Anti-biofilm, Anti-quorum sensing, Anti-swarming, and Antimicrobial Activity of Rubus fruticosus L.

Ülkü Zeynep Üreyen Esertaş; İnci Durukan; Ali Osman Kılıç; Saliha Ekşi

doi:10.18016/ksutarimdoga.vi.1396393

TR EN

Rubus fruticosus L. nin Anti-biyofilm, Anti-quorum sensing, Anti-swarming ve Antimikrobiyal Aktivitesi

Öz

Son on yılda dünya çapında benzeri görülmemiş bir oranda artan antibiyotik direnci sağlık sistemleri için ciddi bir zorluk oluşturmaktadır. Araştırmalar, bu direnç sorununun özellikle 2050'li yıllarda büyük can kayıplarına yol açacağını öngörmektedir. Dirençle mücadelede etkili antibiyotiklerin yerini alabilecek alternatif yöntemler araştırılmaktadır. Rubus fruticosus L., böğürtlen adıyla bilinen ve meyvesiyle ünlü bir çalı bitkisidir. Bu meyvenin tıbbi, kozmetik ve besin değeri oldukça yüksektir. Çalışmamızda, Rize iline ait Rubus fruticosus meyvesinin metanol, etil asetat, etanol ve hekzan ekstraktları antimikrobiyal ve antiquorum sensing aktivite açısından incelenmiştir. Çeşitli Gram-negatif ve Gram-pozitif bakterilere ve iki Candida cinsine ait türe karşı antimikrobiyal aktivite, agar difüzyon yöntemi ile araştırılmıştır. Anti-quorum sensing ve antibiofilm aktiviteleri ise Chromobacterium violaceum ATCC 12472 ve Pseudomonas aeruginosa PAO1 kullanılarak değerlendirilmiştir. Sonuçlar, Rubus fruticosus’un metanol ekstraktının antimikrobiyal aktiviteye sahip olduğunu, etanol ekstraktının ise antibiofilm ve antiswarming aktivitelerine sahip olduğunu göstermektedir. Bu bulgular, Rubus fruticosus’un antimikrobiyal dirençle mücadelede potansiyel bir doğal ajan olarak kullanılabileceğini düşündürmektedir.

Anahtar Kelimeler

Anti-biofilm, Anti-quorum sensing, Anti-swarming, and Antimicrobial Activity of Rubus fruticosus L.

Abstract

Over the past decade, antibiotic resistance has increased at an unprecedented rate, posing a serious challenge to healthcare systems worldwide. Research indicates that this resistance issue, which is projected to cause significant loss of life by the 2050s, is particularly alarming. Consequently, alternative methods to effective antibiotics are being explored to combat resistance. Rubus fruticosus L., commonly known as blackberry, is a shrub plant famous for its fruit. This fruit holds significant medicinal, cosmetic, and nutritional value. In our study, methanol, ethyl acetate, ethanol, and hexane extracts of Rubus fruticosus fruit from the Rize region were screened for their antimicrobial and quorum-sensing activities. Antimicrobial activity was investigated using the agar diffusion method against various Gram-negative and Gram-positive bacteria, as well as two Candida species. Anti-quorum sensing and antibiofilm activities were evaluated using Chromobacterium violaceum ATCC 12472 and Pseudomonas aeruginosa PAO1. The results showed that the methanol extract of Rubus fruticosus exhibited antimicrobial activity, while the ethanol extract demonstrated antibiofilm and anti-swarming activities. These findings suggest that Rubus fruticosus has the potential to be used as a natural agent in combating antimicrobial resistance.

