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Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Letter Article

Disruption of Staphylococcus aureus Biofilms with Purified Moringa oleifera Leaf Extract Protein

Author(s): Lakshmi Menon, Omprakash Chouhan, Rushikesh Walke, Shruti Shah, Samir Damare and Sumit Biswas*

Volume 30, Issue 2, 2023

Published on: 02 February, 2023

Page: [116 - 125] Pages: 10

DOI: 10.2174/0929866530666230123113007

Price: $65

Abstract

Background: A major cause of economic losses in the medical implant sector has been bacterial biofilms due to their ability to persist on various surfaces and their tolerance against endogenous defences, antibiotics, or other anti-microbial agents. The quest for potential sources causing inhibition or disruption of bacterial biofilms has been taken up to alleviate the loss. Plantderived extracts such as essential oils, bioactive compounds and other solvent extracts are regularly being used instead of antibiotics and other synthetic compounds as they are safer, economical, and in many instances, have an elaborate history of traditional medicinal usage.

Objectives: As a plant that has been traditionally used over the centuries, the Moringa oleifera Lam., or more commonly the drumstick tree, is being tapped for myriad pharmaceutical applications. The protein-rich leaf of this tree has not only proved to be of great nutritional value but also divulged numerous potential therapeutic applications.

Methods: While reports of proteinaceous components are rare, here we report the efficacy of the aqueous extract of the leaf of M. oleifera and a 62 kDa protein component in the disruption of staphylococcal biofilms, which are largely implicated in nosocomial infections.

Results: The application of the M. oleifera leaf extract protein had a marked effect on the biofilm growth or formation by Staphylococcus aureus.

Conclusion: While the crude extract itself showed considerable disruption of biofilm formation, the application of the purified protein obtained after a two-step process led to a significant increase in the anti-biofilm activity.

