The in Vitro Antibiofilm Activity of Bacteria Isolated From Waterfall and Marine Environment Against Human Bacterial Pathogens

Stella Magdalena, Natassa Rustandi, Yogiara Yogiara

Abstract


Abstrak

KKeterlibatan biofilm pada infeksi kronis dan pada permukaan peralatan medis selalu menjadi wacana penting bagi kesehatan umum di dunia. Biofilm bakteri berkaitan dengan tingkat resistensi terhadap antibiotik yang menjadikan infeksi sulit untuk diobati. Untuk mengatasi masalah ini, pengendalian yang efektif perlu diimplementasikan, seperti penerapan senyawa antibiofilm. Beberapa tahun terakhir, lingkungan akuatik menjadi salah satu sumber potensi penghasil senyawa bioaktif, termasuk senyawa antibiofilm. Tujuan dari penelitian ini yaitu menapis dan mengkarakterisasi bakteri asal air terjun dan laut yang diperoleh dari beberapa lokasi di Indonesia, sebagai penghasil aktivitas antibiofilm. Isolat dievaluasi berdasarkan kemampuan aktivitas antimikroba terhadap enam bakteri patogen dan diikuti dengan penapisan senyawa antibiofilm. Sebanyak 11 dari 65 isolat menunjukkan aktivitas quorum sensing atau quorum quenching, dan hanya terdapat satu isolat yang memiliki aktivitas keduanya. Supernatan kesebelas isolat menunjukkan penghambatan pembentukan biofilm setidaknya terhadap satu patogen dengan metode uji biofilm statis. Karakterisasi senyawa bioaktif dari lima isolat yang terpilih menunjukkan aktivitas senyawa yang berbeda, seperti karbohidrat, protein, dan asam nukleat. Sekuensing gen penyandi 16S rRNA menetapkan kelima isolat tersebut berada dalam dua genus yang berbeda, Vibrio (WK2.4, WK2.6, and WK2.3) dan Pseudomonas (S1.2 dan S1.3). Penelitian ini memberikan wawasan baru terhadap pencarian kandidat bakteri akuatik sebagai agen antibiofilm yang potensial.

 

Abstract

Biofilm involvement in chronic infections and on the surface of medical equipment have been considered as public health concern worldwide. Bacterial biofilm is related to antibiotic resistance, making the diseases difficult to treat. An effective control strategy should be implemented, for example, by applying antibiofilm agents. The use of aquatic environment as potential sources of bioactive compounds, including the antibiofilm compounds, is recently of concern. This study aimed to screen and characterize bacteria with antibiofilm activity that were isolated from waterfall and marine environment and obtained from several locations in Indonesia. The isolates were firstly evaluated for their antimicrobial activity against six bacterial pathogens and followed by antibiofilm screening. Eleven out of 65 isolates showed quorum sensing or quorum quenching activity, and one of them showed both activities. Supernatants of 11 isolates inhibited biofilm formation of at least one pathogen by using static biofilm assay. Bioactive compounds characterization of the selected five isolates revealed the presence of different compounds, such as carbohydrates, proteins, and nucleic acids. The 16S rRNA gene sequencing analysis classified five isolates into two different genera, namely Vibrio (WK2.4, WK2.6, and WK2.3) and Pseudomonas (S1.2 and S1.3). The present study provides insights into the discovery of aquatic bacteria candidates as antibiofilm agents.


Keywords


Air terjun; Antibiofilm; Bakteri laut; Quorum quenching; Antibiofilm; Marine bacteria; Quorum quenching; Waterfall

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References


Abdel-Aziz, S. M., & Aeron, A. (2014). Bacterial biofilm: Dispersal and inhibition strategies. Scholarena Journal of Biotechnology, 1(1), 105. doi: 10.18875/2375-6713.1.105.

