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Cited by 155Milk Quality and Mastitis in Dairy CowsProbiotics and Fermented FoodsRuminant Nutrition and Digestive Physiology

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Lactic Acid Bacteria Isolated from Bovine Mammary Microbiota: Potential Allies against Bovine Mastitis

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Bouchard, Damien S., Seridan, Bianca, Saraoui, Taous, Rault, Lucie, Germon, Pierre, Gonzalez-Moreno, Candelaria, Nader-Macias, Fatima M. E., Baud, Damien, François, Patrice, Chuat, Victoria, Chain, Florian, Langella, Philippe, Nicoli, Jacques, Le Loir, Yves, Even, Sergine·2015·PLOS ONE
DOI 10.1371/journal.pone.0144831PMC PMC4694705
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Abstract

Bovine mastitis is a costly disease in dairy cattle worldwide. As of yet, the control of bovine mastitis is mostly based on prevention by thorough hygienic procedures during milking. Additional strategies include vaccination and utilization of antibiotics. Despite these measures, mastitis is not fully under control, thus prompting the need for alternative strategies. The goal of this study was to isolate autochthonous lactic acid bacteria (LAB) from bovine mammary microbiota that exhibit beneficial properties that could be used for mastitis prevention and/or treatment. Sampling of the teat canal led to the isolation of 165 isolates, among which a selection of ten non-redundant LAB strains belonging to the genera Lactobacillus and Lactococcus were further characterized with regard to several properties: surface properties (hydrophobicity, autoaggregation); inhibition potential of three main mastitis pathogens, Staphylococcus aureus, Escherichia coli and Streptococcus uberis; colonization capacities of bovine mammary epithelial cells (bMEC); and immunomodulation properties. Three strains, Lactobacillus brevis 1595 and 1597 and Lactobacillus plantarum 1610, showed high colonization capacities and a medium surface hydrophobicity. These strains are good candidates to compete with pathogens for mammary gland colonization. Moreover, nine strains exhibited anti-inflammatory properties, as illustrated by the lower IL-8 secretion by E. coli-stimulated bMEC in the presence of these LAB. Full genome sequencing of five candidate strains allowed to check for undesirable genetic elements such as antibiotic resistance genes and to identify potential bacterial determinants involved in the beneficial properties. This large screening of beneficial properties while checking for undesirable genetic markers allowed the selection of promising candidate LAB strains from bovine mammary microbiota for the prevention and/or treatment of bovine mastitis.

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Figures

Fig 1 Adhesion of lactic acid bacteria to bovine mammary epithelial cells. Lactic acid bacteria populations that adhered to bMEC were determined after 1 h of interaction at a MOI of 400:1 (A) and 2000:1 (B), respectively. Data are presented as mean population per well (i.e., corresponding to 2.5x105 bMEC) ± standard deviation. Each experiment was done in triplicate and differences between strains were assessed using a one-way analysis of variance, followed by Tukey’s range test. Letters a, b, c and d indicate homogeneous statistical processing groups that were significantly different according to Tukey’s range test.
Fig 1 Adhesion of lactic acid bacteria to bovine mammary epithelial cells. Lactic acid bacteria populations that adhered to bMEC were determined after 1 h of interaction at a MOI of 400:1 (A) and 2000:1 (B), respectively. Data are presented as mean population per well (i.e., corresponding to 2.5x105 bMEC) ± standard deviation. Each experiment was done in triplicate and differences between strains were assessed using a one-way analysis of variance, followed by Tukey’s range test. Letters a, b, c and d indicate homogeneous statistical processing groups that were significantly different according to Tukey’s range test.CC BY · PubMed Central
Fig 2 Internalization of lactic acid bacteria into bovine mammary epithelial cells. Lactic acid bacteria populations internalized into bMEC were determined after 2 h of interaction at a MOI of 400:1 (A) and 2000:1 (B), respectively. Data are presented as mean population per well (i.e., corresponding to 2.5x105 bMEC) ± standard deviation. Each experiment was done in triplicate and differences between strains were assessed using one-way analysis of variance, followed by Tukey’s range test. Letters a, b, c and d indicate homogeneous statistical processing groups that were significantly different according to Tukey’s range test.
Fig 2 Internalization of lactic acid bacteria into bovine mammary epithelial cells. Lactic acid bacteria populations internalized into bMEC were determined after 2 h of interaction at a MOI of 400:1 (A) and 2000:1 (B), respectively. Data are presented as mean population per well (i.e., corresponding to 2.5x105 bMEC) ± standard deviation. Each experiment was done in triplicate and differences between strains were assessed using one-way analysis of variance, followed by Tukey’s range test. Letters a, b, c and d indicate homogeneous statistical processing groups that were significantly different according to Tukey’s range test.CC BY · PubMed Central
Fig 3 Modulation of cytokine IL-8 production by LAB isolates. A: modulation of IL-8 production by the PS cell line in the presence of LAB isolates (MOI 100:1). Bars represent the mean IL-8 production ± standard deviation for four assays (two biological and two technical replicates), normalized with regard to IL-8 production by unstimulated PS cells (76 +/-16 pg/mL as a mean); B: modulation of IL-8 production by the E. coli-stimulated PS cell line in the presence of LAB isolates. E. coli was used at MOI 1:1 and LAB at MOI 100:1. Bars represent the mean IL-8 production ± standard deviation for four assays, normalized with regard to IL-8 production by E. coli-stimulated PS cells (368 ± 88 pg/mL as a mean). Differences in IL-8 production with regard to the reference condition were assessed using the Mann-Whitney test (* p < 0.05).
Fig 3 Modulation of cytokine IL-8 production by LAB isolates. A: modulation of IL-8 production by the PS cell line in the presence of LAB isolates (MOI 100:1). Bars represent the mean IL-8 production ± standard deviation for four assays (two biological and two technical replicates), normalized with regard to IL-8 production by unstimulated PS cells (76 +/-16 pg/mL as a mean); B: modulation of IL-8 production by the E. coli-stimulated PS cell line in the presence of LAB isolates. E. coli was used at MOI 1:1 and LAB at MOI 100:1. Bars represent the mean IL-8 production ± standard deviation for four assays, normalized with regard to IL-8 production by E. coli-stimulated PS cells (368 ± 88 pg/mL as a mean). Differences in IL-8 production with regard to the reference condition were assessed using the Mann-Whitney test (* p < 0.05).CC BY · PubMed Central

