Menaquinone (Vitamin K2) Enhancement of Staphylococcus aureus Biofilm Formation
Affiliation(s)
Department of Microbiology and Immunology, Midwestern University, Downers Grove, USA.
Department of Microbiology and Immunology, Midwestern University, Downers Grove, USA.
ABSTRACT
During infection, Staphylococcus aureus is exposed to exogenous menaquinone which is essential for the human blood clotting cascade. The effect of exogenous menaquinone on S. aureus phenotypic expression is not known. To test whether menaquinone affects expression of virulence-associated phenotypes, methicillin-sensitive (MSSA) and -resistant (MRSA) S. aureus strains (n = 8) were grown in the presence of menaquinone (0.001 - 12 μg/ml). Capsule production, biofilm formation (plastic and fibronectin-coated microtiter plates) and carotenoid levels were determined spectrophotometrically after growth in Mueller Hinton broth (MH; 24-hr, 37°C). All experiments were, at minimum, done in triplicate and repeated twice. Menaquinone at physiologic levels (0.01 μg/ml MH) significantly increased (p < 0.05) biofilm formation on plastic in a manner that was bacterial population size dependent. In addition, menaquinone (0.05 - 4 μg/ml) significantly increased (p < 0.05) biofilm formation on fibronectin-coated surfaces for four MSSA strains and one MRSA strain by two to six-fold as compared to medium controls. However, menaquinone had no effect on capsule production or cell-associated carotenoid levels. Menaquinone’s effect on biofilm formation on fibronectin-coated surfaces appears to be regulated by sarA. These findings are the first to demonstrate that a vitamin at concentrations reported in humans affects S. aureus virulence-associated phenotypes.
KEYWORDS
Quorum; S. aureus; Menaquinone; Fibronectin; Biofilm; Capsule; Plastic; Adherence; Carotenoid
Quorum; S. aureus; Menaquinone; Fibronectin; Biofilm; Capsule; Plastic; Adherence; Carotenoid
Cite this paper
Kirby, D. , Savage, J. and Plotkin, B. (2014) Menaquinone (Vitamin K2) Enhancement of Staphylococcus aureus Biofilm Formation. Journal of Biosciences and Medicines, 2, 26-32. doi: 10.4236/jbm.2014.21004.
Kirby, D. , Savage, J. and Plotkin, B. (2014) Menaquinone (Vitamin K2) Enhancement of Staphylococcus aureus Biofilm Formation. Journal of Biosciences and Medicines, 2, 26-32. doi: 10.4236/jbm.2014.21004.
References
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http://dx.doi.org/10.1146/annurev-genet-102108-134304 [3] Lyte, M., Frank, C. and Green, B. (1996) Production of an Autoinducer of Growth by Norepinephrine Cultured Escherichia coli O157:H7. FEMS Microbiology Letters, 139, 155-159.
http://dx.doi.org/10.1111/j.1574-6968.1996.tb08196.x [4] Walters, M. and Sperandio, V. (2006) Autoinducer 3 and Epinephrine Signaling in the Kinetics of Locus of Enterocyte Effacement Gene Expression in Enterohemorrhagic Escherichia coli. Infection and Immunity, 74, 5445-5455.
http://dx.doi.org/10.1128/IAI.00099-06 [5] Plotkin, B. and Konaklieva, M. (2007) Possible Role of sarA in Dehydroepiandosterone (DHEA)—Mediated Increase in Staphylococcus aureus Resistance to Vancomycin. Chemo-therapy, 53, 181-184.
http://dx.doi.org/10.1159/000100863 [6] Klosowska, K. and Plotkin, B. (2006) Human Insulin Modulation of Escherichia coli Adherence and Chemotaxis. American Journal of Infectious Diseases, 2, 197-200.
http://dx.doi.org/10.3844/ajidsp.2006.197.200 [7] Plotkin, B.J. and Viselli, S.M. (2000) Effect of Insulin on Microbial Growth. Current Microbiology, 41, 60-64.
http://dx.doi.org/10.1007/s002840010092 [8] Thoendel, M. and Horswill, A. (2010) Biosynthesis of Peptide Signals in Gram-Positive Bacteria. Advances in Applied Microbiology, 71, 91-112.
