Abstract
Bovine mastitis is an emerging disease that causes large economic losses. Staphylococcus aureus its main etiological agent, is multi-resistant to antimicrobials and produces biofilm. The objective of this study was to investigate the effect of Agave fructans (AF), a type of prebiotic, on multi-resistant and biofilm-forming isolates of S. aureus. Ten isolates of S. aureus from bovine subclinical mastitis previously characterized as highly resistant to antimicrobials and biofilm formers were used in this study. The growth kinetics of S. aureus in the presence of AF was evaluated by the Baranyi and Roberts microbial growth model using the DMFit program. The antibacterial activity of AF against S. aureus was studied by the well-diffusion method and the effect on biofilm formation by the crystal violet method. All assays were performed in triplicate for each isolate and an ANOVA with Tukey’s post hoc was performed considering p < 0.05 as significant. The AF showed a decrease in maximum growth rate (µmax) and OD max levels (Ymax) in all isolates with all concentrations. Also, zones of inhibition were observed due to the effect of all AF concentrations in all isolates in a dose-dependent manner. Interestingly, S. aureus biofilm formation was inhibited by all AF concentrations assessed in this study. More investigations are required to elucidate the mechanisms of action of AF on S. aureus as well as in vivo studies to evaluate its therapeutic efficacy for bovine mastitis.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data sets generated during the present study are available from the corresponding author upon reasonable request.
References
Abdi RD, Gillespie BE, Vaughn J et al (2018) Antimicrobial resistance of Staphylococcus aureus isolates from dairy cows and genetic diversity of resistant isolates. Foodborne Pathog Dis 15:449–458. https://doi.org/10.1089/fpd.2017.2362
Ağçeli GK, Cihangir N (2020) Nano-sized biopolymer levan: its antimicrobial, anti-biofilm and anti-cancer effects. Carbohydr Res 494:108068. https://doi.org/10.1016/j.carres.2020.108068
Al-Ashmawy MA, Sallam KI, Abd-Elghany SM et al (2016) Prevalence, molecular characterization, and antimicrobial susceptibility of methicillin-resistant Staphylococcus aureus isolated from milk and dairy products. Foodborne Pathog Dis 13:156–162. https://doi.org/10.1089/fpd.2015.2038
Aldrete-Herrera PI, López MG, Medina-Torres L et al (2019) Physicochemical composition and apparent degree of polymerization of fructans in five wild agave varieties: potential industrial use. Foods 8:404. https://doi.org/10.3390/foods8090404
Asadpoor M, Ithakisiou G-N, Van Putten JP et al (2021) Antimicrobial activities of alginate and chitosan oligosaccharides against Staphylococcus aureus and Group B Streptococcus. Front Microbiol 12:700605. https://doi.org/10.3389/fmicb.2021.700605
Baranyi J, Roberts TA (1994) A dynamic approach to predicting bacterial growth in food. Int J Food Microbiol 23:277–294. https://doi.org/10.1016/0168-1605(94)90157-0
Byun BY, Lee S-J, Mah J-H (2014) Antipathogenic activity and preservative effect of levan (β-2, 6‐fructan), a multifunctional polysaccharide. Int J Food Sci Technol 49:238–245. https://doi.org/10.1111/ijfs.12304
Cai Y, van Putten JP, Gilbert MS et al (2022) Galacto-oligosaccharides as an anti-bacterial and anti-invasive agent in lung infections. Biomaterials 283:121461. https://doi.org/10.1016/j.biomaterials.2022.121461
Cobirka M, Tancin V, Slama P (2020) Epidemiology and classification of mastitis. Animals 10:2212. https://doi.org/10.3390/ani10122212
Cucarella C, Tormo MA, Ubeda C et al (2004) Role of biofilm-associated protein bap in the pathogenesis of bovine Staphylococcus aureus. Infect Immun 72:2177–2185. https://doi.org/10.1128/iai.72.4.2177-2185.2004
Di Lodovico S, Gasparri F, Di Campli E et al (2020) Prebiotic combinations effects on the colonization of staphylococcal skin strains. Microorganisms 9:37. https://doi.org/10.3390/microorganisms9010037
