Lactic acid bacteria from artisanal raw goat milk cheeses: technological properties and antimicrobial potential

Submitted: 1 July 2023
Accepted: 11 September 2023
Published: 27 October 2023
Abstract Views: 1349
PDF: 280
HTML: 5
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

In cheese-making, a starter culture composed of adequately chosen lactic acid bacteria (LAB) may be suitable to ensure the rapid acidification of milk, improve textural and sensory characteristics, and avoid pathogen proliferation. In this work, 232 LAB isolates collected from artisanal goat’s raw milk cheeses produced in Portugal were evaluated for their antimicrobial capacity (at 10 and 37°C), as well as their acidifying and proteolytic properties. Among the 232 isolates, at least 98% of those isolated in De Man-Rogosa-Sharpe (MRS) agar presented antagonism against Listeria monocytogenes, Salmonella Typhimurium, or Staphylococcus aureus, whereas less than 28.1% of M17-isolated LAB showed antagonism against these pathogens. M17-isolated LAB displayed better results than MRS ones in terms of acidifying capacity. As for the proteolytic assay, only 2 MRS isolates showed casein hydrolysis capacity. Principal component analyses and molecular characterization of a subset of selected isolates were conducted to identify those with promising capacities and to correlate the identified LAB genera and species with their antimicrobial, acidifying, and/or proteolytic properties. Lactococcus strains were associated with the highest acidifying capacity, whereas Leuconostoc and Lacticaseibacillus strains were more related to antimicrobial capacities. Leuconostoc mesenteroides, Lactococcus lactis, and Lacticaseibacillus paracasei were the predominant organisms found. The results of this work highlight various strains with pathogen inhibition capacity and suitable technological properties to be included in a customized starter culture. In future work, it is necessary to appropriately define the starter culture and implement it in the cheese-making process to evaluate if the in-vitro capacities are observable in a real food system.

Dimensions

Altmetric

PlumX Metrics

Downloads

Download data is not yet available.

