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Pseudomonas aeruginosa and Pyoverdines: A Hidden Threat in Apitherapy Applications

Year 2022, , 315 - 324, 08.03.2022
https://doi.org/10.47495/okufbed.1050755

Abstract

Pseudomonas aeruginosa, a Gram-negative rod-shape bacterium, is one of the most common pathogens in nosocomial infections and this pathogenic species draws attention with its high prevalence rate in patients with septicemia. Pyoverdines are fluorescent siderophore produced by some Pseudomonas species such as P. aeruginosa and Pseudomonas fluorescens. These siderophores support biofilm production in these microorganisms and also plays a role as a virulence factor. In this study, anti-Pseudomonas activity of 10 different honey samples was evaluated by agar well diffusion (AWD) method. In addition, minimum inhibition concentration (MIC) and minimum bactericidal concentration (MBC) values of these honey samples were determined via microbroth dilution method. The obtained results showed that only oak honey and chestnut honey have negligible scale low anti-Pseudomonas activity. In addition, it was observed that other honey samples did not have an inhibitory effect against these pathogens. Finally, the promoting property of pyoverdine siderophore production of these honey samples was evaluated and it was concluded that all honey samples stimulated pyoverdin production at a concentration ½ w/v.

References

  • Albelda-Berenguer M., Monachon M., Joseph E. Siderophores: From natural roles to potential applications. Advances in applied microbiology, 2019; 106, 193-225.
  • Anand S., Deighton M., Livanos G., Morrison PD., Pang EC., Mantri N. Antimicrobial activity of Agastache honey and characterization of its bioactive compounds in comparison with important commercial honeys. Frontiers in microbiology 2019; 10, 263.
  • Bayram NE., Canli D., Gercek YC., Bayram S., Celik S., Güzel F., Oz, GC. Macronutrient and micronutrient levels and phenolic compound characteristics of monofloral honey samples. Journal of Food & Nutrition Research 2020; 59(4).
  • Bayram N., Yüzer MO., Bayram S. Melissopalynology analysis, physicochemical properties, multi-element content and antimicrobial activity of honey samples collected from Bayburt, Turkey. Uludağ Arıcılık Dergisi 2019; 19(2): 161-176.
  • Casabona MG., Vandenbrouck Y., Attree I., Couté Y. Proteomic characterization of Pseudomonas aeruginosa PAO1 inner membrane. Proteomics 2013; 13(16): 2419-2423.
  • Castañeda-Montes FJ., Avitia M., Sepúlveda-Robles O., Cruz-Sánchez V., Kameyama L., Guarneros G., Escalante AE. Population structure of Pseudomonas aeruginosa through a MLST approach and antibiotic resistance profiling of a Mexican clinical collection. Infection, Genetics and Evolution 2018; 65: 43-54.
  • Cézard C., Sonnet P., Bouvier B. Ironing out pyoverdine’s chromophore structure: serendipity or design?. JBIC Journal of Biological Inorganic Chemistry 2019; 24(5), 659-673. https://doi.org/10.1007/s00775-019-01678-x
  • da Silva PM., Gauche C., Gonzaga LV., Costa ACO., Fett R. Honey: Chemical composition, stability and authenticity. Food chemistry 2016; 196: 309-323.
  • Dryden M., Lockyer G., Saeed K., Cooke J. Engineered honey: in vitro antimicrobial activity of a novel topical wound care treatment. Journal of global antimicrobial resistance 2014; 2(3): 168-172.
  • Esparcia A., Madrazo M., Alberola J., López‐Cruz I., Eiros JM., Nogueira JM., Artero A. Community‐onset Pseudomonas aeruginosa urinary sepsis in elderly people: Predictive factors, adequacy of empirical therapy and outcomes. International journal of clinical practice 2019; 73(12): e13425.
  • Ecem-Bayram N., Çebi N., Çelik S., Gerçek YC., Bayram S., Tanuğur-Samancı AE., Özkök A. Turkish royal jelly: amino acid, physicochemical, antioxidant, multi-elemental, antibacterial and fingerprint profiles by analytical techniques combined with chemometrics. Journal of Apicultural Research 2021; 60,5: 751-764.
  • Hadagali MD., Chua LS. The anti-inflammatory and wound healing properties of honey. European Food Research and Technology 2014; 239(6): 1003-1014.
