Acknowledgement
The authors would like to acknowledge the KU Research Professor Program of Konkuk University, Seoul, South Korea. This study was supported by the National Research Foundation of Korea (NRF) (NRF-2019R1F1A1058805, NRF-2019M3E6A1103979, 2021R1C1C2010609), and the Research Program to solve the social issues of the NRF funded by the Ministry of Science and ICT (2017M3A9E4077234). We thanks to Dr. Michael Otto. at Pathogen Molecular Genetics Section, Laboratory of Bacteriology, National Institute of Allergy and Infectious Diseases, U.S. National Institutes of Health, kindly giving us Staphylococcus aureus strains for our study.
References
- Gor V, Hoshi M, Takemura AJ, Higashide M, Romero VM, Ohniwa RL. 2021. Morikawa K: virulence reversion in Staphylococcus aureus. In: Multidisciplinary Digital Publishing Institute Proceedings: 2021. 24.
- Kim JS, Kim HS, Song W, Cho HC, Lee KM, Kim EC. 2004. Antimicrobial resistance profiles of Staphylococcus aureus isolated in 13 Korean hospitals. Korean J. Lab. Med. 24: 223-229.
- Abdalrahman LS, Stanley A, Wells H, Fakhr MK. 2015. Isolation, virulence, and antimicrobial resistance of methicillin-resistant Staphylococcus aureus (MRSA) and methicillin sensitive Staphylococcus aureus (MSSA) strains from Oklahoma retail poultry meats. Int. J. Environ. Res. Public Health 12: 6148-6161. https://doi.org/10.3390/ijerph120606148
- Gajdacs M. 2019. The continuing threat of methicillin-resistant Staphylococcus aureus. Antibiotics 8: 52. https://doi.org/10.3390/antibiotics8020052
- Omoshaba E, Ojo O, Oyekunle M, Sonibare A, Adebayo A. 2020. Methicillin-resistant Staphylococcus aureus (MRSA) isolated from raw milk and nasal swabs of small ruminants in Abeokuta, Nigeria. Trop. Anim. Health Prod. 52: 2599-2608. https://doi.org/10.1007/s11250-020-02301-x
- Ngassam Tchamba C, Duprez J-N, Lucas P, Blanchard Y, Boyen F, Haesebrouck F, et al. 2021. Comparison of the staphylococcal chromosome cassette (SCC) mec in methicillin-resistant Staphylococcus aureus (MRSA) and non-aureus staphylococci (MRNAS) from animals and humans. Antibiotics 10: 256. https://doi.org/10.3390/antibiotics10030256
- Cuny C, Wieler LH, Witte W. 2015. Livestock-associated MRSA: the impact on humans. Antibiotics 4: 521-543. https://doi.org/10.3390/antibiotics4040521
- Peng K-T, Huang T-Y, Chiang Y-C, Hsu Y-Y, Chuang F-Y, Lee C-W, et al. 2019. Comparison of methicillin-resistant Staphylococcus aureus isolates from cellulitis and from osteomyelitis in a Taiwan hospital, 2016-2018. J. Clin. Med. 8: 816. https://doi.org/10.3390/jcm8060816
- Cihalova K, Chudobova D, Michalek P, Moulick A, Guran R, Kopel P, et al. 2015. Staphylococcus aureus and MRSA growth and biofilm formation after treatment with antibiotics and SeNPs. Int. J. Mol. Sci 16: 24656-24672. https://doi.org/10.3390/ijms161024656
- Cheung GY, Wang R, Khan BA, Sturdevant DE, Otto M. 2011. Role of the accessory gene regulator agr in community-associated methicillin-resistant Staphylococcus aureus pathogenesis. Infect. Immun. 79: 1927-1935. https://doi.org/10.1128/IAI.00046-11
- Zhang J, Conly J, McClure J, Wu K, Petri B, Barber D, et al. 2021. A murine skin infection model capable of differentiating the dermatopathology of community-associated MRSA strain USA300 from other MRSA strains. Microorganisms 9: 287. https://doi.org/10.3390/microorganisms9020287
- Sahoo KC, Sahoo S, Marrone G, Pathak A, Lundborg CS, Tamhankar AJ. 2014. Climatic factors and community-Associated methicillin-resistant Staphylococcus aureus skin and soft-tissue infections-A time-series analysis study. Int. J. Environ. Res. Public Health 11: 8996-9007. https://doi.org/10.3390/ijerph110908996
- Kim D-r, Lee Y, Kim H-k, Kim W, Kim Y-G, Yang Y-H, et al. 2020. Phenol-soluble modulin-mediated aggregation of community-associated methicillin-resistant staphylococcus aureus in human cerebrospinal fluid. Cells 9: 788. https://doi.org/10.3390/cells9030788
- Barton M, Hawkes M, Moore D, Conly J, Nicolle L, Allen U, et al. 2006. Guidelines for the prevention and management of community-associated methicillin-resistant Staphylococcus aureus: a perspective for Canadian health care practitioners. Can. J. Infect. Dis. Med. Microbiol. 17(Suppl C): 4C-24C. https://doi.org/10.1155/2006/402361
