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. 2023 Dec 12;11(12):2965.
doi: 10.3390/microorganisms11122965.

A-Type Natriuretic Peptide Alters the Impact of Azithromycin on Planktonic Culture and on (Monospecies and Binary) Biofilms of Skin Bacteria Kytococcus schroeteri and Staphylococcus aureus

Ekaterina V Diuvenji  1 , Ekaterina D Nevolina  1 , Ilya D Solovyev  1 , Marina V Sukhacheva  1 , Sergey V Mart'yanov  1 , Aleksandra S Novikova  2 , Marina V Zhurina  1 , Vladimir K Plakunov  1 , Andrei V Gannesen  1
Affiliations

A-Type Natriuretic Peptide Alters the Impact of Azithromycin on Planktonic Culture and on (Monospecies and Binary) Biofilms of Skin Bacteria Kytococcus schroeteri and Staphylococcus aureus

Ekaterina V Diuvenji et al. Microorganisms. .

Abstract

It has been established that the human atrial natriuretic peptide is able to alter the effect of azithromycin on Kytococcus schroeteri H01 and Staphylococcus aureus 209P monospecies and binary biofilms. The effect of the hormone depends on the surface type and cultivation system, and it may have both enhancing and counteracting effects. The antagonistic effect of the hormone was observed mostly on hydrophobic surfaces, whereas the additive effect was observed on hydrophilic surfaces like glass. Also, the effect of the hormone depends on the antibiotic concentration and bacterial species. The combination of azithromycin and ANP led to an amplification of cell aggregation in biofilms, to the potential increase in matrix synthesis, and to a decrease in S. aureus in the binary community. Also, ANP, azithromycin, and their combinations caused the differential expression of genes of resistance to different antibiotics, like macrolides (mostly increasing expression in kytococci), fluoroquinolones, aminoglycosides, and others, in both bacteria.

Keywords: Kytococcus schroeteri; Staphylococcus aureus; antibiotics; atrial natriuretic peptides; azithromycin; biofilms; hormones; human skin microbiota; multispecies biofilms.

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Conflict of interest statement

Miss Aleksandra S. Novikova as an employee of LLC “Bavar+” on behalf of LLC “Bavar+” declares no conflict of interests. Other academic authors declare no conflicts of interests.

Figures

Figure 1
Figure 1
Effects of different azithromycin concentrations on S. aureus planktonic cultures (A,C,E) and biofilms on the PTFE cubes (B,D,F) after 24 h (A,B), 48 h (C,D), and 72 h (E,F) of cultivation. Yellow dotted lines mean 100% level; *: p < 0.05; **: p < 0.01; ***: p < 0.001.
Figure 2
Figure 2
Effects of different azithromycin concentrations on K. schroeteri planktonic cultures (A,C,E), and biofilms on the PTFE cubes (B,D,F), after 24 h (A,B), 48 h (C,D), and 72 h (E,F) of cultivation. Yellow dotted lines mean 100% level; *: p < 0.05; **: p < 0.01; ***: p < 0.001.
Figure 3
Figure 3
Effect of combinations of azithromycin and ANP on planktonic cultures (A,C) and biofilms (B,D) on the PTFE cubes of K. schroeteri (A,B) and S. aureus (C,D). Red dotted lines mean 100% levels. *: p < 0.05; **: p < 0.01; ***: p < 0.001.
Figure 4
Figure 4
CFU counts in biofilms cultivated on the GMFF on the solid RCM medium, in the presence of active compounds and their combinations. (A) Number of CFUs of K. schroeteri in monospecies biofilms; (B) number of CFUs of K. schroeteri in binary biofilms; (C) number of CFUs of S. aureus in monospecies biofilms; and (D) number of CFUs of S. aureus in binary biofilms. *: p < 0.05; ***: p < 0.001.
Figure 5
Figure 5
CFU counts in biofilms cultivated on the GMFF in liquid RCM medium in the presence of active compounds and their combinations. (A) Number of CFUs of K. schroeteri in monospecies biofilms; (B) number of CFUs of S. aureus in monospecies biofilms; and (C) number of CFUs of S. aureus in binary biofilms. *: p < 0.05; ***: p < 0.001.
Figure 6
Figure 6
The MTT staining of biofilms cultivated on the solid (A–C) and in the liquid (D–F) RCM medium in the presence of active compounds and their combinations. (A,D): monospecies K. schroeteri biofilms; (B,E): monospecies S. aureus biofilms; (C,F): binary biofilms. *: p < 0.05.
Figure 7
Figure 7
Cell aggregate size (A,C,E) and percentage of aggregates (B,D,F) in monospecies biofilms of K. schroeteri (A,B), S. aureus (C,D), and binary biofilms (E,F) cultivated on the solid RCM medium in the presence of active compounds and their combinations. *: p < 0.05; **: p < 0.01; ***: p < 0.001.
Figure 8
Figure 8
Cell aggregate size (A,C,E) and percentage of aggregates (B,D,F) in monospecies biofilms of K. schroeteri (A,B), S. aureus (C,D), and binary biofilms (E,F) cultivated in liquid RCM medium in the presence of active compounds and their combinations. *: p < 0.05; **: p < 0.01.
Figure 9
Figure 9
Processing CLSM images. Biomass density of monospecies and binary biofilms of K. schroeteri and S. aureus stained with SYTO9 Green (A,D); monospecies and binary biofilms where S. aureus was labeled with R6G using FISH (B,E); and ratio of S. aureus and K. schroeteri in binary biofilms (C,F). *: p < 0.05; **: p < 0.01.
Figure 10
Figure 10
CLSM image processing. The total pixel volume of the monospecies and binary biofilms of K. schroeteri and S. aureus stained with SYTO9 green (A,D); monospecies and binary biofilms where S. aureus was labeled with R6G using FISH (B,E); ratio of S. aureus to K. schroeteri in binary biofilms (C,F). *: p < 0.05; **: p < 0.01; ***: p < 0.001.
Figure 11
Figure 11
Kinetic curves of monospecies (A–D) of K. schroeteri (A,B), S. aureus (C,D), and binary (E,F) cultures grown in the system without the forced initial adhesion step (A,C,E) and in the system with forced initial adhesion (B,D,F).
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