  • Huttunen S., Riihinen K., Kauhanen J., Tikkanen‐Kaukanen C. Antimicrobial activity of different Finnish monofloral honeys against human pathogenic bacteria. Apmis 2013; 121(9): 827-834.
  • Karlıdağ S., Keskin M., Bayram S., Mayda N., Özkök A. Honey: Determination of volatile compounds, antioxidant and antibacterial activities. Czech Journal of Food Sciences 2021; 39(3): 208–216
  • Leyva-Jimenez FJ., Lozano-Sanchez J., Borras-Linares I., de la Luz Cadiz-Gurrea M., Mahmoodi-Khaledi E. Potential antimicrobial activity of honey phenolic compounds against Gram positive and Gram negative bacteria. LWT 2019; 101: 236-245.
  • Matos ECOD., Andriolo RB., Rodrigues YC., Lima PDLD., Carneiro ICDRS., Lima KVB. Mortality in patients with multidrug-resistant Pseudomonas aeruginosa infections: a meta-analysis. Revista da Sociedade Brasileira de Medicina Tropical 2018; 51, 415-420.
  • Moll H., Johnsson A., Schäfer M., Pedersen K., Budzikiewicz H., Bernhard G. Curium (III) complexation with pyoverdins secreted by a groundwater strain of Pseudomonas fluorescens. Biometals, 2008; 21(2), 219-228. https://doi.org/10.1007/s10534-007-9111-x
  • Nikolaidis M., Mossialos D., Oliver SG., Amoutzias GD. Comparative analysis of the core proteomes among the Pseudomonas major evolutionary groups reveals species-specific adaptations for Pseudomonas aeruginosa and Pseudomonas chlororaphis. Diversity 2020; 12(8): 289.
  • Olatunji KT., Aboh M., Oladosu P. In-Vitro Antimicrobial Effect of Different Honey Samples against Selected Micro-organisms Marketed in Abuja Nigeria. Journal of Applied Life Sciences International 2018; 1-7.
  • Oluwapelumi OB., Morayo A., Buru AS., Richard AY., Funmilayo AJ., Funmi AA. Antimicrobial Activities of Different Honeys Sold in Ado-Ekiti on Bacteria Associated with Upper Respiratory Tract Infections. International Journal of Current Microbiology and Applied Sciences 2017; 6(2): 1-10.
  • Oryan A., Alemzadeh E., Moshiri A. Biological properties and therapeutic activities of honey in wound healing: A narrative review and meta-analysis. Journal of tissue viability 2016; 25(2): 98-118.
  • Osés SM., Pascual-Maté A., de la Fuente D., de Pablo A., Fernández-Muiño MA., Sancho MT. Comparison of methods to determine antibacterial activity of honeys against Staphylococcus aureus. NJAS-Wageningen Journal of Life Sciences 2016; 78: 29-33. DOI: 10.1016/j.njas.2015.12.005.
  • Pecoraro L., Wang X., Shah D., Song X., Kumar V., Shakoor A., Rani R. Biosynthesis Pathways, Transport Mechanisms and Biotechnological Applications of Fungal Siderophores. Journal of Fungi 2022; 8(1): 21. https://doi.org/10.3390/jof8010021
  • Peix A., Ramírez-Bahena MH., Velázquez E. The current status on the taxonomy of Pseudomonas revisited: an update. Infection, Genetics and Evolution 2018; 57: 106-116.
  • Ringel MT., Brüser T. The biosynthesis of pyoverdines. Microbial cell 2018; 5(10): 424.
  • Ronsisvalle S., Lissandrello E., Fuochi V., Petronio-Petronio G., Straquadanio C., Crascì L., Furneri PM Antioxidant and antimicrobial properties of Casteanea sativa Miller chestnut honey produced on Mount Etna (Sicily). Natural product research 2019; 33(6): 843-850.
  • Sherlock O., Dolan A., Athman R., Power A., Gethin G., Cowman S., Humphreys H. Comparison of the antimicrobial activity of Ulmo honey from Chile and Manuka honey against methicillin-resistant Staphylococcus aureus, Escherichia coli and Pseudomonas aeruginosa. BMC complementary and alternative medicine 2010; 10(1): 1-5.
  • Silby MW., Winstanley C., Godfrey SA., Levy SB., Jackson RW. Pseudomonas genomes: diverse and adaptable. FEMS microbiology reviews 2011; 35(4): 652-680.
  • Vică ML., Glevitzky M., Tit DM., Behl T., Heghedűş-Mîndru RC., Zaha DC., Bungău S. The antimicrobial activity of honey and propolis extracts from the central region of Romania. Food Bioscience 2021; 41: 101014.
  • Zavascki AP., Barth AL., Gonçalves ALS., Moro ALD., Fernandes JF., Martins AF., Goldani LZ. The influence of metallo-β-lactamase production on mortality in nosocomial Pseudomonas aeruginosa infections. Journal of Antimicrobial Chemotherapy 2006; 58(2): 387-392.

