The effects of dopamine at physiological concentration on the growth and biofilm formation of Staphylococcus aureus, Staphylococcus epidermidis, and Escherichia coli

Anissa Febrianti, Endry Nugroho Prasetyo, Enny Zulaika, Arif Luqman, DOI: 10.46793/BiolNyss.16.1.21F

Abstract


Iron is an essential macronutrient for almost all living organisms, including pathogenic bacteria. Pathogenic bacteria have developed iron acquisition mechanisms due to the low bioavailability of iron inside the host. One of them is ability to utilize dopamine as a xenosiderophore. In this study we investigated the effects of dopamine at physiological concentrations (0.1–2 μM) on the growth and biofilm formation of bacteria grown in iron-limited and iron-enriched media. The significant growth enhancement was observed in Staphylococcus aureus USA300 grown in iron-enriched media. Dopamine at the concentration of 1 μM increased biofilm formation in S. aureus USA300, Staphylococcus epidermidis O47, and Escherichia coli K12 in both iron-limited and iron-enriched media after 3 days of incubation. These findings provide an insight into the effects of dopamine on bacteria at the physiological concentrations.


Keywords


dopamine, siderophore, biofilm, bacteria, microorganisms

Full Text:

PDF

References


Avidan, O., Satanower, S., & Banin, E. (2010). Iron and Bacterial Biofilm Development. In: J. Seckbach & A. Oren (Eds.), Microbial Mats: Modern and Ancient Microorganisms in Stratified Systems (pp. 359-383). Netherlands: Springer. https://doi.org/10.1007/978-90-481-3799-2_19

Blake, R.C., Shute, E.A., Greenwood, M.M., Spencer, G.H., & Ingledew, W.J. (1993). Enzymes of aerobic respiration on iron. FEMS Microbiology Reviews, 11(1-3), 9-18. https://doi.org/10.1111/j.1574-6976.1993.tb00261.x

Bullen, J.J. (1981). The significance of iron in infection. Reviews of Infectious Diseases, 3(6), 1127-1138. https://doi.org/10.1093/clinids/3.6.1127

Dey, P. & Ray Chaudhuri, S. (2023). The opportunistic nature of gut commensal microbiota. Critical Reviews in Microbiology, 49(6), 739-763. https://doi.org/10.1080/1040841X.2022.2133987

Dichtl, S., Demetz, E., Haschka, D., Tymoszuk, P., Petzer, V., Nairz, M., Seifert, M., Hoffmann, A., Brigo, N., Wurzner, R., Theurl, I., Karlinsey, J.E., Fang, F.C., & Weiss, G. (2019). Dopamine Is a Siderophore-Like Iron Chelator That Promotes Salmonella enterica Serovar Typhimurium Virulence in Mice. mBio, 10(1). https://doi.org/10.1128/mBio.02624-18

Ellermann, M. & Arthur, J.C. (2017). Siderophore-mediated iron acquisition and modulation of host-bacterial interactions. Free Radical Biology and Medicine, 105, 68-78. https://doi.org/10.1016/j.freeradbiomed.2016.10.489

Endicott, N.P., Lee, E., & Wencewicz, T.A. (2017). Structural Basis for Xenosiderophore Utilization by the Human Pathogen Staphylococcus aureus. ACS Infectious Diseases, 3(7), 542-553. https://doi.org/10.1021/acsinfecdis.7b00036

Escobar-Paramo, P., Grenet, K., Le Menac'h, A., Rode, L., Salgado, E., Amorin, C., Gouriou, S., Picard, B., Rahimy, M.C., Andremont, A., Denamur, E., & Ruimy, R. (2004). Large-scale population structure of human commensal Escherichia coli isolates. Applied and Environmental Biology, 70(9), 5698-5700. https://doi.org/10.1128/AEM.70.9.5698-5700.2004

Garcia, E.C., Brumbaugh, A.R., & Mobley, H.L. (2011). Redundancy and specificity of Escherichia coli iron acquisition systems during urinary tract infection. Infection and Immunity, 79(3), 1225–1235. https://doi.org/10.1128/IAI.01222-10