Anand, T. P., Bhat, A. W., Shouche, Y. S., Roy, U., Siddhart, J., & Sarma, S. P. (2006). Antimicrobial activity of marine bacteria associated with sponges from the waters off the coast of South East India. Microbiological Research, 161(3), 252-262. doi: 10.1016/j.micres.2005.09.002.

Banat, I. M., De Rienzo, M. A., & Quinn, G. A. (2014). Microbial biofilms: Biosurfactants as antibiofilm agents. Applied Microbiology and Biotechnology, 98(24), 9915-9929. doi: 10.1007/s00253-014-6169-6.

Berne, C., Kysela, D. T., & Brun, Y. V. (2010). A bacterial extracellular DNA inhibits settling of motile progeny cells within a biofilm. Molecular Microbiology, 77(4), 815-829. doi: 10.1111/j.1365-2958.2010.07267.x.

Berne, C., Ellison, C. K., Ducret, A., & Brun, Y. V. (2018). Bacterial adhesion at the single-cell level. Nature Reviews Microbiology, 16(10), 616-627. doi:10.1038/s41579-018-0057-5.

Boşgelmez-Tinaz, G., Ulusoy, S., Aridoğan, B., Eroğlu, F., & Kaya, S. (2005). N-butanoyl-L-homoserine lactone (BHL) deficient Pseudomonas aeruginosa isolates from an intensive care unit. Microbiological Research, 160(4), 399-403. doi: 10.1016/j.micres.2005.03.005.

Brackman, G., & Coenye, T. (2015). Quorum sensing inhibitors as anti-biofilm agents. Current Pharmaceutical Design, 21(1), 5-11. doi: 10.2174/1381612820666140905114627.

Busscher, H. J., & Hanny, C., V., D., M. (2012). How do bacteria know they are on a surface and regulate their response to an adhering state?. PLoS Pathogens, 8(1), e1002440. doi: 10.1371/journal.ppat.1002440.

Camesi, A. B. R., Lukito, A., Waturangi, D. E., & Hwang, J. K. (2016). Screening of antibiofilm activity from marine bacteria against pathogenic bacteria. Microbiology Indonesia, 10(3), 87-94. doi: 10.5454/mi.10.3.2.

Chambers, J. R., & Sauer, K. (2013). Small RNAs and their role in biofilm formation. Trends in Microbiology, 21(1), 39-49. doi: 10.1016/j.tim.2012.10.008.

Chong, T. M., Koh, C. L., Sam, C. K., Choo, Y. M., Yin, W. F., & Chan, K. G. (2012). Characterization of quorum sensing and quorum quenching soil bacteria isolated from Malaysian tropical montane forest. Sensors, 12(4), 4846-4859. doi: 10.3390/s120404846.

Choo, J. H., Rukayadi, Y., & Hwang, J. -K. (2006). Inhibition of bacterial quorum sensing by vanilla extract. Letters in Applied Microbiology, 42(6), 637-641. doi:10.1111/j.1472-765X.2006.01928.x.

Coenye, T. (2010). Social interactions in the Burkholderia cepacia complex: Biofilms and quorum sensing. Future Microbiology, 5(7),1087-1099. doi: 10.2217/fmb.10.68.

Cuadrado-Silva, C. T., Castellanos, L., Arĕvalo-Ferro, C., & Osorno, O. E. (2013). Detection of quorum sensing systems of bacteria isolated from fouled marine organisms. Biochemical Systemics and Ecology, 46(2013), 101-107. doi: 10.1016/j.bse.2012.09.010

Dong, Y. H., Wang, L. H., & Zhang, L. H. (2007). Quorum-quenching microbial infections: Mechanisms and implications. Philosophical transactions of the Royal Society of London, Series B, Biological sciences, 362(1483), 1201-1211. doi: 10.1098/rstb.2007.2045.

Ghani, N. A., Norizan, S. N., Chan, X. Y., Yin, W. F., & Chan, K. G. (2014). Labrenzia sp. BM1: A quorum quenching bacterium that degrades n-acyl homoserine lactones via lactonase activity. Sensors, 14(7), 11760-11769. doi: 10.3390/s140711760.