Pseudomonas aeruginosa ve Pyoverdinler: Apiterapi Uygulamalarında Gizli bir Tehdit

Year 2022, , 315 - 324, 08.03.2022
https://doi.org/10.47495/okufbed.1050755

Abstract

Gram negatif çubuk şeklinde bir bakteri olan Pseudomonas aeruginosa, hastane enfeksiyonlarında en sık görülen patojenlerden biridir ve bu patojenik tür, septisemili hastalarda yüksek prevalansı ile dikkat çekmektedir. Pyoverdinler, P. aeruginosa ve Pseudomonas fluorescens gibi bazı Pseudomonas türleri tarafından üretilen floresan sideroforlardır. Bu sideroforlar, bu mikroorganizmalarda biyofilm üretimini destekler ve aynı zamanda bir virülans faktörü olarak rol oynar. Bu çalışmada 10 farklı bal örneğinin anti-Pseudomonas aktivitesi agar kuyusu difüzyon (AWD) yöntemi ile değerlendirilmiştir. Ayrıca bu bal örneklerinin minimum inhibisyon konsantrasyonu (MIC) ve minimum bakterisidal konsantrasyon (MBC) değerleri mikrobroth seyreltme yöntemi ile belirlenmiştir. Elde edilen sonuçlar sadece meşe balı ve kestane balının ihmal edilebilir ölçekte düşük anti-Pseudomonas aktivitesine sahip olduğunu göstermiştir. Ayrıca diğer bal örneklerinin bu patojenlere karşı inhibitör etkisinin olmadığı gözlemlenmiştir. Son olarak, bu bal örneklerinin pyoverdin siderofor üretimini teşvik edici özelliği değerlendirilmiş ve tüm bal örneklerinin ½ w/v konsantrasyonda pyoverdin üretimini uyardığı sonucuna varılmıştır.