Graphical Abstract

[1]
Algburi, A.; Comito, N.; Kashtanov, D.; Dicks, L.M.T.; Chikindas, M.L. Control of biofilm formation: Antibiotics and beyond. Appl. Environ. Microbiol., 2017, 83(3), e02508-e02516.
[http://dx.doi.org/10.1128/AEM.02508-16] [PMID: 27864170]
[2]
Dolatabadi, S.; Moghadam, H.N.; Mahdavi-Ourtakand, M. Evaluating the anti-biofilm and antibacterial effects of Juglans regia L. extracts against clinical isolates of Pseudomonas aeruginosa. Microb. Pathog., 2018, 118, 285-289.
[http://dx.doi.org/10.1016/j.micpath.2018.03.055] [PMID: 29605650]
[3]
Lahiri, D.; Dash, S.; Dutta, R.; Nag, M. Elucidating the effect of anti-biofilm activity of bioactive compounds extracted from plants. J. Biosci., 2019, 44(2), 52.
[http://dx.doi.org/10.1007/s12038-019-9868-4] [PMID: 31180065]
[4]
Otto, M. Staphylococcal biofilms. Microbiol. Spectr., 2018, 6(4), 6.4.27.
[http://dx.doi.org/10.1128/microbiolspec.GPP3-0023-2018] [PMID: 30117414]
[5]
Khatoon, Z.; McTiernan, C.D.; Suuronen, E.J.; Mah, T.F.; Alarcon, E.I. Bacterial biofilm formation on implantable devices and approaches to its treatment and prevention. Heliyon, 2018, 4(12), e01067.
[http://dx.doi.org/10.1016/j.heliyon.2018.e01067] [PMID: 30619958]
[6]
Deivamarudachalam, T.P.D.; Srinivasan, P.; Guna, G.; Manime-kalai, K.; Jaganathan, D. In vitro anti biofilm activity of Piper longum and Piper nigrum against clinical isolates of streptococcus pyogenes isolated from pharyngitis patients. Int. Res. J. Pharm., 2015, 6(2), 122-132.
[http://dx.doi.org/10.7897/2230-8407.06229]
[7]
Arciola, C.R.; Campoccia, D.; Speziale, P.; Montanaro, L.; Costerton, J.W. Biofilm formation in staphylococcus implant infections. a review of molecular mechanisms and implications for biofilm-resistant materials. Biomaterials, 2012, 33(26), 5967-5982.
[http://dx.doi.org/10.1016/j.biomaterials.2012.05.031] [PMID: 22695065]
[8]
Connaughton, A.; Childs, A.; Dylewski, S.; Sabesan, V.J. Biofilm disrupting technology for orthopedic implants: What’s on the horizon? Front. Med., 2014, 1, 22.
[http://dx.doi.org/10.3389/fmed.2014.00022] [PMID: 25705632]
[9]
Kumar, S.; Kamboj, J.; Suman, S.; Sharma, S. Overview for various aspects of the health benefits of Piper longum linn. fruit. J. Acupunct. Meridian Stud., 2011, 4(2), 134-140.
[http://dx.doi.org/10.1016/S2005-2901(11)60020-4] [PMID: 21704957]
[10]
Taganna, J.C.; Quanico, J.P.; Perono, R.M.G.; Amor, E.C.; Rivera, W.L. Tannin-rich fraction from Terminalia catappa inhibits quorum sensing (QS) in Chromobacterium violaceum and the QS-controlled biofilm maturation and LasA staphylolytic activity in Pseudomonas aeruginosa. J. Ethnopharmacol., 2011, 134(3), 865-871.
[http://dx.doi.org/10.1016/j.jep.2011.01.028] [PMID: 21291979]
[11]
Sankar Ganesh, P.; Rai Vittal, R. In vitro antibiofilm activity of Murraya koenigii essential oil extracted using supercritical fluid CO2 method against Pseudomonas aeruginosa PAO1. Nat. Prod. Res., 2015, 29(24), 2295-2298.
[http://dx.doi.org/10.1080/14786419.2015.1004673] [PMID: 25635569]
[12]
Perumal, S.; Mahmud, R. Chemical analysis, inhibition of biofilm formation and biofilm eradication potential of Euphorbia hirta L. against clinical isolates and standard strains. BMC Complement. Altern. Med., 2013, 13(1), 346.
[http://dx.doi.org/10.1186/1472-6882-13-346] [PMID: 24321370]
[13]
Farrag, H.A.; Hosny, A.E.D.M.S.; Hawas, A.M.; Hagras, S.A.A.; Helmy, O.M. Potential efficacy of garlic lock therapy in combating biofilm and catheter-associated infections; experimental studies on an animal model with focus on toxicological aspects. Saudi Pharm. J., 2019, 27(6), 830-840.
[http://dx.doi.org/10.1016/j.jsps.2019.05.004] [PMID: 31516325]
[14]
Vergara-Jimenez, M.; Almatrafi, M.; Fernandez, M. Bioactive components in Moringa oleifera leaves protect against chronic disease. Antioxidants, 2017, 6(4), 91.
