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Staphylococcal Biofilm on the Surface of Catheters: Electron Microscopy Evaluation of the Inhibition of Biofilm Growth by RNAIII Inhibiting Peptide

de Oliveira, Adilson, Pinheiro-Hubinger, Luiza, Pereira, Valéria Cataneli, Riboli, Danilo Flávio Moraes, Martins, Katheryne Benini, Romero, Letícia Calixto, Cunha, Maria de Lourdes Ribeiro de Souza da·2021·Antibiotics
DOI 10.3390/antibiotics10070879PMC PMC8300745
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Abstract

Staphylococcus aureus and coagulase-negative staphylococci (CoNS) have become the main causative agents of medical device-related infections due to their biofilm-forming capability, which protects them from the host’s immune system and from the action of antimicrobials. This study evaluated the ability of RNA III inhibiting peptide (RIP) to inhibit biofilm formation in 10 strains isolated from clinical materials, including one S. aureus strain, two S. epidermidis, two S. haemolyticus, two S. lugdunensis, and one isolate each of the following species: S. warneri, S. hominis, and S. saprophyticus. The isolates were selected from a total of 200 strains evaluated regarding phenotypic biofilm production and the presence and expression of the ica operon. The isolates were cultured in trypticase soy broth with 2% glucose in 96-well polystyrene plates containing catheter segments in the presence and absence of RIP. The catheter segments were observed by scanning electron microscopy. The results showed inhibition of biofilm formation in the presence of RIP in all CoNS isolates; however, RIP did not interfere with biofilm formation by S. aureus. RIP is a promising tool that might be used in the future for the prevention of biofilm-related infections caused by CoNS.

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Figure 1 Schematic representation of agr control in staphylococci. As the bacteria multiply, RAP reaches a concentration threshold, inducing the phosphorylation of TRAP that triggers a poorly known mechanism for the synthesis of QSII, which consists of the products of the agr system. The agr system is composed of two divergent transcripts, RNAII and RNAIII. RNAII encodes AgrA, AgrC, AgrD, and AgrB. AgrD produces autoinducing peptide (AIP) that is processed by AgrB maturation and export. At a certain threshold concentration, AIP induces the phosphorylation of its receptor AgrC, and phosphorylated AgrA activates transcription from the P3 promoter, leading to the production of RNAIII. In addition to the presence of the RAP-TRAP system, there is also an antagonist, RIP, that can inhibit RNAIII activity. RIP competes with RAP to block TRAP phosphorylation, shutting down QS1 and agr expression.
Figure 1 Schematic representation of agr control in staphylococci. As the bacteria multiply, RAP reaches a concentration threshold, inducing the phosphorylation of TRAP that triggers a poorly known mechanism for the synthesis of QSII, which consists of the products of the agr system. The agr system is composed of two divergent transcripts, RNAII and RNAIII. RNAII encodes AgrA, AgrC, AgrD, and AgrB. AgrD produces autoinducing peptide (AIP) that is processed by AgrB maturation and export. At a certain threshold concentration, AIP induces the phosphorylation of its receptor AgrC, and phosphorylated AgrA activates transcription from the P3 promoter, leading to the production of RNAIII. In addition to the presence of the RAP-TRAP system, there is also an antagonist, RIP, that can inhibit RNAIII activity. RIP competes with RAP to block TRAP phosphorylation, shutting down QS1 and agr expression.CC BY · PubMed Central
Figure 2 (a,b): SEM results for the positive control S. epidermidis ATCC 35983 (weakly adherent) (a) pure culture; (b) S. epidermidis ATCC 35983 isolate incubated with 200 µg/mL RIP. Scale bar (a,b): 10 µm.
Figure 2 (a,b): SEM results for the positive control S. epidermidis ATCC 35983 (weakly adherent) (a) pure culture; (b) S. epidermidis ATCC 35983 isolate incubated with 200 µg/mL RIP. Scale bar (a,b): 10 µm.CC BY · PubMed Central
Figure 3 (a,b): SEM results for the same S. saprophyticus isolate: (a): pure culture; (b): S. saprophyticus isolate incubated with 200 µg/mL RIP. (c,d): S. epidermidis ADBC carrying the complete operon; (c): pure culture; (d): S. epidermidis incubated with 200 µg/mL RIP. (e,f): S. epidermidis DBC carrying the icaDBC genes; (e): pure culture; (f): S. epidermidis incubated with 200 µg/mL RIP. (g,h): S. haemolyticus A expressing only the icaA gene; (g): pure culture; (h): S. haemolyticus incubated with 200 µg/mL RIP. (i,j): SEM results for the same S. hominis isolate; (i): pure culture; (j): S. hominis incubated with 200 µg/mL RIP. (k,l): SEM results for the same S. warneri isolate; (k): pure culture; (l): S. warneri incubated with 200 µg/mL RIP. (m,n): SEM results for S. lugdunensis: (m): pure culture; (n): S. lugdunensis incubated with 200 µg/mL RIP. (o,p): SEM results for the same S. aureus isolate: (o): pure culture; (p): S. aureus incubated with 200 µg/mL RIP. Scale bars: (a,b): 10 µm; (c,d,k–p): 20 µm; (e–h): 10 µm; (i,j): 5 µm.
Figure 3 (a,b): SEM results for the same S. saprophyticus isolate: (a): pure culture; (b): S. saprophyticus isolate incubated with 200 µg/mL RIP. (c,d): S. epidermidis ADBC carrying the complete operon; (c): pure culture; (d): S. epidermidis incubated with 200 µg/mL RIP. (e,f): S. epidermidis DBC carrying the icaDBC genes; (e): pure culture; (f): S. epidermidis incubated with 200 µg/mL RIP. (g,h): S. haemolyticus A expressing only the icaA gene; (g): pure culture; (h): S. haemolyticus incubated with 200 µg/mL RIP. (i,j): SEM results for the same S. hominis isolate; (i): pure culture; (j): S. hominis incubated with 200 µg/mL RIP. (k,l): SEM results for the same S. warneri isolate; (k): pure culture; (l): S. warneri incubated with 200 µg/mL RIP. (m,n): SEM results for S. lugdunensis: (m): pure culture; (n): S. lugdunensis incubated with 200 µg/mL RIP. (o,p): SEM results for the same S. aureus isolate: (o): pure culture; (p): S. aureus incubated with 200 µg/mL RIP. Scale bars: (a,b): 10 µm; (c,d,k–p): 20 µm; (e–h): 10 µm; (i,j): 5 µm.CC BY · PubMed Central

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Metadata

Authors
de Oliveira, A., Pinheiro-Hubinger, L., Pereira, V. C., Riboli, D. F. M., Martins, K. B., Romero, L. C., & Cunha, M. D. L. R. D. S. D.
Venue
Antibiotics
Publisher
MDPI AG
Published
2021-07-20
Volume
10
Issue
7
Pages
879
ISSN
2079-6382
DOI
10.3390/antibiotics10070879
PMC
PMC8300745
Cited by
10
References
1
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
  • FAPESP (2011/07285-5)
  • São Paulo State Department of Education (1)

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