Garenaux, A., Caza, M., & Dozois, C.M. (2011). The ins and outs of siderophore-mediated iron uptake by extra-intestinal pathogenic Escherichia coli. Veterinary Microbiology, 153(1–2), 89–98. https://doi.org/10.1016/j.vetmic.2011.05.023

Greenberg, E.P., & Banin, E. (2008). Ironing out the biofilm problem: The role of iron in biofilm formation. In N. Balaban (Ed.), Control of Biofilm Infections by Signal Manipulation (pp. 141–156). Berlin, Heidelberg: Springer. https://doi.org/10.1007/7142_2007_014

Gu, S., Wan, W., Shao, Z., & Zhong, W. (2021). High-throughput method for detecting siderophore production by rhizosphere bacteria. BioProtocol, 11(9), e4001. https://doi.org/10.21769/BioProtoc.4001

Hammer, N.D., & Skaar, E.P. (2011). Molecular mechanisms of Staphylococcus aureus iron acquisition. Annual Review of Microbiology, 65, 129–147. https://doi.org/10.1146/annurev-micro-090110-102851

Hanke, M.L., & Kielian, T. (2012). Deciphering mechanisms of staphylococcal biofilm evasion of host immunity. Frontiers in Cellular and Infection Microbiology, 2, 62. https://doi.org/10.3389/fcimb.2012.00062

Herlinger, E., Jameson, R.F., & Linert, W. (1995). Spontaneous autoxidation of dopamine. Journal of the Chemical Society, Perkin Transactions, 2(2), 259–263. https://doi.org/10.1039/P29950000259

Kramer, J., Ozkaya, O., & Kümmerli, R. (2020). Bacterial siderophores in community and host interactions. Nature Reviews Microbiology, 18(3), 152–163. https://doi.org/10.1038/s41579-019-0284-4

Krzyminiewski, R., Kruczynski, Z., Dobosz, B., Zajac, A., Mackiewicz, A., Leporowska, E., & Folwaczna, S. (2011). EPR study of iron ion complexes in human blood. Applied Magnetic Resonance, 40(3), 321–330. https://doi.org/10.1007/s00723-011-0219-3

Le, K.Y., Park, M.D., & Otto, M. (2018). Immune evasion mechanisms of Staphylococcus epidermidis biofilm infection. Frontiers in Microbiology, 9, 359. https://doi.org/10.3389/fmicb.2018.00359

Leventhal, G.E., Ackermann, M., & Schiessl, K.T. (2016). Benefits of siderophore release lie in mediating diffusion limitation at low iron solubility. BioRxiv, 093948. https://doi.org/10.1101/093948

Levi, S., & Rovida, E. (2009). The role of iron in mitochondrial function. Biochimica et Biophysica Acta, 1790(7), 629–636. https://doi.org/10.1016/j.bbagen.2008.09.008

Liu, X., & Liu, J. (2021). Biosensors and sensors for dopamine detection. VIEW, 2(1), 20200102. https://doi.org/10.1002/VIW.20200102

Luqman, A. (2023). The orchestra of human bacteriome by hormones. Microbial Pathogenesis, 180, 106125. https://doi.org/10.1016/j.micpath.2023.106125

Luqman, A., Muttaqin, M.Z., Yulaipi, S., Ebner, P., Matsuo, M., Zabel, S., Tribelli, P.M., Nieselt, K., Hidayati, D., & Götz, F. (2020). Trace amines produced by skin bacteria accelerate wound healing in mice. Communications Biology, 3(1), 277. https://doi.org/10.1038/s42003-020-1000-7

Luqman, A., Nega, M., Nguyen, M.T., Ebner, P., & Götz, F. (2018). SadA-expressing staphylococci in the human gut show increased cell adherence and internalization. Cell Reports, 22(2), 535–545. https://doi.org/10.1016/j.celrep.2017.12.058

Luqman, A., & Ohlsen, K. (2024). Adrenergic system: A gateway of reciprocal signaling between host and bacteria. Current Opinion in Endocrine and Metabolic Research, 35, 100523. https://doi.org/10.1016/j.coemr.2024.100523