http://dx.doi.org/10.1016/S0065-2164(10)71004-2 [9] Plotkin, B., Erickson, Q., Roose, R. and Viselli, S. (2003) Effect of Androgens and Glucocorticoids on Microbial Growth and Antimicrobial Susceptibility. Current Microbiology, 47, 514-520.
http://dx.doi.org/10.1007/s00284-003-4080-y [10] Sturme, M.H.J., Kleerebezem, M., Nakayama, J., Akkermans, A.D.L., Vaughan, E.E. and de Vos, W.M. (2002) Cell to Cell Communication by Autoinducing Peptides in Gram-Positive Bacteria. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology, 81, 233-243.
http://dx.doi.org/10.1023/A:1020522919555 [11] Harraghy, N., Kerdudou, S. and Herrmann, M. (2007) Quorum-Sensing Systems in Staphylococci as Therapeutic Targets. Analytical and Bioanalytical Chemistry, 387, 437-444.
http://dx.doi.org/10.1007/s00216-006-0860-0 [12] Bentley, R. and Meganathan, R. (1982) Biosynthesis of Vitamin K (Menaquinone) in Bacteria. Microbiological Reviews, 46, 241-280. [13] Tacconelli, E. (2009) Methicillin-Resistant Staphylococcus aureus: Source Control and Surveillance Organization. Clinical Microbiology and Infection, 15, 31-38.
http://dx.doi.org/10.1111/j.1469-0691.2009.03096.x [14] Oldenburg, J., Marinova, M., Muller-Reible, C. and Watzka, M. (2008) The Vitamin K Cycle. Vitamin Hormone, 78, 35-62.
http://dx.doi.org/10.1016/S0083-6729(07)00003-9 [15] Goldenbaum, P., Keyser, P. and White, D. (1975) Role of Vitamin K2 in the Organization and Function of Staphylococcus aureus Membranes. Journal of Bacteriology, 121, 442-449. [16] Meganathan, R. (2001) Ubiquinone Biosynthesis in Microorganisms. FEMS Microbiology Letters, 203, 131-139.
http://dx.doi.org/10.1111/j.1574-6968.2001.tb10831.x [17] Spronk, H.M.H., Soute, B.A.M., Schurgers, L.J., Thijssen, H.H.W., De Mey, J.G.R. and Vermeer, C. (2003) Tissue-Specific Utilization of Menaquinone-4 Results in the Prevention of Arterial Calcification in Warfarin-Treated Rats. Journal of Vascular Research, 40, 531-537.
http://dx.doi.org/10.1159/000075344 [18] Walther, B., Karl, J.P., Booth, S.L. and Boyaval, P. (2013) Menaquinones, Bacteria, and the Food Supply: The Relevance of Dairy and Fermented Food Products to Vitamin K Requirements. Advances in Nutrition, 4, 463-473.
http://dx.doi.org/10.3945/an.113.003855 [19] Plata, K., Rosato, A. and Wegrzyn, G. (2009) Staphylococcus aureus as an Infectious Agent: Overview of Biochemistry and Molecular Genetics of Its Pathogenicity. Acta Biochimica Polonica, 56, 597-612. [20] Kirby, D., Raino, C.J., Rabor Jr., S.F., Wasson, C.J. and Plotkin, B.J. (2012) Semi-Automated Method for Multi-Tasking Measurement of Microbial Growth, Capsule, and Biofilm Formation. Advances in Microbiology, 2, 623-628.
http://dx.doi.org/10.4236/aim.2012.24081 [21] Farzam, F. and Plotkin, B. (2001) Effect of Sub-MICs of Antibiotics on the Hydrophobicity and Production of Acidic Polysaccharide by Vibrio vulnificus. Chemotherapy, 47, 184-193.
