Commensal coagulase-negative Staphylococcus from the udder of healthy cows inhibits biofilm formation of mastitis-related pathogens

Isaac, Paula; Bohl, Luciana Paola; Breser, María Laura; Orellano, María Soledad; Conesa, Agustín; Ferrero, Marcela Alejandra; Porporatto, Carina

doi:10.1016/j.vetmic.2017.05.025

Cited by 34 publications

(21 citation statements)

References 31 publications

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“…Also, a cell-free supernatant from commensal Staphylococcus chromogenes was shown to have antibiofilm properties against coagulase-negative Staphylococcus clinical isolates and a limited impact on S. aureus clinical isolates (36). Unlike the bioactivity described herein, the authors found that the activity was lost when the supernatant was treated with heat or proteinase K (36).…”

Section: Discussionmentioning

confidence: 62%

“…Antibiofilm compounds derived from marine microorganisms were described, and recently, butenolide, a nontoxic compound derived from a marine Streptomyces sp., was shown to be effective in inhibiting MRSA biofilm formation and eradicating established biofilms (35). Also, a cell-free supernatant from commensal Staphylococcus chromogenes was shown to have antibiofilm properties against coagulase-negative Staphylococcus clinical isolates and a limited impact on S. aureus clinical isolates (36). Unlike the bioactivity described herein, the authors found that the activity was lost when the supernatant was treated with heat or proteinase K (36).…”

Section: Discussionmentioning

confidence: 73%

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Small Molecules Produced by Commensal Staphylococcus epidermidis Disrupt Formation of Biofilms by Staphylococcus aureus

Glatthardt

Campos

Chamon

et al. 2020

Appl Environ Microbiol

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The microbiota influences host health through several mechanisms, including protecting it from pathogen colonization. Staphylococcus epidermidis is one of the most frequently found species in the skin microbiota, and its presence can limit the development of pathogens such as Staphylococcus aureus. S. aureus causes diverse types of infections ranging from skin abscesses to bloodstream infections. Given the increasing prevalence of S. aureus drug-resistant strains, it is imperative to search for new strategies for treatment and prevention. Thus, we investigated the activity of molecules produced by a commensal S. epidermidis isolate against S. aureus biofilms. We showed that molecules present in S. epidermidis cell-free conditioned media (CFCM) caused a significant reduction in biofilm formation in most S. aureus clinical isolates, including all 4 agr types and agr-defective strains, without any impact on growth. S. epidermidis molecules also disrupted established S. aureus biofilms and reduced the antibiotic concentration required to eliminate them. Preliminary characterization of the active compound showed that its activity is resistant to heat, protease inhibitors, trypsin, proteinase K, and sodium periodate treatments, suggesting that it is not proteinaceous. RNA sequencing revealed that S. epidermidis-secreted molecules modulate the expression of hundreds of S. aureus genes, some of which are associated with biofilm production. Biofilm formation is one of the main virulence factors of S. aureus and has been associated with chronic infections and antimicrobial resistance. Therefore, molecules that can counteract this virulence factor may be promising alternatives as novel therapeutic agents to control S. aureus infections. IMPORTANCE S. aureus is a leading agent of infections worldwide, and its main virulence characteristic is the ability to produce biofilms on surfaces such as medical devices. Biofilms are known to confer increased resistance to antimicrobials and to the host immune responses, requiring aggressive antibiotic treatment and removal of the infected surface. Here, we investigated a new source of antibiofilm compounds, the skin microbiome. Specifically, we found that a commensal strain of S. epidermidis produces molecules with antibiofilm activity, leading to a significant decrease of S. aureus biofilm formation and to a reduction of previously established biofilms. The molecules potentiated the activity of antibiotics and affected the expression of hundreds of S. aureus genes, including those associated with biofilm formation. Our research highlights the search for compounds that can aid us in the fight against S. aureus infections.

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Section: Discussionmentioning

confidence: 62%

Section: Discussionmentioning

confidence: 73%

Small Molecules Produced by Commensal Staphylococcus epidermidis Disrupt Formation of Biofilms by Staphylococcus aureus

Glatthardt

Campos

Chamon

et al. 2020

Appl Environ Microbiol

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“…Therefore, it is not clear whether NAS should be considered commensal bacteria or opportunistic pathogens. Additionally, the effects of individual NAS species on udder health are not well characterized (7–9). Mechanisms that allow these organisms to colonize and cause mastitis are not well-known (2, 3, 10).…”

