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Commensal production of a broad-spectrum and short-lived antimicrobial peptide polyene eliminates nasal Staphylococcus aureus.

ABSTRACT: Antagonistic bacterial interactions often rely on antimicrobial bacteriocins, which attack only a narrow range of target bacteria. However, antimicrobials with broader activity may be advantageous. Here we identify an antimicrobial called epifadin, which is produced by nasal Staphylococcus epidermidis IVK83. It has an unprecedented architecture consisting of a non-ribosomally synthesized peptide, a polyketide component and a terminal modified amino acid moiety. Epifadin combines a wide antimicrobial target spectrum with a short life span of only a few hours. It is highly unstable under in vivo-like conditions, potentially as a means to limit collateral damage of bacterial mutualists. However, Staphylococcus aureus is eliminated by epifadin-producing S. epidermidis during co-cultivation in vitro and in vivo, indicating that epifadin-producing commensals could help prevent nasal S. aureus carriage. These insights into a microbiome-derived, previously unknown antimicrobial compound class suggest that limiting the half-life of an antimicrobial may help to balance its beneficial and detrimental activities.

SUBMITTER: Torres Salazar BO

PROVIDER: S-EPMC11310079 | biostudies-literature | 2024 Jan

REPOSITORIES: biostudies-literature

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Commensal production of a broad-spectrum and short-lived antimicrobial peptide polyene eliminates nasal Staphylococcus aureus.

Torres Salazar Benjamin O BO Dema Taulant T Schilling Nadine A NA Janek Daniela D Bornikoel Jan J Berscheid Anne A Elsherbini Ahmed M A AMA Krauss Sophia S Jaag Simon J SJ Lämmerhofer Michael M Li Min M Alqahtani Norah N Horsburgh Malcolm J MJ Weber Tilmann T Beltrán-Beleña José Manuel JM Brötz-Oesterhelt Heike H Grond Stephanie S Krismer Bernhard B Peschel Andreas A

Nature microbiology 20231218 1

Antagonistic bacterial interactions often rely on antimicrobial bacteriocins, which attack only a narrow range of target bacteria. However, antimicrobials with broader activity may be advantageous. Here we identify an antimicrobial called epifadin, which is produced by nasal Staphylococcus epidermidis IVK83. It has an unprecedented architecture consisting of a non-ribosomally synthesized peptide, a polyketide component and a terminal modified amino acid moiety. Epifadin combines a wide antimicro ...[more]

PMID: 38110697

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Project description:BackgroundBacterial pathogens such as Staphylococcus aureus colonize body surfaces of part of the human population, which represents a critical risk factor for skin disorders and invasive infections. However, such pathogens do not belong to the human core microbiomes. Beneficial commensal bacteria can often prevent the invasion and persistence of such pathogens by using molecular strategies that are only superficially understood. We recently reported that the commensal bacterium Staphylococcus lugdunensis produces the novel antibiotic lugdunin, which eradicates S. aureus from the nasal microbiomes of hospitalized patients. However, it has remained unclear if S. lugdunensis may affect S. aureus carriage in the general population and which external factors might promote S. lugdunensis carriage to enhance its S. aureus-eliminating capacity.ResultsWe could cultivate S. lugdunensis from the noses of 6.3% of healthy human volunteers. In addition, S. lugdunensis DNA could be identified in metagenomes of many culture-negative nasal samples indicating that cultivation success depends on a specific bacterial threshold density. Healthy S. lugdunensis carriers had a 5.2-fold lower propensity to be colonized by S. aureus indicating that lugdunin can eliminate S. aureus also in healthy humans. S. lugdunensis-positive microbiomes were dominated by either Staphylococcus epidermidis, Corynebacterium species, or Dolosigranulum pigrum. These and further bacterial commensals, whose abundance was positively associated with S. lugdunensis, promoted S. lugdunensis growth in co-culture. Such mutualistic interactions depended on the production of iron-scavenging siderophores by supportive commensals and on the capacity of S. lugdunensis to import siderophores. Video Abstract CONCLUSIONS: These findings underscore the importance of microbiome homeostasis for eliminating pathogen colonization. Elucidating mechanisms that drive microbiome interactions will become crucial for microbiome-precision editing approaches.

Project description:ObjectivesAntimicrobial resistance (AMR) has become a global public health concern which threatens the effective treatment of bacterial infections. Resistant Staphylococcus aureus (including MRSA) increasingly appears in individuals with no healthcare associated risks. Our study assessed risk factors for nasal carriage of resistant S. aureus in a multinational, healthy, community-based population, including ecological exposure to antibiotics.MethodsData were collected in eight European countries (Austria, Belgium, Croatia, France, Hungary, the Netherlands, Spain and Sweden). Commensal AMR patterns were assessed by collecting 28,929 nasal swabs from healthy persons (aged 4+). Ecological exposure to antibiotics was operationalized as systemic antibiotic treatment patterns, extracted from electronic medical records of primary care practices in which the participants were listed (10-27 per country). A multilevel analysis related AMR in nasal commensal S. aureus to antibiotic exposure and other risk factors (e.g. age and profession).ResultsOf the 6,093 S. aureus isolates, 77% showed resistance to at least one antibiotic. 7.1% exhibited multidrug resistance (defined as resistance to 3 or more antibiotic classes), and we found 78 cases MRSA (1.3%). A large variation in antibiotic exposure was found between and within countries. Younger age and a higher proportion of penicillin prescriptions in a practice were associated with higher odds for carriage of a resistant S. aureus. Also, we found higher multidrug resistance rates in participants working in healthcare or nurseries.ConclusionsThis study indicates that in a population with no recent antibiotic use, the prescription behavior of the general practitioner affects the odds for carriage of a resistant S. aureus, highlighting the need for cautious prescribing in primary care. Finally, since variation in AMR could partly be explained on a national level, policy initiatives to decrease AMR should be encouraged at the national level within Europe.

Dataset Information

Commensal production of a broad-spectrum and short-lived antimicrobial peptide polyene eliminates nasal Staphylococcus aureus.

Publications

Commensal production of a broad-spectrum and short-lived antimicrobial peptide polyene eliminates nasal Staphylococcus aureus.

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