Murakami, C., Tanaka, A.R., Sato, Y., Kimura, Y., & Morimoto, K. (2021). Easy detection of siderophore production in diluted growth media using an improved CAS reagent. Journal of Microbiological Methods, 189, 106310. https://doi.org/10.1016/j.mimet.2021.106310

O'Toole, G.A. (2011). Microtiter dish biofilm formation assay. Journal of Visualized Experiments, 47. https://doi.org/10.3791/2437

Oliveira, F., Franca, A., & Cerca, N. (2017). Staphylococcus epidermidis is largely dependent on iron availability to form biofilms. International Journal of Medical Microbiology, 307(8), 552–563. https://doi.org/10.1016/j.ijmm.2017.08.009

Otto, M. (2006). Bacterial evasion of antimicrobial peptides by biofilm formation. Current Topics in Microbiology and Immunology, 306, 251–258. https://doi.org/10.1007/3-540-29916-5_10

Otto, M. (2009). Staphylococcus epidermidis – the ‘accidental’ pathogen. Nature Reviews Microbiology, 7(8), 555–567. https://doi.org/10.1038/nrmicro2182

Perraud, Q., Kuhn, L., Fritsch, S., Graulier, G., Gasser, V., Normant, V., Hammann, P., & Schalk, I.J. (2022). Opportunistic use of catecholamine neurotransmitters as siderophores to access iron by Pseudomonas aeruginosa. Environmental Microbiology, 24(2), 878–893. https://doi.org/10.1111/1462-2920.15372

Porter, J., Arreguin, S., & Pierpont, C.G. (2010). Ferric iron complexes of dopamine and 5,6-dihydroxyindole with NTA, EDDA, and EDTA as ancillary ligands. Inorganica Chimica Acta, 363(12), 2800–2803. https://doi.org/10.1016/j.ica.2010.05.011

Puig, S., Ramos-Alonso, L., Romero, A.M., & Martinez-Pastor, M.T. (2017). The elemental role of iron in DNA synthesis and repair. Metallomics, 9(11), 1483–1500. https://doi.org/10.1039/c7mt00116a

Sanchez, C.J., Mende, K., Beckius, M.L., Akers, K.S., Romano, D.R., Wenke, J.C., & Murray, C.K. (2013). Biofilm formation by clinical isolates and the implications in chronic infections. BMC Infectious Diseases, 13, 47. https://doi.org/10.1186/1471-2334-13-47

Schiessl, K.T., Janssen, E.M., Kraemer, S.M., McNeill, K., & Ackermann, M. (2017). Magnitude and mechanism of siderophore-mediated competition at low iron solubility in the Pseudomonas aeruginosa pyochelin system. Frontiers in Microbiology, 8, 1964. https://doi.org/10.3389/fmicb.2017.01964

Schwyn, B., & Neilands, J.B. (1987). Universal chemical assay for the detection and determination of siderophores. Analytical Biochemistry, 160(1), 47–56. https://doi.org/10.1016/0003-2697(87)90612-9

Soto, S.M., Smithson, A., Horcajada, J.P., Martinez, J.A., Mensa, J.P., & Vila, J. (2006). Implication of biofilm formation in the persistence of urinary tract infection caused by uropathogenic Escherichia coli. Clinical Microbiology and Infection, 12(10), 1034–1036. https://doi.org/10.1111/j.1469-0691.2006.01543.x

Umek, N., Gersak, B., Vintar, N., Sostaric, M., & Mavri, J. (2018). Dopamine autoxidation is controlled by acidic pH. Frontiers in Molecular Neuroscience, 11, 467. https://doi.org/10.3389/fnmol.2018.00467

Vigani, G. & Murgia, I. (2018). Iron-Requiring Enzymes in the Spotlight of Oxygen. Trends in Plant Science, 23(10), 874-882. https://doi.org/10.1016/j.tplants.2018.07.005


Refbacks

  • There are currently no refbacks.