[http://dx.doi.org/10.3390/antiox6040091] [PMID: 29144438]
[15]
Teixeira, E.M.B.; Carvalho, M.R.B.; Neves, V.A.; Silva, M.A.; Arantes-Pereira, L. Chemical characteristics and fractionation of proteins from Moringa oleifera Lam. leaves. Food Chem., 2014, 147, 51-54.
[http://dx.doi.org/10.1016/j.foodchem.2013.09.135] [PMID: 24206684]
[16]
Dzotam, J.K.; Touani, F.K.; Kuete, V. Antibacterial and antibiotic-modifying activities of three food plants (Xanthosoma mafaffa Lam., Moringa oleifera (L.) Schott and Passiflora edulis Sims) against multidrug-resistant (MDR) Gram-negative bacteria. BMC Complement. Altern. Med., 2015, 16(1), 9.
[http://dx.doi.org/10.1186/s12906-016-0990-7] [PMID: 26753836]
[17]
de Oliveira, A.M.; de Abreu Filho, B.A.; de Jesus Bassetti, F.; Bergamasco, R.; Gomes, R.G. Natural extract of Moringa oleifera leaves promoting control of Staphylococcus aureus strains biofilm on pvc surface. Food Bioprocess Technol., 2020, 13(10), 1817-1832.
[http://dx.doi.org/10.1007/s11947-020-02521-x]
[18]
Abdulkadir, A.R.; Hasan, M.M.; Jahan, M.S. Antimalarial, antioxidant, antimicrobial properties of Moringa oliefera Lam: A review. Aust. J. Crop Sci., 2018, 12(6), 905-908.
[http://dx.doi.org/10.21475/ajcs.18.12.06.PNE920]
[19]
Gopalakrishnan, L.; Doriya, K.; Kumar, D.S. Moringa oleifera: A review on nutritive importance and its medicinal application. Food Sci. Hum. Wellness, 2016, 5(2), 49-56.
[http://dx.doi.org/10.1016/j.fshw.2016.04.001]
[20]
Saucedo-Pompa, S.; Torres-Castillo, J.A.; Castro-López, C.; Rojas, R.; Sánchez-Alejo, E.J.; Ngangyo-Heya, M.; Martínez-Ávila, G.C.G. Moringa plants: Bioactive compounds and promising applications in food products. Food Res. Int., 2018, 111, 438-450.
[http://dx.doi.org/10.1016/j.foodres.2018.05.062] [PMID: 30007707]
[21]
Husni, E.; Badriyya, E.; Putri, L.; Aldi, Y. The effect of ethanol extract of moringa leaf (Moringa oleifera lam) against the activity and capacity of phagocytosis of macrofag cells and the percentage of leukosit cells of white mice. Pharmacogn. J., 2021, 13(3), 706-712.
[http://dx.doi.org/10.5530/pj.2021.13.90]
[22]
Mohamad Shariff, N.F.S.; Singgampalam, T.; Ng, C.H.; Kue, C.S. Antioxidant activity and zebrafish teratogenicity of hydroalcoholic Moringa oleifera L. leaf extracts. Br. Food J., 2020, 122(10), 3129-3137.
[http://dx.doi.org/10.1108/BFJ-02-2020-0113]
[23]
Al_husnan, L.A.; Alkahtani, M.D.F. Impact of moringa aqueous extract on pathogenic bacteria and fungi in vitro. Ann. Agric. Sci., 2016, 61, 247-250.
[http://dx.doi.org/10.1016/j.aoas.2016.06.003]
[24]
Peixoto, J.R.O.; Silva, G.C.; Costa, R.A.; de Sousa, F.J.L.; Vieira, G.H.F.; Filho, A.A.F.; Vieira, R.H.S.F. In vitro antibacterial effect of aqueous and ethanolic moringa leaf extracts. Asian Pac. J. Trop. Med., 2011, 4(3), 201-204.
[http://dx.doi.org/10.1016/S1995-7645(11)60069-2] [PMID: 21771453]
[25]
de Oliveira, A.M.; da Silva Férnandes, M.; de Abreu Filho, B.A.; Gomes, R.G.; Bergamasco, R. Inhibition and removal of staphylococcal biofilms using Moringa oleifera Lam. aqueous and saline extracts. J. Environ. Chem. Eng., 2018, 6(2), 2011-2016.
[http://dx.doi.org/10.1016/j.jece.2018.02.043]
[26]
Mahmood, K.T.; Mugal, T.; Haq, I.U. Moringa oleifera: A natural gift-a review. J. Pharm. Sci. Res., 2010, 2, 775-781.
[27]
Onsare, J.G.; Arora, D.S. Antibiofilm potential of flavonoids extracted from Moringa oleifera seed coat against Staphylococcus aureus, Pseudomonas aeruginosa and Candida albicans. J. Appl. Microbiol., 2015, 118(2), 313-325.
[http://dx.doi.org/10.1111/jam.12701] [PMID: 25410525]
[28]
Busani, M.; Patrick, J.M.; Arnold, H.; Voster, M. Nutritional characterization of moringa (Moringa oleifera lam.) leaves. Afr. J. Biotechnol., 2011, 10(60), 12925-12933.
[http://dx.doi.org/10.5897/AJB10.1599]
[29]
