Dataset Information

Induction of mastitis by cow-to-mouse fecal and milk microbiota transplantation causes microbiome dysbiosis and genomic functional perturbation in mice.

ABSTRACT:

Background

Mastitis pathogenesis involves a wide range of opportunistic and apparently resident microorganims including bacteria, viruses and archaea. In dairy animals, microbes reside in the host, interact with environment and evade the host immune system, providing a potential for host-tropism to favor mastitis pathogenesis. To understand the host-tropism phenomena of bovine-tropic mastitis microbiomes, we developed a cow-to-mouse mastitis model.

Methods

A cow-to-mouse mastitis model was established by fecal microbiota transplantation (FMT) and milk microbiota transplantation (MMT) to pregnant mice to assess microbiome dysbiosis and genomic functional perturbations through shotgun whole metagenome sequencing (WMS) along with histopathological changes in mice mammary gland and colon tissues.

Results

The cow-to-mouse FMT and MMT from clinical mastitis (CM) cows induced mastitis syndromes in mice as evidenced by histopathological changes in mammary gland and colon tissues. The WMS of 24 samples including six milk (CM = 3, healthy; H = 3), six fecal (CM = 4, H = 2) samples from cows, and six fecal (CM = 4, H = 2) and six mammary tissue (CM = 3, H = 3) samples from mice generating 517.14 million reads (average: 21.55 million reads/sample) mapped to 2191 bacterial, 94 viral and 54 archaeal genomes. The Kruskal-Wallis test revealed significant differences (p = 0.009) in diversity, composition, and relative abundances in microbiomes between CM- and H-metagenomes. These differences in microbiome composition were mostly represented by Pseudomonas aeruginosa, Lactobacillus crispatus, Klebsiella oxytoca, Enterococcus faecalis, Pantoea dispersa in CM-cows (feces and milk), and Muribaculum spp., Duncaniella spp., Muribaculum intestinale, Bifidobacterium animalis, Escherichia coli, Staphylococcus aureus, Massilia oculi, Ralstonia pickettii in CM-mice (feces and mammary tissues). Different species of Clostridia, Bacteroida, Actinobacteria, Flavobacteriia and Betaproteobacteria had a strong co-occurrence and positive correlation as the indicator species of murine mastitis. However, both CM cows and mice shared few mastitis-associated microbial taxa (1.14%) and functional pathways regardless of conservation of mastitis syndromes, indicating the higher discrepancy in mastitis-associated microbiomes among lactating mammals.

Conclusions

We successfully induced mastitis by FMT and MMT that resulted in microbiome dysbiosis and genomic functional perturbations in mice. This study induced mastitis in a mouse model through FMT and MMT, which might be useful for further studies- focused on pathogen(s) involved in mastitis, their cross-talk among themselves and the host.

SUBMITTER: Hoque MN

PROVIDER: S-EPMC9258091 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Lactating cows are routinely treated at dry-off with antibiotic infusions in each quarter for the cure and prevention of pathogenic intramammary infection, which remains the most common disease in dairy herds. This approach is known as blanket dry-cow therapy, usually effective for the prevention and cure of infections, but has been shown to potentially contribute to the emergence and spreading of antibiotic resistant bacterial strains. Exploring the use of non-antibiotic treatments coupled with selective dry-cow therapy is necessary to reduce the risk of antibiotic resistance and potential interference with milk microbiome balance. The impact of selective dry-cow therapy on the physiological milk microbiome needs to be carefully evaluated. In this small-scale trial, five healthy (no mastits, SCC <200,000 cells mL-1) second-parity cows from dry-off to 5 days after calving were sampled. For every cow, each quarter received a different treatment: (i) bismuth salnitrate (internal teat sealant, OrbSeal®, Zoetis, Italy), front right quarter; (ii) cephalonium dihydrate (Cepravin®, MSD, Italy), rear right quarter; (iii) benzathine cloxacillin (Cloxalene dry, Ati, Italy), rear left quarter. No treatment was applied to the remaining quarter (front left) which served as experimental control. For 16S rRNA gene sequencing, bacterial DNA was extracted from 5 ml of milk samples, amplified using the primers for the V3-V4 hypervariable regions and sequenced in one MiSeq (Illumina) run with 2 × 250-base paired-end reads. Bacteriological results confirmed that the quarters were all healthy. The phyla Proteobacteria, Firmicutes, and Actinobacteria were the most abundant for all treatments and controls at all three timepoints, accounting for over 80% of the entire milk microbiota composition. No significant differences were found between treatments and controls in terms of the major alpha and beta diversity indexes, revealing that antibiotic, and non-antibiotic treatments for selective dry-cow therapy did not alter significantly the milk microbiome of dairy cows. The milk microbiota composition showed a clear evolution over the lactation cycle, and the overall changes in the milk microbiota diversity over the lactation cycle were mainly independent of treatments.