Jiang, P., Li, J., Han, F., Duan, G., Lu, X., Gu, Y., & Yu, W. (2011). Antibiofilm activity of an exopolysaccharide from marine bacterium Vibrio sp. QY101. PLoS One, 6(4), e18514. doi: 10.1371/journal.pone.0018514.

Jorge, P., Lourenço, A., & Pereira, M. O. (2012). New trends in peptide-based anti-biofilm strategies: A review of recent achievements and bioinformatic approaches. Biofouling, 28(10), 1033-1061. doi: 10.1080/08927014.2012.728210.

Koopman, J. A., Marshall, J. M., Bhatiya, A., Eguale, T., Kwiek, J. J., & Gunn, J. S. (2015). Inhibition of Salmonella enterica biofilm formation using small-molecule adenosine mimetics. Antimicrobial Agents and Chemotherapy, 59(1), 76-84. doi: 10.1128/AAC.03407-14.

Lebeaux, D., Chauhan, A., Rendueles, O., & Beloin, C. (2013). From in vitro to in vivo models of bacterial biofilm-related infections. Pathogens, 2(2), 288-356. doi: 10.3390/pathogens2020288.

Lee, J., & Zhang, L. (2015). The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell, 6(1), 26-41. doi: 10.1007/s13238-014-0100-x.

Leroy, C., Delbarre, C., Ghillebaert, F., Compere, C., & Combes, D. (2008). Effects of commercial enzymes on the adhesion of a marine biofilm-forming bacterium. Biofouling, 24(1), 11-22.

Lewis, K. (2001). Riddle of biofilm resistance. Antimicrobial Agents and Chemotherapy, 45(4), 999-1007. doi: 10.1128/AAC.45.4.999-1007.2001.

Li, Y. H., & Tian, X. (2012). Quorum sensing and bacterial social interactions in biofilms. Sensors, 12(3), 2519-2538. doi: 10.3390/s120302519.

Lin, W., Kovacikova, G., & Skorupski, K. (2007). The quorum sensing regulator HapR downregulates the expression of the virulence gene transcription factor AphA in Vibrio cholerae by antagonizing Lrp- and VpsR-mediated activation. Molecular Microbiology, 64(4), 953-967. doi: 10.1111/j.1365-2958.2007.05693.x.

Liu, H., Srinivas, S., He, X., Gong, G., Dai, C., Feng, Y., ... Wang, S. (2013). Quorum sensing in Vibrio and its relevance to bacterial virulence. Journal of Bacteriology and Parasitology, 4(3), 172. doi: 10.4172/2155-9597.1000172.

Longo, F., Vuotto, C., & Donelli, G. (2014). Biofilm formation in Acinetobacter baumannii. The New Microbiologica, 37(2), 119-127. doi: 10.1128/AAC.01563-16.

Manavathu, E. K., Vager, D. L., & Vazquez, J. A. (2014). Development and antimicrobial susceptibility studies of in vitro monomicrobial and polymicrobial biofilm models with Aspergillus fumigatus and Pseudomonas aeruginosa. BMC Microbiology, 14, 53. doi: 10.1186/1471-2180-14-53.

Marchesi, J. R., Sato, T., Weightman, A. J., Martin, T. A. Fry, J. C. Hiom, S. J., ... Wade, W. G. (1998). Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Applied and Environmental Microbiology, 64(2), 795-799.

McClean, K. H., Winson, M. K., Fish, L., Taylor, A., Chhabra, S. M., Camara, M., ... Williams, P. (1997). Quorum sensing and Chromobacter violaceum: Exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology, 143(12), 3703-3711.

Papa, R., Selan, L., Parrilli, E., Tilotta, M., Sannino, F., Feller, G., ... Artini, M. (2015). Anti-biofilm activites from marine cold adapted bacteria against Staphylococci and Pseudomonas aeruginosa. Frontiers in Microbiology, 6,1333. doi: 10.3389/fmicb.2015.01333.