http://dx.doi.org/10.1159/000063220 [22] McKinney, R.E. (1953) Staining Bacterial Polysaccharides. Journal of Bacteriology, 66, 453-454. [23] Morikawa, K., Maruyama, A., Inose, Y., Higashide, M., Hayashi, H. and Ohta, T. (2001) Overexpression of Sigma Factor B Urges Staphylococcus aureus to Thicken the Cell Wall and Resist Beta Lactams. Biochemical Biophysical Research Communications, 288, 385-389. [24] Chan, P. and Foster, S. (1998) Role of SarA in Virulence Determinant Production and Environmental Signal Transduction in Staphylococcus aureus. Journal of Bacteriology, 180, 6232-6241. [25] Novick, R., Ross, H., Projan, S., Kornblum, J., Kreiswirth, B. and Moghazeh, S. (1993) Synthesis of Staphylococcal Virulence Factors Is Controlled by a Regulatory RNA Molecule. The EMBO Journal, 12, 3967-3975. [26] Blevins, J., Beenken, K., Elasri, M., Hurlburt, B. and Smeltzer, M. (2002) Strain-Dependent Differences in the Regulatory Roles of sarA and agr in Staphylococcus aureus. Infection and Immunity, 70, 470-480.
http://dx.doi.org/10.1128/IAI.70.2.470-480.2002
[1] Plotkin, B. and Konaklieva, M. (2008) Inter-Kingdom Communication—The Host-Pathogen Communication Party Line. Current Trends in Microbiology, 4, 15-25. [2] Ng, W. and Bassler, B. (2009) Bacterial Quorum-Sensing Network Architectures. Annual Review of Genetics, 43, 197-222.
http://dx.doi.org/10.1146/annurev-genet-102108-134304 [3] Lyte, M., Frank, C. and Green, B. (1996) Production of an Autoinducer of Growth by Norepinephrine Cultured Escherichia coli O157:H7. FEMS Microbiology Letters, 139, 155-159.
http://dx.doi.org/10.1111/j.1574-6968.1996.tb08196.x [4] Walters, M. and Sperandio, V. (2006) Autoinducer 3 and Epinephrine Signaling in the Kinetics of Locus of Enterocyte Effacement Gene Expression in Enterohemorrhagic Escherichia coli. Infection and Immunity, 74, 5445-5455.
http://dx.doi.org/10.1128/IAI.00099-06 [5] Plotkin, B. and Konaklieva, M. (2007) Possible Role of sarA in Dehydroepiandosterone (DHEA)—Mediated Increase in Staphylococcus aureus Resistance to Vancomycin. Chemo-therapy, 53, 181-184.
http://dx.doi.org/10.1159/000100863 [6] Klosowska, K. and Plotkin, B. (2006) Human Insulin Modulation of Escherichia coli Adherence and Chemotaxis. American Journal of Infectious Diseases, 2, 197-200.
http://dx.doi.org/10.3844/ajidsp.2006.197.200 [7] Plotkin, B.J. and Viselli, S.M. (2000) Effect of Insulin on Microbial Growth. Current Microbiology, 41, 60-64.
http://dx.doi.org/10.1007/s002840010092 [8] Thoendel, M. and Horswill, A. (2010) Biosynthesis of Peptide Signals in Gram-Positive Bacteria. Advances in Applied Microbiology, 71, 91-112.
http://dx.doi.org/10.1016/S0065-2164(10)71004-2 [9] Plotkin, B., Erickson, Q., Roose, R. and Viselli, S. (2003) Effect of Androgens and Glucocorticoids on Microbial Growth and Antimicrobial Susceptibility. Current Microbiology, 47, 514-520.
http://dx.doi.org/10.1007/s00284-003-4080-y [10] Sturme, M.H.J., Kleerebezem, M., Nakayama, J., Akkermans, A.D.L., Vaughan, E.E. and de Vos, W.M. (2002) Cell to Cell Communication by Autoinducing Peptides in Gram-Positive Bacteria. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology, 81, 233-243.
http://dx.doi.org/10.1023/A:1020522919555 [11] Harraghy, N., Kerdudou, S. and Herrmann, M. (2007) Quorum-Sensing Systems in Staphylococci as Therapeutic Targets. Analytical and Bioanalytical Chemistry, 387, 437-444.