Franco-Robles E, López MG (2015) Implication of fructans in health: Immunomodulatory and antioxidant mechanisms. Sci World J 2015. https://doi.org/10.1155/2015/289267
García-Gamboa R, Gradilla-Hernández MS, Ortiz-Basurto RI et al (2020) Assessment of intermediate and long chains agave fructan fermentation on the growth of intestinal bacteria cultured in a gastrointestinal tract simulator. Rev Mex Ing Quím 19:827–838. https://doi.org/10.24275/rmiq/Bio842
García-Gamboa R, Domínguez-Simi M, Gradilla-Hernández MS et al (2022) Anticandidal and antibiofilm effect of synbiotics including probiotics and inulin-type fructans. Antibiotics 11:1135
González-Díaz RL, Rodríguez-Gómez F, Cortés-Romero C (2020) Exohidrolasas fructosílicas y su importancia en el metabolismo de fructanos en Agave tequilana Weber var. Azul. Rev Colomb Quím 49:3–12. https://doi.org/10.15446/rcq.v49n3.84882
González-Pérez CJ, Vargas-Arispuro I, Aispuro-Hernández E et al (2019) Potential control of foodborne pathogenic bacteria by Pediococcus pentosaceus and Lactobacillus graminis isolated from fresh vegetables. Microbiol Biotechnol Lett 47:183–194. https://doi.org/10.4014/mbl.1808.08014
Guillen-Torres LE, Franco-Robles E (2018) Efecto Antimicrobiano in Vitro de los Fructanos de Agave Frente a Listeria Monocytogenes. Jóvenes en Cienc 4:125–128
Guzmán-Rodríguez JJ, León-Galván MF, Barboza-Corona JE et al (2020) Analysis of virulence traits of Staphylococcus aureus isolated from bovine mastitis in semi-intensive and family dairy farms. J Vet Sci 21. https://doi.org/10.4142/jvs.2020.21.e77
Guzmán-Rodríguez JJ, Salinas-Pérez E, León-Galván F et al (2021) Relación entre la resistencia a antibióticos y la producción de biofilm de aislados de Staphylococcus aureus provenientes de mastitis bovina. Rev Mex Cienc Pecu 12:1117–1132. https://doi.org/10.22319/rmcp.v12i4.5645
Heikkilä A-M, Liski E, Pyörälä S, Taponen S (2018) Pathogen-specific production losses in bovine mastitis. J Dairy Sci 101:9493–9504. https://doi.org/10.3168/jds.2018-14824
Jamali H, Paydar M, Radmehr B et al (2015) Prevalence and antimicrobial resistance of Staphylococcus aureus isolated from raw milk and dairy products. Food Control 54:383–388. https://doi.org/10.1016/j.foodcont.2015.02.013
Khan MTJ, Ahmad K, Alvi MN et al (2010) Antibacterial and irritant activities of organic solvent extracts of Agave americana Linn., Albizzia lebbek Benth. Achyranthes aspera Linn. And Abutilon indicum Linn-A Preliminary Investigation. Pak J Zool 42:93–97
Maity S, Ambatipudi K (2021) Mammary microbial dysbiosis leads to the zoonosis of bovine mastitis: a one-health perspective. FEMS Microbiol Ecol 97:fiaa241. https://doi.org/10.1093/femsec/fiaa241
Mancilla-Margalli NA, López MG (2006) Water-soluble carbohydrates and fructan structure patterns from Agave and Dasylirion species. J Agric Food Chem 54:7832–7839. https://doi.org/10.1021/jf060354v
Martínez-Ortega EA, López-Briones JS, Rodríguez-Hernández G et al (2020) Antibacterial activity of agave fructans against salmonella typhimurium. Nat Prod Res 34:2639–2641. https://doi.org/10.1080/14786419.2018.1548446
Mellado-Mojica E, López MG (2012) Fructan metabolism in A. tequilana Weber Blue variety along its developmental cycle in the field. J Agric Food Chem 60:11704–11713. https://doi.org/10.1021/jf303332n
Melo P de C, Ferreira LM, Nader Filho A, et al (2013) Comparison of methods for the detection of biofilm formation by Staphylococcus aureus isolated from bovine subclinical mastitis. Braz J Microbiol 44:119–124. https://doi.org/10.1590/S1517-83822013005000031
Moon J-S, Kim H-K, Koo HC et al (2007) The antibacterial and immunostimulative effect of chitosan-oligosaccharides against infection by Staphylococcus aureus isolated from bovine mastitis. Appl Microbiol Biotechnol 75:989–998. https://doi.org/10.1007/s00253-007-0898-8