Section: Introductionmentioning

confidence: 99%

Comprehensive Virulence Gene Profiling of Bovine Non- aureus Staphylococci Based on Whole-Genome Sequencing Data

et al. 2019

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Non-aureus staphylococci (NAS) are the most frequently isolated pathogens from intramammary infection (IMI) in dairy cattle. Virulence factors (VFs) and mechanisms by which NAS cause IMI are not fully known. Herein, we analyzed the distribution of 191 VFs in 441 genomes of 25 NAS species, after classifying VFs into functional categories: adherence (n = 28), exoenzymes (n = 21), immune evasion (n = 20), iron metabolism (n = 29), and toxins (n = 93). In addition to establishing VF gene profiles, associations of VF genes between and among functional categories were computed, revealing distinctive patterns of association among VFs for various NAS species. Associations were also computed for low, medium, and high somatic cell count (SCC) and clinical mastitis (CM) isolates, demonstrating distinctive patterns of associations for low SCC and CM isolates, but no differences between high SCC and CM isolates. To determine whether VF distributions had any association with SCC or CM, various clustering approaches, including complete linkages, Ward clustering, and t-distributed stochastic neighbor embedding, were applied. However, no clustering of isolates representing low SCC, medium SCC, or high SCC or CM was identified. Regression analysis to test for associations with individual VF functional categories demonstrated that each additional toxin and host immune evasion gene increased the odds of having high SCC or CM, although an overall increase in the number of VFs was not associated with increased SCC or occurrence of CM. In conclusion, we established comprehensive VF gene profiling, determined VF gene distributions and associations, calculated pathogenic potentials of all NAS species, and detected no clear link between VF genes and mastitis. IMPORTANCE Non-aureus staphylococci (NAS) are the most frequently isolated pathogens from milk in dairy cattle worldwide. The virulence factors (VFs) and mechanisms by which these bacteria cause udder infection are not fully known. We determined the distribution and associations of 191 VFs in 25 NAS species and investigated the relationship between VFs and disease. Although the overall number of VFs was not associated with disease severity, increasing numbers of toxin and host immune evasion genes specifically were associated with more severe disease outcomes. These findings suggest that the development of disease and the interactions of VFs with the host are complex and determined by the interplay of genes rather than just the presence of virulence genes. Together, our results provide foundational genetic knowledge to other researchers to design and conduct further experiments, focusing on understanding the synergy between VFs and roles of individual NAS species in IMI and characterizing species-specific effects on udder health.

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“…Similar to S. aureus , various CNS species have been isolated from extramammary sites such as bovine skin and teats [7,14,15]. Some authors suggest that some CNS strains as a native part of a microflora may play a positive role in the maintenance of udder health [16]. These facts have to be considered in regard to the promotion of a prudent use of antimicrobials, as in such cases these bacteria can be recovered from milk samples of dairy cows without any apparent increase in somatic cell count (SCC) [17,18,19].…”

Section: Introductionmentioning

confidence: 99%

Characterization of Staphylococcus Species Isolated from Bovine Quarter Milk Samples

Wald

Heß

Urbantke

et al. 2019

Animals

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Staphylococcus (S.) aureus is considered as a major mastitis pathogen, with considerable epidemiological information on such infections while the epidemiology of coagulase-negative staphylococci (CNS) is more controversial. The aim of this study was to use matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOF MS) technology for identification of staphylococci isolated from bovine milk at species level and to characterize them in reference to presentation, somatic cell count (SCC), bacterial shedding (cfu) and antimicrobial resistance patterns. A total of 200 staphylococcal isolates (S. aureus n = 100; CNS n = 100) originating from aseptically collected quarter milk samples from different quarters of dairy cows were included in the study. They originated from cases of clinical (CM) and subclinical mastitis (SCM) or were isolated from milk with SCC ≤ 100,000 cells/mL in pure culture. We found staphylococci predominantly in cases of SCM (n = 120). In low-SCC cows, 12 S. aureus and 32 CNS isolates were detected. Eighteen percent of each were associated with CM. Eleven CNS species were identified, S. chromogenes (n = 26) and S. xylosus (n = 40) predominated. CNS, particularly those in low-SCC cows, showed higher MIC90 (minimal inhibitory concentration) values for penicillin, ampicillin, cefoperazone, pirlimycin and marbofloxacin. Based on the present results, a careful interpretation of laboratory results is recommended to avoid antimicrobial therapy of staphylococci without clinical relevance and to ensure prudent use of antimicrobials.

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Commensal coagulase-negative Staphylococcus from the udder of healthy cows inhibits biofilm formation of mastitis-related pathogens

Cited by 34 publications

References 31 publications

Small Molecules Produced by Commensal Staphylococcus epidermidis Disrupt Formation of Biofilms by Staphylococcus aureus

Small Molecules Produced by Commensal Staphylococcus epidermidis Disrupt Formation of Biofilms by Staphylococcus aureus

Comprehensive Virulence Gene Profiling of Bovine Non- aureus Staphylococci Based on Whole-Genome Sequencing Data

Characterization of Staphylococcus Species Isolated from Bovine Quarter Milk Samples

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