References

  • Albelda-Berenguer M., Monachon M., Joseph E. Siderophores: From natural roles to potential applications. Advances in applied microbiology, 2019; 106, 193-225.
  • Anand S., Deighton M., Livanos G., Morrison PD., Pang EC., Mantri N. Antimicrobial activity of Agastache honey and characterization of its bioactive compounds in comparison with important commercial honeys. Frontiers in microbiology 2019; 10, 263.
  • Bayram NE., Canli D., Gercek YC., Bayram S., Celik S., Güzel F., Oz, GC. Macronutrient and micronutrient levels and phenolic compound characteristics of monofloral honey samples. Journal of Food & Nutrition Research 2020; 59(4).
  • Bayram N., Yüzer MO., Bayram S. Melissopalynology analysis, physicochemical properties, multi-element content and antimicrobial activity of honey samples collected from Bayburt, Turkey. Uludağ Arıcılık Dergisi 2019; 19(2): 161-176.
  • Casabona MG., Vandenbrouck Y., Attree I., Couté Y. Proteomic characterization of Pseudomonas aeruginosa PAO1 inner membrane. Proteomics 2013; 13(16): 2419-2423.
  • Castañeda-Montes FJ., Avitia M., Sepúlveda-Robles O., Cruz-Sánchez V., Kameyama L., Guarneros G., Escalante AE. Population structure of Pseudomonas aeruginosa through a MLST approach and antibiotic resistance profiling of a Mexican clinical collection. Infection, Genetics and Evolution 2018; 65: 43-54.
  • Cézard C., Sonnet P., Bouvier B. Ironing out pyoverdine’s chromophore structure: serendipity or design?. JBIC Journal of Biological Inorganic Chemistry 2019; 24(5), 659-673. https://doi.org/10.1007/s00775-019-01678-x
  • da Silva PM., Gauche C., Gonzaga LV., Costa ACO., Fett R. Honey: Chemical composition, stability and authenticity. Food chemistry 2016; 196: 309-323.
  • Dryden M., Lockyer G., Saeed K., Cooke J. Engineered honey: in vitro antimicrobial activity of a novel topical wound care treatment. Journal of global antimicrobial resistance 2014; 2(3): 168-172.
  • Esparcia A., Madrazo M., Alberola J., López‐Cruz I., Eiros JM., Nogueira JM., Artero A. Community‐onset Pseudomonas aeruginosa urinary sepsis in elderly people: Predictive factors, adequacy of empirical therapy and outcomes. International journal of clinical practice 2019; 73(12): e13425.
  • Ecem-Bayram N., Çebi N., Çelik S., Gerçek YC., Bayram S., Tanuğur-Samancı AE., Özkök A. Turkish royal jelly: amino acid, physicochemical, antioxidant, multi-elemental, antibacterial and fingerprint profiles by analytical techniques combined with chemometrics. Journal of Apicultural Research 2021; 60,5: 751-764.
  • Hadagali MD., Chua LS. The anti-inflammatory and wound healing properties of honey. European Food Research and Technology 2014; 239(6): 1003-1014.
  • Huttunen S., Riihinen K., Kauhanen J., Tikkanen‐Kaukanen C. Antimicrobial activity of different Finnish monofloral honeys against human pathogenic bacteria. Apmis 2013; 121(9): 827-834.
  • Karlıdağ S., Keskin M., Bayram S., Mayda N., Özkök A. Honey: Determination of volatile compounds, antioxidant and antibacterial activities. Czech Journal of Food Sciences 2021; 39(3): 208–216
  • Leyva-Jimenez FJ., Lozano-Sanchez J., Borras-Linares I., de la Luz Cadiz-Gurrea M., Mahmoodi-Khaledi E. Potential antimicrobial activity of honey phenolic compounds against Gram positive and Gram negative bacteria. LWT 2019; 101: 236-245.
  • Matos ECOD., Andriolo RB., Rodrigues YC., Lima PDLD., Carneiro ICDRS., Lima KVB. Mortality in patients with multidrug-resistant Pseudomonas aeruginosa infections: a meta-analysis. Revista da Sociedade Brasileira de Medicina Tropical 2018; 51, 415-420.
  • Moll H., Johnsson A., Schäfer M., Pedersen K., Budzikiewicz H., Bernhard G. Curium (III) complexation with pyoverdins secreted by a groundwater strain of Pseudomonas fluorescens. Biometals, 2008; 21(2), 219-228. https://doi.org/10.1007/s10534-007-9111-x
  • Nikolaidis M., Mossialos D., Oliver SG., Amoutzias GD. Comparative analysis of the core proteomes among the Pseudomonas major evolutionary groups reveals species-specific adaptations for Pseudomonas aeruginosa and Pseudomonas chlororaphis. Diversity 2020; 12(8): 289.
  • Olatunji KT., Aboh M., Oladosu P. In-Vitro Antimicrobial Effect of Different Honey Samples against Selected Micro-organisms Marketed in Abuja Nigeria. Journal of Applied Life Sciences International 2018; 1-7.
  • Oluwapelumi OB., Morayo A., Buru AS., Richard AY., Funmilayo AJ., Funmi AA. Antimicrobial Activities of Different Honeys Sold in Ado-Ekiti on Bacteria Associated with Upper Respiratory Tract Infections. International Journal of Current Microbiology and Applied Sciences 2017; 6(2): 1-10.
  • Oryan A., Alemzadeh E., Moshiri A. Biological properties and therapeutic activities of honey in wound healing: A narrative review and meta-analysis. Journal of tissue viability 2016; 25(2): 98-118.
  • Osés SM., Pascual-Maté A., de la Fuente D., de Pablo A., Fernández-Muiño MA., Sancho MT. Comparison of methods to determine antibacterial activity of honeys against Staphylococcus aureus. NJAS-Wageningen Journal of Life Sciences 2016; 78: 29-33. DOI: 10.1016/j.njas.2015.12.005.
  • Pecoraro L., Wang X., Shah D., Song X., Kumar V., Shakoor A., Rani R. Biosynthesis Pathways, Transport Mechanisms and Biotechnological Applications of Fungal Siderophores. Journal of Fungi 2022; 8(1): 21. https://doi.org/10.3390/jof8010021
  • Peix A., Ramírez-Bahena MH., Velázquez E. The current status on the taxonomy of Pseudomonas revisited: an update. Infection, Genetics and Evolution 2018; 57: 106-116.
  • Ringel MT., Brüser T. The biosynthesis of pyoverdines. Microbial cell 2018; 5(10): 424.
  • Ronsisvalle S., Lissandrello E., Fuochi V., Petronio-Petronio G., Straquadanio C., Crascì L., Furneri PM Antioxidant and antimicrobial properties of Casteanea sativa Miller chestnut honey produced on Mount Etna (Sicily). Natural product research 2019; 33(6): 843-850.
  • Sherlock O., Dolan A., Athman R., Power A., Gethin G., Cowman S., Humphreys H. Comparison of the antimicrobial activity of Ulmo honey from Chile and Manuka honey against methicillin-resistant Staphylococcus aureus, Escherichia coli and Pseudomonas aeruginosa. BMC complementary and alternative medicine 2010; 10(1): 1-5.
  • Silby MW., Winstanley C., Godfrey SA., Levy SB., Jackson RW. Pseudomonas genomes: diverse and adaptable. FEMS microbiology reviews 2011; 35(4): 652-680.
  • Vică ML., Glevitzky M., Tit DM., Behl T., Heghedűş-Mîndru RC., Zaha DC., Bungău S. The antimicrobial activity of honey and propolis extracts from the central region of Romania. Food Bioscience 2021; 41: 101014.
  • Zavascki AP., Barth AL., Gonçalves ALS., Moro ALD., Fernandes JF., Martins AF., Goldani LZ. The influence of metallo-β-lactamase production on mortality in nosocomial Pseudomonas aeruginosa infections. Journal of Antimicrobial Chemotherapy 2006; 58(2): 387-392.
There are 30 citations in total.