Keywords

Destekleyen Kurum

Recep Tayyip Erdoğan Üniversitesi

Proje Numarası

TDK-2018-959

Kaynakça

Abachi, S., Khademi, F., Fatemi, H., & Malekzadeh, F. (2013). Study of antibacterial activity of selected Iranian plant extracts on Helicobacter pylori. Journal of Dental and Medical Sciences, 5(1), 55-59.
Abay, G., Batan, N., & Özdemır, T. (2016). Bryophyte checklist of Rize, north-east Turkey. Arctoa, 25(1), 386-392. https://doi.org/10.15298/arctoa.25.31
Abdou, R., Shabana, S., & Rateb, M. E. (2018). Terezine E, bioactive prenylated tryptophan analogue from an endophyte of Centaurea stoebe. Natural Product Research, 34(4), 503-510. https://doi.org/10.1080/ 14786419.2018.1489393.
Acet, T. (2021). Determining the phenolic components by using HPLC and the biological activity of Centaurea triumfetti. Plant Biosystems, 155(1), 159-164. https://doi.org/10.1080/11263504.2020.1722275.
Ahmed, A., Ahmad, A., Li, R., Al‐Ansi, W., Fatima, M., Mushtaq, B. S., … & Bai, Z. (2021). Recent advances in synthetic, industrial and biological applications of violacein and its heterologous production. Journal of Microbiology and Biotechnology, 31(11), 1465-1480. https://doi.org/10.4014/jmb.2107.07045
Antimicrobial Resistance Collaborators (2022). Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet, 399(10325), 629-655. https://doi.org/10.1016/S0140-6736(21)02724-0.
Bezuidenhout, M., Dimitrov, D., Staden, A. D. v., Oosthuizen, G. A., & Dicks, L. M. T. (2015). Titanium-based hip stems with drug delivery functionality through additive manufacturing. BioMed Research International, 2015(1), 134093. https://doi.org/10.1155/2015/134093
Bru, J., Kasallis, S. J., Zhuo, Q., Høyland-Kroghsbo, N. M., & Siryaporn, A. (2023). Swarming of p. aeruginosa: through the lens of biophysics. Biophysics Reviews, 4(3),031305. https://doi.org/10.1063/5.0128140