http://dx.doi.org/10.1007/s00216-006-0860-0 [12] Bentley, R. and Meganathan, R. (1982) Biosynthesis of Vitamin K (Menaquinone) in Bacteria. Microbiological Reviews, 46, 241-280. [13] Tacconelli, E. (2009) Methicillin-Resistant Staphylococcus aureus: Source Control and Surveillance Organization. Clinical Microbiology and Infection, 15, 31-38.
http://dx.doi.org/10.1111/j.1469-0691.2009.03096.x [14] Oldenburg, J., Marinova, M., Muller-Reible, C. and Watzka, M. (2008) The Vitamin K Cycle. Vitamin Hormone, 78, 35-62.
http://dx.doi.org/10.1016/S0083-6729(07)00003-9 [15] Goldenbaum, P., Keyser, P. and White, D. (1975) Role of Vitamin K2 in the Organization and Function of Staphylococcus aureus Membranes. Journal of Bacteriology, 121, 442-449. [16] Meganathan, R. (2001) Ubiquinone Biosynthesis in Microorganisms. FEMS Microbiology Letters, 203, 131-139.
http://dx.doi.org/10.1111/j.1574-6968.2001.tb10831.x [17] Spronk, H.M.H., Soute, B.A.M., Schurgers, L.J., Thijssen, H.H.W., De Mey, J.G.R. and Vermeer, C. (2003) Tissue-Specific Utilization of Menaquinone-4 Results in the Prevention of Arterial Calcification in Warfarin-Treated Rats. Journal of Vascular Research, 40, 531-537.
http://dx.doi.org/10.1159/000075344 [18] Walther, B., Karl, J.P., Booth, S.L. and Boyaval, P. (2013) Menaquinones, Bacteria, and the Food Supply: The Relevance of Dairy and Fermented Food Products to Vitamin K Requirements. Advances in Nutrition, 4, 463-473.
http://dx.doi.org/10.3945/an.113.003855 [19] Plata, K., Rosato, A. and Wegrzyn, G. (2009) Staphylococcus aureus as an Infectious Agent: Overview of Biochemistry and Molecular Genetics of Its Pathogenicity. Acta Biochimica Polonica, 56, 597-612. [20] Kirby, D., Raino, C.J., Rabor Jr., S.F., Wasson, C.J. and Plotkin, B.J. (2012) Semi-Automated Method for Multi-Tasking Measurement of Microbial Growth, Capsule, and Biofilm Formation. Advances in Microbiology, 2, 623-628.
http://dx.doi.org/10.4236/aim.2012.24081 [21] Farzam, F. and Plotkin, B. (2001) Effect of Sub-MICs of Antibiotics on the Hydrophobicity and Production of Acidic Polysaccharide by Vibrio vulnificus. Chemotherapy, 47, 184-193.
http://dx.doi.org/10.1159/000063220 [22] McKinney, R.E. (1953) Staining Bacterial Polysaccharides. Journal of Bacteriology, 66, 453-454. [23] Morikawa, K., Maruyama, A., Inose, Y., Higashide, M., Hayashi, H. and Ohta, T. (2001) Overexpression of Sigma Factor B Urges Staphylococcus aureus to Thicken the Cell Wall and Resist Beta Lactams. Biochemical Biophysical Research Communications, 288, 385-389. [24] Chan, P. and Foster, S. (1998) Role of SarA in Virulence Determinant Production and Environmental Signal Transduction in Staphylococcus aureus. Journal of Bacteriology, 180, 6232-6241. [25] Novick, R., Ross, H., Projan, S., Kornblum, J., Kreiswirth, B. and Moghazeh, S. (1993) Synthesis of Staphylococcal Virulence Factors Is Controlled by a Regulatory RNA Molecule. The EMBO Journal, 12, 3967-3975. [26] Blevins, J., Beenken, K., Elasri, M., Hurlburt, B. and Smeltzer, M. (2002) Strain-Dependent Differences in the Regulatory Roles of sarA and agr in Staphylococcus aureus. Infection and Immunity, 70, 470-480.
http://dx.doi.org/10.1128/IAI.70.2.470-480.2002