Details

Primary Language English
Subjects Structural Biology
Journal Section RESEARCH ARTICLES
Authors

Sinan Bayram 0000-0002-2156-1566

Publication Date March 8, 2022
Submission Date December 30, 2021
Acceptance Date February 1, 2022
Published in Issue Year 2022

Cite

APA Bayram, S. (2022). Pseudomonas aeruginosa and Pyoverdines: A Hidden Threat in Apitherapy Applications. Osmaniye Korkut Ata Üniversitesi Fen Bilimleri Enstitüsü Dergisi, 5(1), 315-324. https://doi.org/10.47495/okufbed.1050755
AMA Bayram S. Pseudomonas aeruginosa and Pyoverdines: A Hidden Threat in Apitherapy Applications. Osmaniye Korkut Ata University Journal of The Institute of Science and Techno. March 2022;5(1):315-324. doi:10.47495/okufbed.1050755
Chicago Bayram, Sinan. “Pseudomonas Aeruginosa and Pyoverdines: A Hidden Threat in Apitherapy Applications”. Osmaniye Korkut Ata Üniversitesi Fen Bilimleri Enstitüsü Dergisi 5, no. 1 (March 2022): 315-24. https://doi.org/10.47495/okufbed.1050755.
EndNote Bayram S (March 1, 2022) Pseudomonas aeruginosa and Pyoverdines: A Hidden Threat in Apitherapy Applications. Osmaniye Korkut Ata Üniversitesi Fen Bilimleri Enstitüsü Dergisi 5 1 315–324.
IEEE S. Bayram, “Pseudomonas aeruginosa and Pyoverdines: A Hidden Threat in Apitherapy Applications”, Osmaniye Korkut Ata University Journal of The Institute of Science and Techno, vol. 5, no. 1, pp. 315–324, 2022, doi: 10.47495/okufbed.1050755.
ISNAD Bayram, Sinan. “Pseudomonas Aeruginosa and Pyoverdines: A Hidden Threat in Apitherapy Applications”. Osmaniye Korkut Ata Üniversitesi Fen Bilimleri Enstitüsü Dergisi 5/1 (March 2022), 315-324. https://doi.org/10.47495/okufbed.1050755.
JAMA Bayram S. Pseudomonas aeruginosa and Pyoverdines: A Hidden Threat in Apitherapy Applications. Osmaniye Korkut Ata University Journal of The Institute of Science and Techno. 2022;5:315–324.
MLA Bayram, Sinan. “Pseudomonas Aeruginosa and Pyoverdines: A Hidden Threat in Apitherapy Applications”. Osmaniye Korkut Ata Üniversitesi Fen Bilimleri Enstitüsü Dergisi, vol. 5, no. 1, 2022, pp. 315-24, doi:10.47495/okufbed.1050755.
Vancouver Bayram S. Pseudomonas aeruginosa and Pyoverdines: A Hidden Threat in Apitherapy Applications. Osmaniye Korkut Ata University Journal of The Institute of Science and Techno. 2022;5(1):315-24.

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