Bru, J., Rawson, B., Trinh, C., Whiteson, K., Høyland‐Kroghsbo, N. M., & Siryaporn, A. (2019). Pqs produced by the pseudomonas aeruginosa stress response repels swarms away from bacteriophage and antibiotics. Journal of Bacteriology, 201(23), 10-1128. https://doi.org/10.1128/jb.00383-19
Cavanagh HMA, Hipwel Ml, Wilkinson JM (2003). Antibacterial activity of berry fruits used for culinary purposes. Journal of medicinal food, 6(1), 57-61.
Cepas, V., Lopez, Y., Munoz, E., Rolo, D., Ardanuy, C., Marti, S., Xercavins, M., Horcajada, J. P., Bosch, J., & Soto, S. M. (2019). Relationship Between Biofilm Formation and Antimicrobial Resistance in Gram-Negative Bacteria. Microbial Drug Resistance, 25(1), 72-79. https://doi.org/10.1089/mdr.2018.0027.
Chu, W., Zhou, S., Jiang, Y., Zhu, W., Zhuang, X., & Fu, J. (2013). Efect of traditional Chinese herbal medicine with antiquorum sensing activity on Pseudomonas aeruginosa. Evidence Based Complementary and Alternative Medicine, 2013(1), 648257. https://doi.org/10.1155/2013/648257.
Cieplik, F., Deng, D., Crielaard, W., Buchalla, W., Hellwig, E., Al‐Ahmad, A., … & Maisch, T. (2018). Antimicrobial photodynamic therapy – what we know and what we don’t. Critical Reviews in Microbiology, 44(5), 571-589. https://doi.org/10.1080/1040841x.2018.1467876
Dalar, A. (2018). Plant taxa used in the treatment of diabetes in van province, Turkey. International Journal of Secondary Metabolite, 5(3), 171-185. https://doi.org/10.21448/ijsm.430703
Denev, P., Kratchanova, M., Ciz, M., Lojek, A., Vasicek, O., Nedelcheva, P., Blazheva, D., Toshkova, R., Gardeva, E., Yossifova, L., Hyrsl, P., & Vojtek, L. (2014). Biological activities of selected polyphenol-rich fruits related to immunity and gastrointestinal health. Food Chemistry, 15(157), 37-44. doi: 10.1016/j.foodchem.2014.02.022.
Durán, N., Justo, G. Z., Ferreira, C. V., Melo, P. S., Cordi, L., & Martins, D. (2007). Violacein: properties and biological activities. Biotechnology and Applied Biochemistry, 48(3), 127-133. https://doi.org/10.1042/ ba20070115
Ercan, U. K., Özdemir, G., Özdemir, M. A., & Güren, O. (2023). Plasma medicine: the era of artificial intelligence. Plasma Processes and Polymers, 20(12), https://doi.org/10.1002/ppap.202300066
Esertaş, Ü. Z. Ü., & Cora, M. (2024). Biological activities of Elaeagnus umbellata methanol extract. Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 27(6), 1262-1268.
Esertaş, Ü. Z. Ü., Durukan, İ., Kılıç, A. O., & Ekşi, S. (2024). Determination of antimicrobial and quorum sensing inhibition potentials of different types of berries from Rize. Kastamonu University Journal of Forestry Faculty, 24(1), 74-80.
Fontaine, B. M., Nelson, K., Lyles, J. T., Jariwala, P. B., García-Rodriguez, J. M., Quave, C. L., & Weinert, E. E. (2017). Identification of Ellagic Acid Rhamnoside as a Bioactive Component of a Complex Botanical Extract with Anti-biofilm Activity. Frontiers in Microbiology, 23(8), 496. https://doi.org/10.3389/fmicb.2017.00496.
Gür, D. (2016). Antibiyotik Duyarlılık Testleri, EUCAST: Uygulama, Yorum ve Uzman Kurallar. Türk Mikrobiyoloji Cemiyeti Dergisi, 46.
Hayer, S. S., Casanova-Higes, A., Paladino, E., Elnekave, E., Nault, A., Johnson, T. J., … & Álvarez, J. (2022). Global distribution of fluoroquinolone and colistin resistance and associated resistance markers in escherichia coli of swine origin – a systematic review and meta-analysis. Frontiers in Microbiology, 13, 834793. https://doi.org/10.3389/fmicb.2022.834793
Kanade, Y., Mohan, W., & Patwardhan, R. B. (2022). Violacein: a promising bacterial secondary metabolite. Research Journal of Chemistry and Environment, 26(6), 165-177. https://doi.org/10.25303/2606rjce165177
Kiymaci, M. E., Savluk, M., Gumustas, M., Uvey, M., & Unal, N. (2023). Antibacterial and antibiofilm activity of Melaleuca alternifolia (tea tree) essential oil against colistin resistant Salmonella enterica serotypes isolated from poultry environmental specimens. Journal of Research in Pharmacy, 27(2), 508-518. htpp://dx.doi.org/10.29228/jrp.333
Koh, K. H., & Tham, F. Y. (2011). Screening of traditional Chinese medicinal plants for quorum-sensing inhibitors activity. Journal of Microbiology Immunology and Infection, 44(2), 144-148. https://doi.org/10.1016/ j.jmii.2009.10.001.
Kranjec, C., Angeles, D. M., Mårli, M. T., Fernández, L., Garcı́a, P., Kjos, M., … & Diep, D. B. (2021). Staphylococcal biofilms: challenges and novel therapeutic perspectives. Antibiotics, 10(2), 131. https://doi.org/10.3390/ antibiotics10020131
Mahadwar, G., Chauhan, K. R., Bhagavathy, G. V., Murphy, C., Smith, A., & Bhagwat, A. A. (2015). Swarm motility of salmonella enterica serovar typhimurium is inhibited by compounds from fruit peel extracts. Letters in Applied Microbiology, 60(4), 334-340. https://doi.org/10.1111/lam.12364
McLean, R. J. C., Pierson, L. S., & Fuqua, C. (2004). A simple screening protocol for the identification of quorum signal antagonist. Journal of Microbiological Methods, 58(3), 351-60. https://doi.org/10.1016/ j.mimet.2004.04.016.
Mehta, T., Vercruysse, K., Johnson, T. L., Ejiofor, A. O., Myles, E. L., & Quick, Q. A. (2015). Violacein induces p44/42 mitogen-activated protein kinase-mediated solid tumor cell death and inhibits tumor cell migration. Molecular Medicine Reports, 12(1), 1443-1448. https://doi.org/10.3892/mmr.2015.3525
Merghni, A., Haddaji, N., Bouali, N., Alabbosh, K. F., Adnan, M., Snoussi, M., & Noumi, E. (2022). Comparative Study of Antibacterial, Antibiofilm, Antiswarming and Antiquorum Sensing Activities of Origanum vulgare Essential Oil and Terpinene-4-ol against Pathogenic Bacteria. Life, 12(10), 1616. https://doi.org/10.3390/life12101616.