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Metadata

Authors
Bouchard, D. S., Seridan, B., Saraoui, T., Rault, L., Germon, P., Gonzalez-Moreno, C., Nader-Macias, F. M. E., Baud, D., François, P., Chuat, V., Chain, F., Langella, P., Nicoli, J., Le Loir, Y., & Even, S.
Affiliations
  • Institut Agro Rennes-Angers (FR)
  • Infectiologie et santé publique (FR)
  • University Hospital of Geneva (CH)
  • Microbiologie de l’alimentation au service de la santé (FR)
  • Universidade Federal de Minas Gerais (BR)
Corresponding author
Even, Sergine
ORCID
Venue
PLOS ONE
Publisher
Public Library of Science (PLoS)
Published
2015-12-29
Volume
10
Issue
12
Pages
e0144831
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0144831
PMC
PMC4694705
OpenAlex
W2219521950
Cited by
144
References
40
Citations by year
2026: 5 · 2025: 10 · 2024: 23 · 2023: 15 · 2022: 15 · 2021: 20 · 2020: 16 · 2019: 6 · 2018: 12 · 2017: 15 · 2016: 7
FWCI
24.59
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (publishedVersion, other-oa)
  • Archive ouverte UNIGE (University of Geneva) (publishedVersion, other-oa)
  • HAL (submittedVersion, cc-by)
  • Americanae (AECID Library) (submittedVersion, cc-by-nc-sa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, cc-by-nc-sa)
  • Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
  • Greater South Information System
Funders
  • Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
  • Institut National de la Recherche Agronomique
  • Campus France
Topics
  • Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Milk Quality and Mastitis in Dairy Cows
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
  • Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Ruminant Nutrition and Digestive Physiology
Keywords
bovine mastitis, lactic acid bacteria, Lactobacillus brevis, Lactobacillus plantarum, Lactococcus, mastitis prevention, competitive exclusion, anti-inflammatory activity, IL-8 secretion, Staphylococcus aureus, Escherichia coli, Streptococcus uberis, hydrophobicity, self-aggregation, antibiotic resistance genes, dairy cattle
MeSH terms
Animals, Bacterial Adhesion, Bacterial Infections, Cattle, Female, Humans, Lactobacillus, Mammary Glands, Animal, Mastitis, Bovine, Milk, Molecular Sequence Data, RNA, Bacterial, RNA, Ribosomal, 16S, Genome, Bacterial, Lactococcus, Sequence Analysis, DNA, HT29 Cells, Molecular Typing, Microbiota

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