.1007/s11274-019-2675-0
Rosolen MD, Bordini FW, Oliveira PD, Conceição FR, Pohndorf RS, Fiorentini AM, Silva WP, Pieniz S (2019) Symbiotic microencapsulation of Lactococcus lactis subsp. lactis R7 using whey and inulin by spray drying. LWT 115:108411. https://doi.org/10.1016/j.lwt.2019.108411
Sheoran P, Tiwari SK (2019) Enterocin LD3 from Enterococcus hirae LD3 causing efflux of intracellular ions and UV-absorbing materials in Gram-negative bacteria. J Appl Microbiol 126:1059–1069. https://doi.org/10.1111/jam.14203
Sidhu PK, Nehra K (2020) Bacteriocin-capped silver nanoparticles for enhanced antimicrobial efficacy against food pathogen. IET Nanobiotechnol 14:245–252. https://doi.org/10.1049/iet-nbt.2019.0323
Smith MK, Draper LA, Hazelhoff PJ, Cotter PD, Ross RP, Hill C (2016) A bioengineered nisin derivative, M21A, in combination with food grade additives eradicates biofilms of Listeria monocytogenes. Front Microbiol 7:1939. https://doi.org/10.3389/fmicb.2016.01939
Tavares L, Barros HLB, Vaghetti JCP, Norena C (2019) Microencapsulation of garlic extract by complex coacervation using whey protein isolate/chitosan and gum arabic/chitosan as wall materials: influence of anionic biopolymers on the physicochemical and structural properties of microparticles. Food Bioprocess Technol 12:2093–2106. https://doi.org/10.1007/s11947-019-02375-y
Tosoni NF, Perini HF, Terra MR, Katsuda MS, Furlaneto MC, Maia LF (2019) Antimicrobial activity of enterocin obtained from Enterococcus durans on Shiga-like toxin-producing Escherichia coli. Cienc Rural. https://doi.org/10.1590/0103-8478cr20190297
Xiao LJ, Kamau E, Donze D, Grove A (2011) Expression of yeast high mobility group protein HMO1 is regulated by TOR signaling. Gene 489:55–62. https://doi.org/10.1016/j.gene.2011.08.017
Yin X, Fu X, Cheng H, Liang L (2020) α-Tocopherol and naringenin in whey protein isolate particles: partition, antioxidant activity, stability and bioaccessibility. Food Hydrocolloids 106:105895. https://doi.org/10.1016/j.foodhyd.2020.105895
Funding
This work was supported by Fundação Araucária/Governo do Paraná—Brazil, UTFPR-Londrina Campus and State University of Londrina-Paraná. The authors thank the “Central Analítica Multiusuário da UTFPR Campo Mourão (CAMulti-CM)¨ and “Laboratório Multiusuário da UTFPR Campus Londrina (LabMulti-LD)¨ for the analyses. Fernanda V. Leimann (process 039/2019) thanks to Fundação Araucária (CP 15/2017- Programa de Bolsas de Produtividade em Pesquisa e Desenvolvimento Tecnológico) and to CNPq (process number 421541/2018-0, Chamada Universal MCTIC/CNPq n.° 28/2018).
Author information
Authors and Affiliations
Contributions
RR, NAA de S, TFMM and A De O: Methodology and Investigation; HFP: MEV Investigation; MCF and FVL : Writing–review; LF-M: Writing–original draft, Funding acquisition and Project administration.
Corresponding author
Ethics declarations
Conflict of interest
The authors declared that they have no conflicts of interest to this work.
Consent to participate
The authors express their consent to cooperate in this article.
Consent for publication
The authors express their consent to the publication on Journal of Food Science and Technology.
Ethics approval
We declare no ethical issue related with this article.
Additional information
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 (e.g. a society or other partner) 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.
About this article
Cite this article
Ramalho, R., de Souza, N.A.A., Moreira, T.F.M. et al. Antibacterial efficacy of Enterococcus microencapsulated bacteriocin on Listeria monocytogenes, Listeria innocua and Listeria ivanovi. J Food Sci Technol 60, 262–271 (2023). https://doi.org/10.1007/s13197-022-05611-0
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13197-022-05611-0