- Jones MB, Montgomery CP, Boyle-Vavra S, Shatzkes K, Maybank R, Frank BC, et al. 2014. Genomic and transcriptomic differences in community acquired methicillin resistant Staphylococcus aureus USA300 and USA400 strains. BMC Genomics 15: 1145. https://doi.org/10.1186/1471-2164-15-1145
- Vornhagen J, Burnside K, Whidbey C, Berry J, Qin X, Rajagopal L. 2015. Kinase inhibitors that increase the sensitivity of methicillin resistant Staphylococcus aureus to β-lactam antibiotics. Pathogens 4: 708-721. https://doi.org/10.3390/pathogens4040708
- Zhang K, McClure J-A, Elsayed S, Louie T, Conly JM. 2005. Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. J. Clin. Microbiol. 43: 5026-5033. https://doi.org/10.1128/JCM.43.10.5026-5033.2005
- Kim J-S, Song W, Kim H-S, Cho HC, Lee KM, Choi M-S, Kim E-C. 2006. Association between the methicillin resistance of clinical isolates of Staphylococcus aureus, their staphylococcal cassette chromosome mec (SCCmec) subtype classification, and their toxin gene profiles. Diagn. Microbiol. Infect. Dis. 56: 289-295. https://doi.org/10.1016/j.diagmicrobio.2006.05.003
- Wang Y, Lin J, Zhang T, He S, Li Y, Zhang W, et al. 2020. Environmental contamination prevalence, antimicrobial resistance and molecular characteristics of methicillin-resistant Staphylococcus aureus and Staphylococcus epidermidis isolated from secondary schools in Guangzhou, China. Int. J. Environ. Res. Public Health 17: 623. https://doi.org/10.3390/ijerph17020623
- Lounsbury N, Reeber MG, Mina G, Chbib C. 2019. A mini-review on ceftaroline in bacteremia patients with methicillin-resistant Staphylococcus aureus (MRSA) infections. Antibiotics 8: 30. https://doi.org/10.3390/antibiotics8010030
- Montgomery CP, Boyle-Vavra S, Adem PV, Lee JC, Husain AN, Clasen J, et al. 2008. Comparison of virulence in community-associated methicillin-resistant Staphylococcus aureus pulsotypes USA300 and USA400 in a rat model of pneumonia. J. Infect. Dis. 198: 561-570. https://doi.org/10.1086/590157
- Montgomery CP, Boyle-Vavra S, Daum RS. 2010. Importance of the global regulators Agr and SaeRS in the pathogenesis of CA-MRSA USA300 infection. PLoS One 5: e15177. https://doi.org/10.1371/journal.pone.0015177
- Queck SY, Jameson-Lee M, Villaruz AE, Bach T-HL, Khan BA, Sturdevant DE, et al. 2008. RNAIII-independent target gene control by the agr quorum-sensing system: insight into the evolution of virulence regulation in Staphylococcus aureus. Mol. Cell 32: 150-158. https://doi.org/10.1016/j.molcel.2008.08.005
- Song H-S, Bhatia SK, Choi T-R, Gurav R, Kim HJ, Lee SM, et al. 2021. Increased antibiotic resistance of methicillin-resistant Staphylococcus aureus USA300 ∆psm mutants and a complementation study of ∆psm mutants using synthetic phenol-soluble modulins. 31: 115-122. https://doi.org/10.4014/jmb.2007.07034
- Choi T-R, Song H-S, Han Y-H, Park Y-L, Park JY, Yang S-Y, et al. 2020. Enhanced tolerance to inhibitors of Escherichia coli by heterologous expression of cyclopropane-fatty acid-acyl-phospholipid synthase (cfa) from Halomonas socia. Bioprocess Biosys. Eng. 43: 909-918. https://doi.org/10.1007/s00449-020-02287-8
- Ike B, Ugwu MC, Ikegbunam MN, Nwobodo D, Ejikeugwu C, Gugu T, et al. 2016. Prevalence, antibiogram and molecular characterization of comunity-acquired methicillin-resistant Staphylococcus aureus in AWKA, Anambra Nigeria. Open Microbiol. J. 10: 211. https://doi.org/10.2174/1874285801610010211
- Pollitt EJ, Diggle SP. 2017. Defining motility in the Staphylococci. Cell. Mol. Life Sci. 74: 2943-2958. https://doi.org/10.1007/s00018-017-2507-z
- Tsompanidou E, Denham EL, Becher D, de Jong A, Buist G, van Oosten M, et al. 2013. Distinct roles of phenol-soluble modulins in spreading of Staphylococcus aureus on wet surfaces. Appl. Environ. Microbiol. 79: 886-895. https://doi.org/10.1128/AEM.03157-12
- Pollitt EJ, Crusz SA, Diggle SP. 2015. Staphylococcus aureus forms spreading dendrites that have characteristics of active motility. Sci. Rep. 5: 17698. https://doi.org/10.1038/srep17698
- Zhang J, Suo Y, Zhang D, Jin F, Zhao H, Shi C. 2018. Genetic and virulent difference between pigmented and non-pigmented Staphylococcus aureus. Front. Microbiol. 9: 598. https://doi.org/10.3389/fmicb.2018.00598
- Jusuf S, Hui J, Dong P-T, Cheng J-X. 2020. Staphyloxanthin photolysis potentiates low concentration silver nanoparticles in eradication of methicillin-resistant Staphylococcus aureus. J. Phys. Chem. 124: 5321-5330.