Mphahlele MP, Oguttu JW, Petzer I-M, Qekwana DN (2020) Prevalence and antimicrobial drug resistance of Staphylococcus aureus isolated from cow milk samples. Vet World 13:2736. https://doi.org/10.14202/vetworld.2020.2736-2742
Nagasawa R, Sato T, Senpuku H (2017) Raffinose induces biofilm formation by Streptococcus mutans in low concentrations of sucrose by increasing production of extracellular DNA and fructan. Appl Environ Microbiol 83:e00869–e00817. https://doi.org/10.1128/AEM.00869-17
Peralta-García I, González-Muñoz F, Elena R-AM et al (2020) Evolution of fructans in Aguamiel (Agave Sap) during the plant production lifetime. Front Nutr 7:566950. https://doi.org/10.3389/fnut.2020.566950
Rainard P, Foucras G, Fitzgerald JR et al (2018) Knowledge gaps and research priorities in Staphylococcus aureus mastitis control. Transbound Emerg Dis 65:149–165. https://doi.org/10.1111/tbed.12698
Rozen R, Bachrach G, Bronshteyn M et al (2001) The role of fructans on dental biofilm formation by Streptococcus sobrinus, Streptococcus mutans, Streptococcus gordonii and Actinomyces viscosus. FEMS Microbiol Lett 195:205–210. https://doi.org/10.1111/j.1574-6968.2001.tb10522.x
Ruegg PL (2017) A 100-Year review: Mastitis detection, management, and prevention. J Dairy Sci 100:10381–10397. https://doi.org/10.3168/jds.2017-13023
Sauer K, Stoodley P, Goeres DM et al (2022) The biofilm life cycle: expanding the conceptual model of biofilm formation. Nat Rev Microbiol 20:608–620. https://doi.org/10.1038/s41579-022-00767-0
Shang Y, Kumar S, Thippareddi H, Kim WK (2018) Effect of dietary fructooligosaccharide (FOS) supplementation on ileal microbiota in broiler chickens. Poult Sci 97:3622–3634. https://doi.org/10.3382/ps/pey131
Silva V, Capelo JL, Igrejas G, Poeta P (2022) Molecular mechanisms of antimicrobial resistance in staphylococcus aureus biofilms. Emerg Modalities Mitig Antimicrob Resist 291–314. https://doi.org/10.1007/978-3-030-84126-3_12
Vasudevan P, Nair MKM, Annamalai T, Venkitanarayanan KS (2003) Phenotypic and genotypic characterization of bovine mastitis isolates of Staphylococcus aureus for biofilm formation. Vet Microbiol 92:179–185. https://doi.org/10.1016/S0378-1135(02)00360-7
Verástegui Á, Verde J, García S et al (2008) Species of Agave with antimicrobial activity against selected pathogenic bacteria and fungi. World J Microbiol Biotechnol 24:1249–1252. https://doi.org/10.1007/s11274-007-9563-8
Acknowledgements
Amador-Sánchez MA thanks CONACYT for a scholarship for their postgraduate studies.
Guzmán-Rodríguez JJ thanks CONACYT for the postdoc fellowship.
We thank Dr. Pedro Damián Loeza Lara from the Universidad de la Ciénega del Estado de Michoacán de Ocampo who donated the S. aureus isolates for this research.
Project conducted by Elena Franco-Robles, member of Thematic network Sustainable Integral Use and Biotechnology of Agaves (AGARED), CONACYT, Mexico.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study’s conception and design. Material preparation, data collection and analysis were performed by J.J.G.R., M.A.A.S, and E.F.R. The first draft of the manuscript was written by J.J.G.R. and E.F.R. and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interest
The authors have no relevant financial or non-financial interests to disclose.
Conflict of interest
The authors declare no conflicts of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Below is the link to the electronic supplementary material.
ESM 1
(PDF 151 KB)
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
Guzmán-Rodríguez, J.J., Gutiérrez-Chávez, A.J., Meléndez-Soto, R.M. et al. Antimicrobial activities of Agave fructans against multi-resistant and biofilm-producing Staphylococcus aureus isolated from bovine mastitis. Vet Res Commun 48, 61–67 (2024). https://doi.org/10.1007/s11259-023-10180-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11259-023-10180-4