Citations

Araújo-Rodrigues H, dos Santos MTPG, Ruiz-Moyano S, Tavaria FK, Martins APL, Alvarenga N, Pintado ME, 2021. Technological and protective performance of LAB isolated from Serpa PDO cheese: towards selection and development of an autochthonous starter culture. LWT 150:112079. DOI: https://doi.org/10.1016/j.lwt.2021.112079
Beresford TP, Fitzsimons NA, Brennan NL, Cogan TM, 2001. Recent advances in cheese microbiology. Int Dairy J 11:259-74. DOI: https://doi.org/10.1016/S0958-6946(01)00056-5
Campagnollo FB, Margalho LP, Kamimura BA, Feliciano MD, Freire L, Lopes LS, Alvarenga VO, Cadavez VAP, Gonzales-Barron U, Schaffner DW, Sant'Ana AS, 2018. Selection of indigenous lactic acid bacteria presenting anti-listerial activity, and their role in reducing the maturation period and assuring the safety of traditional Brazilian cheeses. Food Microbiol 73:288-97. DOI: https://doi.org/10.1016/j.fm.2018.02.006
Castro RCS, de Oliveira APD, de Souza EAR, Correia TMA, de Souza JV, Dias FS, 2018. Lactic acid bacteria as biological control of Staphylococcus aureus in Coalho goat cheese. Food Technol Biotechnol 56:431-40.
Coelho MC, Malcata FX, Silva CCG, 2022. Lactic acid bacteria in raw-milk cheeses: from starter cultures to probiotic functions. Foods 11:2276. DOI: https://doi.org/10.3390/foods11152276
Cogan TM, Barbosa M, Beuvier E, Bianchi-Salvadori B, Cocconceli PS, Fernandes I, Gomez J, Gomez R, Kalantzopoulos G, Ledda A, Medina M, Rea MC, Rodriguez E, 1997. Characterization of the lactic acid bacteria in artisanal dairy products. J Dairy Res 64:409-21. DOI: https://doi.org/10.1017/S0022029997002185
Durlu-Ozkaya F, Xanthopoulos V, Tunail N, Litopoulou-Tzanetaki E, 2001. Technologically important properties of lactic acid bacteria isolates from Beyaz cheese made from raw ewes’ milk. J Appl Microbiol 91:861-70. DOI: https://doi.org/10.1046/j.1365-2672.2001.01448.x
EFSA, 2007. Introduction of a qualified presumption of safety (QPS) approach for assessment of selected microorganisms referred to EFSA - opinion of the scientific committee. EFSA J 587:1-16. DOI: https://doi.org/10.2903/j.efsa.2007.587
Faria AS, Fernandes N, Cadavez V, Gonzales-Barron U, 2021. Screening of lactic acid bacteria isolated from artisanally produced “Alheira” fermented sausages as potential starter cultures. Available from: https://bibliotecadigital.ipb.pt/bitstream/10198/28573/1/Screening%20of%20Lactic.pdf.
Favaro L, Penna ALB, Todorov SD, 2015. Bacteriocinogenic LAB from cheeses - application in biopreservation? Trends Food Sci Technol 41:37-48. DOI: https://doi.org/10.1016/j.tifs.2014.09.001
Franciosi E, Settanni L, Cavazza A, Poznanski E, 2009. Biodiversity and technological potential of wild lactic acid bacteria from raw cows’ milk. Int Dairy J 19:3-11. DOI: https://doi.org/10.1016/j.idairyj.2008.07.008
Gonçalves MTP, Benito MJ, Córdoba MDG, Egas C, Merchán AV, Galván AI, Ruiz-Moyano S, 2018. Bacterial communities in Serpa cheese by culture dependent techniques, 16S rRNA gene sequencing and high-throughput sequencing analysis. J Food Sci 83:1333-41. DOI: https://doi.org/10.1111/1750-3841.14141
Gonzales-Barron U, Campagnollo FB, Schaffner DW, Sant’Ana AS, Cadavez VAP, 2020. Behavior of Listeria monocytogenes in the presence or not of intentionally-added lactic acid bacteria during ripening of artisanal Minas semi-hard cheese. Food Microbiol 91:103545. DOI: https://doi.org/10.1016/j.fm.2020.103545
Gonzales-Barron U, Gonçalves-Tenório A, Rodrigues V, Cadavez V, 2017. Foodborne pathogens in raw milk and cheese of sheep and goat origin: a meta-analysis approach. Curr Opin Food Sci 18:7-13. DOI: https://doi.org/10.1016/j.cofs.2017.10.002
HiMedia Laboratories, 2021. SM agar - technical data. Available from: https://himedialabs.com/td/m763.pdf.
Hou Q, Bai X, Li W, Gao X, Zhang F, Sun Z, Zhang H, 2018. Design of primers for evaluation of lactic acid bacteria populations in complex biological samples. Front Microbiol 9:2045. DOI: https://doi.org/10.3389/fmicb.2018.02045
ISO, 1998. Microbiology of food and animal feeding stuffs - horizontal method for the enumeration of mesophilic lactic acid bacteria—colony-count technique at 30 degrees C. ISO 15214:1998. International Organization for Standardization ed., Geneva, Switzerland.
Margalho LP, Feliciano MD, Silva CE, Abreu JS, Piran MVF, Sant’Ana AS, 2020. Brazilian artisanal cheeses are rich and diverse sources of nonstarter lactic acid bacteria regarding technological, biopreservative, and safety properties - insights through multivariate analysis. J Dairy Sci 103:7908-26. DOI: https://doi.org/10.3168/jds.2020-18194
Margalho LP, Jorge GP, Noleto DAP, Silva CE, Abreu JS, Piran MVF, Brocchi M, Sant'Ana AS, 2021. Biopreservation and probiotic potential of a large set of lactic acid bacteria isolated from Brazilian artisanal cheeses: from screening to in product approach. Microbiol Res 242:126622. DOI: https://doi.org/10.1016/j.micres.2020.126622
Mazdeh FZ, Sasanfar S, Chalipour A, Pirhadi E, Yahyapour G, Mohammadi A, Rostami A, Amini M, Hajimahmoodi M, 2017. Simultaneous determination of preservatives in dairy products by HPLC and chemometric analysis. Int J Anal Chem 2017:3084359. DOI: https://doi.org/10.1155/2017/3084359
Ministry for Primary Industries, 2011. Minimum growth temperatures of foodborne pathogens and recommended chiller temperatures. Available from: https://www.mpi.govt.nz/dmsdocument/44050-Minimum-Growth-Temperatures-of-Foodbourne-Pathogens-and-Recommended-Chiller-Temperatures.
Morandi S, Silvetti T, Batteli G, Brasca M, 2019. Can lactic acid bacteria be an efficient tool for controlling Listeria monocytogenes contamination on cheese surface? The case of Gorgonzola cheese. Food Control 96:499-507. DOI: https://doi.org/10.1016/j.foodcont.2018.10.012
Piraino P, Zotta T, Ricciardi A, McSweeney PLH, Parente E, 2008. Acid production, proteolysis, autolytic and inhibitory properties of lactic acid bacteria isolated from pasta filata cheeses: a multivariate screening study. Int Dairy J 18:81-92. DOI: https://doi.org/10.1016/j.idairyj.2007.06.002
Piraino P, Zotta T, Ricciardi A, Parente E, 2005. Discrimination of commercial Caciocavallo cheeses on the basis of the diversity of lactic microflora and primary proteolysis. Int Dairy J 15:1138-49. DOI: https://doi.org/10.1016/j.idairyj.2004.12.006
Ribeiro SC, Coelho MC, Todorov SD, Franco BDGM, Dapkevicius MLE, Silva CCG, 2014. Technological properties of bacteriocin-producing lactic acid bacteria isolated from Pico cheese an artisanal cow’s milk cheese. J Appl Microbiol 116:573-85. DOI: https://doi.org/10.1111/jam.12388
Silva CCG, Silva SPM, Ribeiro SC, 2018. Application of bacteriocins and protective cultures in dairy food preservation. Front Microbiol 9:594. DOI: https://doi.org/10.3389/fmicb.2018.00594

Supporting Agencies

This work was funded within the EU H2020 PRIMA Project ArtiSaneFood “Innovative bio-interventions and risk modelling approaches for ensuring microbial safety and quality of Mediterranean artisanal fermented foods” (PRIMA/0001/2018). U. Gonzales-Barron and V. Cadavez are also grateful to the Portuguese Foundation for Science and Technology (FCT) for funding PRIMA/0001/2018; and for financial support through national funds FCT/MCTES (PIDDAC) to CIMO (UIDB/00690/2020 and UIDP/00690/2020) and SusTEC (LA/P/0007/2021).

How to Cite

1.
Silva BN, Fernandes N, Carvalho L, Faria AS, Teixeira JA, Rodrigues C, Gonzales-Barron U, Cadavez V. Lactic acid bacteria from artisanal raw goat milk cheeses: technological properties and antimicrobial potential. Ital J Food Safety [Internet]. 2023 Oct. 27 [cited 2024 Nov. 25];12(4). Available from: https://www.pagepressjournals.org/ijfs/article/view/11559