Murray, P. R., Baron, E. J., Pfaller, M. A., Jorgensen, J. H., & Yolken, R. H. (2009). Manual of Clinical Microbiology. Birinci Cilt. Dokuzuncu Baskı. ASM Press, Washington, DC. 390- 770.
Noumi, E., Merghni, A., Alreshidi, M., Haddad, O., Akmadar, G., De Martino, L., Mastouri, M., Ceylan, O., Snoussi, M., Al-Sieni, A., & De Feo, V. (2018). Chromobacterium violaceum and Pseudomonas aeruginosa PAO1: Models for Evaluating Anti-Quorum Sensing Activity of Melaleuca alternifolia Essential Oil and Its Main Component Terpinen-4-ol. Molecules, 23(10), 2672. https://doi.org/10.3390/molecules23102672.
Oliveira, B. D. Á., Rodrigues, A. C., Cardoso, B. M. I., Ramos, A. L. C. C., Bertoldi, M. C., Taylor, J. G., ... & Pinto, U. M. (2016). Antioxidant, antimicrobial and anti-quorum sensing activities of Rubus rosaefolius phenolic extract. Industrial Crops and Products, 84, 59-66.
Packiavathy, S. V., Priya, S., Pandian, S. K., & Arumugam V. R. (2014). Inhibition of biofilm development of uropathogens by curcumin-An anti-quorum sensing agent from Curcuma longa. Food Chemistry, 148, 453-460. https://doi.org/10.1016/j.foodchem.2012.08.002.
Permatananda, P. A. N. K., Pandit, I. G. S., Cahyawati, P. N., & Aryastuti, A. A. S. A. (2023). Antimicrobial properties of eco enzyme: a literature review. Bioscientia Medicina: Journal of Biomedicine and Translational Research, 7(6), 3370-3376. https://doi.org/10.37275/bsm.v7i6.831
Rashid, M. H., & Kornberg, A. (2000). Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proceedins of the National Academy of Science, 97(9), 4885-4890. https://doi.org/10.1073/pnas.060030097.
Saliha, E. K. Ş. İ., Esertaş, Ü. Z. Ü., Kilic, A. O., Ejder, N., & Uzunok, B. (2020). Determination of the antimicrobial and antibiofilm effects and ‘Quorum Sensing’inhibition potentials of Castanea sativa Mill. extracts. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 48(1), 66-78.
Singh, R., Joshi, D. B., & Bhadauria, R. S. (2022). Hydrotropic solvents used for extraction techniques of barleria elegans l. leaves. International Journal of Scientific Research and Management, 10(04), 594-604. https://doi.org/10.18535/ijsrm/v10i04.mp01
Solanki, R., & Nagori, B. P. (2012). New method for extracting phytoconstituents from plants. International. Journal of Biomedical and Advance Research, 3(10), 770-774.
Terreni, M., Taccani, M., & Pregnolato, M. (2021). New antibiotics for multidrug-resistant bacterial strains: latest research developments and future perspectives. Molecules, 26(9), 2671. https://doi.org/10.3390/molecules 26092671
The European Committee on Antimicrobial Susceptibility Testing (EUCAST) (2022) European committee on antimicrobial susceptibility testing Broth microdilution - EUCAST reading guide v 4.0 (1 January 2022). https://www.eucast.org/
Truchado, P., Gil-Izqierdo, A., Tomas-Barberan, F., & Allenda, A. (2009). Inhibition by chenut honey of N-Acyl-L-homoserine lactones and biofilm formation in Erwinia carotovora, Yersinia enterocolitica and Aeromonas hydrophila. Journal of agricultural and food chemistry, 57(23), 11186-11193. https://doi.org/10.1021/jf9029139.
Tsui, C., Kong, E. F., & Jabra‐Rizk, M. A. (2016). Pathogenesis of candida albicans biofilm. Pathogens and Disease, 74(4), ftw018. https://doi.org/10.1093/femspd/ftw018
Uğurlu, A. (2013). Pseudomonas aeroginosa Suşlarında Çevreyi Algılama Sistemine Fenolik Maddelerin Etkisinin Araştırılması (Tez No 336766). [Uzmanlık tezi, Marmara Üniversitesi Tıp Fakültesi Tıbbi Mikrobiyoloji Ana Bilim Dalı]. Yükseköğretim Kurulu Ulusal Tez Merkezi.
Üreyen Esertaş, Ü. Z., Kara, Y., Kiliç, A. O., & Kolayli, S. (2022). A comparative study of antimicrobial, anti-quorum sensing, anti-biofilm, anti-swarming, and antioxidant activities in flower extracts of pecan (Carya illinoinensis) and chestnut (Castanea sativa). Archives of Microbiology, 204(9), 589.
Vattem, D. A., Mihalik, K., Crixell, S. H., & McLean, R. J. (2007). Dietary phytochemicals as quorum sensing inhibitors. Fitoterapia, 78(4), 302-310. https://doi.org/10.1016/j.fitote.2007.03.009.
Venkatesan, T., Choi, Y., & Kim, Y. (2019). Impact of different extraction solvents on phenolic content and antioxidant potential of pinus densiflora bark extract. BioMed Research International, 2019, 1-14. https://doi.org/10.1155/2019/3520675
Weli, A. M., Al-Saadi, H. S., Al-Fudhaili, R. S., Hossain, A., Putit, Z. B., & Jasim, M. K. (2020). Cytotoxic and antimicrobial potential of different leaves extracts of R. fruticosus used traditionally to treat diabetes. Toxicology Reports, 18(7), 183-187. https://doi.org/10.1016/j.toxrep.2020.01.006.
Woods, G. L., Brown-Elliott, B. A., Desmond EP, Hall GS, Heifets L, et al (2003). Susceptibility testing of mycobacteria, nocardiae, and other aerobic actinomycetes; Approved Standard. NCCLS document M24-A, 23 (18), 1-18.
Yazıcı, K., Balijagic, J., Göksu, B., Bilgin, Ö. F., & Erċışlı, S. (2023). Comparison of some fruit quality parameters of selected 12 mandarin genotypes from black sea region in Turkey. ACS Omega, 8(22), 19719-19727. https://doi.org/10.1021/acsomega.3c01364
Zhou, X. (2023). Antibiotic culture: a history of antibiotic use in the second half of the 20th and early 21st century in the people’s republic of China. Antibiotics, 12(3), 510. https://doi.org/10.3390/antibiotics12030510
Zia-Ul-Haq, M., Riaz, M., De Feo, V., Jaafar, Z. E. H., & Moga, M. (2014). Rubus Fruticosus L.: Constituents, Biological Activities and Health Related Uses. Molecules, 19(8), 10998-11029. https://doi.org/10.3390/ molecules190810998.