a) Sahoo, S.; Raghavendra, K.M.; Biswas, S. Identification of a proteinaceous component in the leaf of Moringa oleifera Lam. with effects on high serum creatinine. Indian J. Pharm. Sci., 2014, 76(1), 78-81.
[PMID: 24799742];
b) Liu, M.; Wu, X.; Li, J.; Liu, L.; Zhang, R.; Shao, D.; Du, X. The specific anti-biofilm effect of gallic acid on Staphylococcus aureus by regulating the expression of the ica operon. Food Control, 2017, 73, 613-618.
[http://dx.doi.org/10.1016/j.foodcont.2016.09.015]
[30]
Sjahfirdi, L.; Nasikin, M. Mayangsari, protein identification using fourier transform infrared. Int. J. Res. Rev. Appl. Sci., 2012, 10, 418-421.
[31]
Shevchenko, A.; Tomas, H.; Havli, J.; Olsen, J.V.; Mann, M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc., 2006, 1(6), 2856-2860.
[http://dx.doi.org/10.1038/nprot.2006.468] [PMID: 17406544]
[32]
Boyd, A.; Chakrabarty, A.M. Pseudomonas aeruginosa biofilms: Role of the alginate exopolysaccharide. J. Ind. Microbiol., 1995, 15(3), 162-168.
[http://dx.doi.org/10.1007/BF01569821] [PMID: 8519473]
[33]
Bandekar, D.; Chouhan, O.P.; Mohapatra, S.; Hazra, M.; Hazra, S.; Biswas, S. Putative protein VC0395_0300 from Vibrio cholerae is a diguanylate cyclase with a role in biofilm formation. Microbiol. Res., 2017, 202, 61-70.
[http://dx.doi.org/10.1016/j.micres.2017.05.003] [PMID: 28647124]
[34]
Allan-Wojtas, P.; Truelstrup Hansen, L.; Paulson, A.T. Microstructural studies of probiotic bacteria-loaded alginate microcapsules using standard electron microscopy techniques and anhydrous fixation. Lebensm. Wiss. Technol., 2008, 41(1), 101-108.
[http://dx.doi.org/10.1016/j.lwt.2007.02.003]
[35]
Lamed, R.; Naimark, J.; Morgenstern, E.; Bayer, E.A. Scanning electron microscopic delineation of bacterial surface topology using cationized ferritin. J. Microbiol. Methods, 1987, 7(4-5), 233-240.
[http://dx.doi.org/10.1016/0167-7012(87)90045-5]
[36]
Rio, L.; Kusiak-Nejman, E.; Kiwi, J.; Bétrisey, B.; Pulgarin, C.; Trampuz, A.; Bizzini, A. Comparison of methods for evaluation of the bactericidal activity of copper-sputtered surfaces against methicillin-resistant Staphylococcus aureus. Appl. Environ. Microbiol., 2012, 78(23), 8176-8182.
[http://dx.doi.org/10.1128/AEM.02266-12] [PMID: 22983970]
[37]
Maiti, P.K.; Chatterjee, S.; Dey, R.; Kundu, A.K.; Dey, R.K. Biofilms on indwelling urologic devices: Microbes and antimicrobial management prospect. Ann. Med. Health Sci. Res., 2014, 4(1), 100-104.
[http://dx.doi.org/10.4103/2141-9248.126612] [PMID: 24669340]
[38]
O’Gara, J.P. ica and beyond: Biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol. Lett., 2007, 270(2), 179-188.
[http://dx.doi.org/10.1111/j.1574-6968.2007.00688.x] [PMID: 17419768]
[39]
Kranjec, C.; Morales, A.D.; Torrissen, M.M.; Fernández, L.; García, P.; Kjos, M.; Diep, D.B. Staphylococcal biofilms: Challenges and novel therapeutic perspectives. Antibiotics, 2021, 10(2), 131.
[http://dx.doi.org/10.3390/antibiotics10020131] [PMID: 33573022]
[40]
Brooks, J.L.; Jefferson, K.K. Phase variation of poly-N-acetylglucosamine expression in Staphylococcus aureus. PLoS Pathog., 2014, 10(7), e1004292.
[http://dx.doi.org/10.1371/journal.ppat.1004292] [PMID: 25077798]
[41]
Schilcher, K.; Horswill, A.R. Staphylococcal biofilm development: Structure, regulation, and treatment strategies. Microbiol. Mol. Biol. Rev., 2020, 84(3), e00026-e19.
[http://dx.doi.org/10.1128/MMBR.00026-19] [PMID: 32792334]
[42]
Barrett, L.; Atkins, B. The clinical presentation of prosthetic joint infection. J. Antimicrob. Chemother., 2014, 69(S1), i25-i27.
[http://dx.doi.org/10.1093/jac/dku250] [PMID: 25135085]
[43]
Corrigan, R.M.; Rigby, D.; Handley, P.; Foster, T.J. The role of Staphylococcus aureus surface protein SasG in adherence and biofilm formation. Microbiology, 2007, 153(8), 2435-2446.
[http://dx.doi.org/10.1099/mic.0.2007/006676-0] [PMID: 17660408]

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