- Song H-S, Choi T-R, Han Y-H, Park Y-L, Park JY, Yang S-Y, et al. 2020. Increased resistance of a methicillin-resistant Staphylococcus aureus ∆ agr mutant with modified control in fatty acid metabolism. AMB Express 10: 64. https://doi.org/10.1186/s13568-020-01000-y
- Choi T-R, Park Y-L, Song H-S, Lee SM, Park SL, Lee HS, et al. 2020. Effects of a ∆-9-fatty acid desaturase and a cyclopropane-fatty acid synthase from the novel psychrophile Pseudomonas sp. B14-6 on bacterial membrane properties. J. Ind. Microbiol. Biotechnol. 47: 1045-1057. https://doi.org/10.1007/s10295-020-02333-0
- Bhatia SK, Kim J-H, Kim M-S, Kim J, Hong JW, Hong YG, 2018. Production of (3-hydroxybutyrate-co-3-hydroxyhexanoate) copolymer from coffee waste oil using engineered Ralstonia eutropha. Bioprocess Biosys. Eng. 41: 229-235. https://doi.org/10.1007/s00449-017-1861-4
- Hong Y-G, Moon Y-M, Hong J-W, Choi T-R, Jung H-R, Yang S-Y, et al. 2019. Discarded egg yolk as an alternate source of poly (3-hydroxybutyrate-co-3-hydroxyhexanoate). J. Microbiol. Biotechnol. 29: 382-391. https://doi.org/10.4014/jmb.1811.11028
- Song H-S, Bhatia SK, Gurav R, Choi T-R, Kim HJ, Park Y-L, et al. 2020. Naringenin as an antibacterial reagent controlling of biofilm formation and fatty acid metabolism in MRSA. bioRxiv. doi.org/10.1101/2020.03.08.983049.
- Royce LA, Liu P, Stebbins MJ, Hanson BC, Jarboe LR. 2013. The damaging effects of short chain fatty acids on Escherichia coli membranes. Appl. Microbiol. Biotechnol. 97: 8317-8327. https://doi.org/10.1007/s00253-013-5113-5
- Mykytczuk N, Trevors J, Leduc L, Ferroni G. 2007. Fluorescence polarization in studies of bacterial cytoplasmic membrane fluidity under environmental stress. Pro. Biophys. Mol. Biol. 95: 60-82. https://doi.org/10.1016/j.pbiomolbio.2007.05.001
- Dong PT, Mohammad H, Hui J, Leanse LG, Li J, Liang L, et al. 2019. Photolysis of Staphyloxanthin in methicillin-resistant Staphylococcus aureus potentiates killing by reactive oxygen species. Adv. Sci. 6: 1900030.
- AL-Kazaz EJ, Melconian AK, Kandela NJ. 2014. Extraction of staphyloxanthin from Staphylococcus aureus isolated from clinical sources to determine its antibacterial activity against other bacteria. Iraq J. Sci. 55: 1823-1832.
- Singh R, Ray P. 2014. Quorum sensing-mediated regulation of staphylococcal virulence and antibiotic resistance. Future Microbiol. 9: 669-681. https://doi.org/10.2217/fmb.14.31
- Grundstad ML, Parlet CP, Kwiecinski JM, Kavanaugh JS, Crosby HA, Cho Y-S, et al. 2019. Quorum sensing, virulence, and antibiotic resistance of USA100 methicillin-resistant Staphylococcus aureus isolates. mSphere 4: e00553-19.