Ayrıntılar

Birincil Dil

İngilizce

Konular

Mikrobiyoloji (Diğer)

Bölüm

Araştırma Makalesi

Yazarlar

Ülkü Zeynep Üreyen Esertaş ^*
0000-0001-9897-5313
Türkiye

İnci Durukan
0000-0002-9789-4738
Türkiye

Ali Osman Kılıç
0000-0002-5506-0866
Türkiye

Saliha Ekşi
0000-0002-8818-7855
Türkiye

Erken Görünüm Tarihi

10 Haziran 2025

Yayımlanma Tarihi

4 Temmuz 2025

Gönderilme Tarihi

26 Kasım 2023

Kabul Tarihi

7 Mayıs 2025

Yayımlandığı Sayı

Yıl 2025 Cilt: 28 Sayı: 4

DOI

https://doi.org/10.18016/ksutarimdoga.vi.1396393

IZ

https://izlik.org/JA65JS79AF

Kaynak Göster

RIS / Bibtex

APA

Üreyen Esertaş, Ü. Z., Durukan, İ., Kılıç, A. O., & Ekşi, S. (2025). Anti-biofilm, Anti-quorum sensing, Anti-swarming, and Antimicrobial Activity of Rubus fruticosus L. Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 28(4), 903-913. https://doi.org/10.18016/ksutarimdoga.vi.1396393

Cited By

Anticancer, Antibiofilm, Antimicrobial Effects and Anti-Quorum Sensing Inhibition Potentials of Alchemilla oriturcica and Helichrysum armenium Extracts

Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi

https://doi.org/10.18016/ksutarimdoga.vi.1511359

Rubus fruticosus L. nin Anti-biyofilm, Anti-quorum sensing, Anti-swarming ve Antimikrobiyal Aktivitesi

Öz

Anahtar Kelimeler

Anti-biofilm, Anti-quorum sensing, Anti-swarming, and Antimicrobial Activity of Rubus fruticosus L.

Abstract

Keywords

Destekleyen Kurum

Proje Numarası

Kaynakça

Ayrıntılar

Birincil Dil

Konular

Bölüm

Yazarlar

Erken Görünüm Tarihi

Yayımlanma Tarihi

Gönderilme Tarihi

Kabul Tarihi

Yayımlandığı Sayı

DOI

IZ

Kaynak Göster

Cited By

Anticancer, Antibiofilm, Antimicrobial Effects and Anti-Quorum Sensing Inhibition Potentials of Alchemilla oriturcica and Helichrysum armenium Extracts

e-ISSN: 2619-9149