- Beenken KE, Blevins JS, Smeltzer MS. 2003. Mutation of sarA in Staphylococcus aureus limits biofilm formation. Infect. Immun. 71: 4206-4211. https://doi.org/10.1128/IAI.71.7.4206-4211.2003
- Vuong C, Saenz HL, Gotz F, Otto M. 2000. Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus. J. Iinfect. Dis. 182: 1688-1693. https://doi.org/10.1086/317606
- Le KY, Villaruz AE, Zheng Y, He L, Fisher EL, Nguyen TH, et al. 2019. Role of phenol-soluble modulins in Staphylococcus epidermidis biofilm formation and infection of indwelling medical devices. J. Mol. Biol. 431: 3015-3027. https://doi.org/10.1016/j.jmb.2019.03.030
- Dong P-T, Mohammad H, Hui J, Wang X, Li J, Liang L, et al. 2018. Staphyloxanthin photobleaching sensitizes methicillin-resistant Staphylococcus aureus to reactive oxygen species attack. In: Light-Based Diagnosis and Treatment of Infectious Diseases: International Society for Optics and Photonics: 104790R. doi.org/10.1117/12.2291248.
- Pelz A, Wieland K-P, Putzbach K, Hentschel P, Albert K, Gotz F. 2005. Structure and biosynthesis of staphyloxanthin from Staphylococcus aureus. J. Biol. Chem. 280: 32493-32498. https://doi.org/10.1074/jbc.M505070200
- Mishra NN, Liu GY, Yeaman MR, Nast CC, Proctor RA, McKinnell J, 2011. Carotenoid-related alteration of cell membrane fluidity impacts Staphylococcus aureus susceptibility to host defense peptides. Antimicrob. Agents Chemother. 55: 526-531. https://doi.org/10.1128/AAC.00680-10
- Vila T, Kong EF, Ibrahim A, Piepenbrink K, Shetty AC, McCracken C, et al. 2019. Candida albicans quorum-sensing molecule farnesol modulates staphyloxanthin production and activates the thiol-based oxidative-stress response in Staphylococcus aureus. Virulence 10: 625-642. https://doi.org/10.1080/21505594.2019.1635418
- Wanner S, Schade J, Keinhorster D, Weller N, George SE, Kull L, et al. 2017. Wall teichoic acids mediate increased virulence in Staphylococcus aureus. Nat. Microbiol. 2: 16257. https://doi.org/10.1038/nmicrobiol.2016.257
- Rutherford ST, Bassler BL. 2012. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb. Perspect. Med. 2: a012427. https://doi.org/10.1101/cshperspect.a012427
- Bezar IF, Mashruwala AA, Boyd JM, Stock AM. 2019. Drug-like fragments inhibit agr-mediated virulence expression in Staphylococcus aureus. Sci. Rep. 9: 6786. https://doi.org/10.1038/s41598-019-42853-z
- Tan L, Li SR, Jiang B, Hu XM, Li S. 2018. Therapeutic targeting of the Staphylococcus aureus accessory gene regulator (agr) system. Front. Microbiol. 9: 55. https://doi.org/10.3389/fmicb.2018.00055
- Cosgriff CJ, White CR, Teoh WP, Grayczyk JP, Alonzo F. 2019. Control of Staphylococcus aureus quorum sensing by a membrane-embedded peptidase. Infect. Immun. 87: e00019-19.
- George SE, Hrubesch J, Breuing I, Vetter N, Korn N, Hennemann K, 2019. Oxidative stress drives the selection of quorum sensing mutants in the Staphylococcus aureus population. Proc. Natl. Acad. Sci. USA 116: 19145-19154. https://doi.org/10.1073/pnas.1902752116
- Regassa LB, Novick RP, Betley MJ. 1992. Glucose and nonmaintained pH decrease expression of the accessory gene regulator (agr) in Staphylococcus aureus. Infect. Immun. 60: 3381-3388. https://doi.org/10.1128/iai.60.8.3381-3388.1992
- Boles BR, Horswill AR. 2008. Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog. 4: e1000052. https://doi.org/10.1371/journal.ppat.1000052
- Croes S, Deurenberg RH, Boumans M-LL, Beisser PS, Neef C, Stobberingh EE. 2009. Staphylococcus aureus biofilm formation at the physiologic glucose concentration depends on the S. aureus lineage. BMC Microbiol. 9: 229. https://doi.org/10.1186/1471-2180-9-229