Rabin, N., Zheng, Y., Opoku-Temeng, C., Du, Y., Bonsu, E., & Sintim, H. O. (2015). Agents that inhibit bacterial biofilm formation. Future Medicinal Chemistry, 7(5), 647-671. doi: 10.4155/fmc.15.7.

Rajalakshmi, M., Srinivasan, P., Poffe, M. F., Suresh, R., & Priyadarisini, V. B. (2014). Crude fatty acid extracts of Streptomyces sps inhibits the biofilm forming Streptococcus pyogenes ATCC 19615. Journal of Biochemical Technology, 5(2), 679-684.

Rasamiravaka, T., Labtani, Q., Duez, P., & El Jaziri, M. (2015). The formation of biofilms by Pseudomonas aeruginosa: A review of the natural and synthetic compounds interfering with control mechanisms. BioMed Research International 2015, 759348. doi: 10.1155/2015/759348.

Rendueles, O., Kaplan, J. B., & Ghigo, J. M. (2013). Antibiofilm polysaccharides. Enviromental Microbiology, 15(2), 334-346. doi: 10.1111/j.1462-2920.2012.02810.x.

Romero, M., Martin-Cuadrado, A. B., Roca-Rivada, A., Cabello, A. M., & Otero, A. (2011). Quorum quenching in cultivable bacteria from dense marine coastal microbial communities. FEMS Microbiology Ecology, 75(2), 205-217. doi: 10.1111/j.1574-6941.2010.01011.x.

Roy, R., Tiwari, M., Donelli, G., & Tiwari, V. (2018). Strategies for combating bacterial biofilms: A focus on anti-biofilm agents and their mechanisms of action. Virulence, 9(1), 522-524. doi: 10.1080/21505594.2017.1313372.

Sandasi, M., Leonard, C. M., & Viljoen, A. M. (2010). The in vitro antibiofilm activity of selected culinary herbs and medicinal plants against Listeria monocytogenes. Letters in Applied Microbiology, 50(1), 30-35. doi: 10.1111/j.1472-765X.2009.02747.x.

Tchesnokova, V., Aprikian, P., Kisiela, D., Gowey, S., Korotkova, N., Thomas, W., & Sokurenko, E. (2011). Type 1 fimbrial adhesin FimH elicits an immune response that enhances cell adhesion of Escherichia coli. Infection and Immunity, 79(10), 3895-3904. doi: 10.1128/IAI.05169-11.

Trautner, B. W., & Darouiche, R. O. (2004). Role of biofilm in catheter-associated urinary tract infection. American Journal of Infection Control, 32(3), 177-183. doi: 10.1016/j.ajic.2003.08.005.

Uğur, A., Ceylan, Ő., & Aslim, B. (2012). Characterization of Pseudomonas spp. from seawater of The Southwest Coast of Turkey. Journal of Biodiversity and Environmental Sciences, 6(16), 15-23.

Vasavi, H. S., Arun, A. B., & Rekha, P. D. (2015). Anti-quorum sensing potential of Adenanthera pavonina. Pharmacognosy Research, 7(1), 105-109. doi: 10.4103/0974-8490.147220.

Vu, B., Chen, M., Crawford, R. J., & Ivanova, E. P. (2009). Bacterial extracelullar polysaccharides involved in biofilm formation. Molecules, 14(7), 2535-2554. doi: 10.3390/molecules14072535.

Wahjudi, M., Papaioannou, E., Hendrawati, O., Aart, H. G. V. A., Ronald, V. M., Cool, R. H., ... Quax, W. J. (2011). PA0305 of Pseudomonas aeruginosa is a quorum quenching acylhomoserine lactone acylase belonging to the Ntn hydrolase superfamily. Microbiology, 157(7), 2042-2055. doi: 10.1099/mic.0.043935-0.

Wang, W., Li, D., Huang, X., Yang, H., Qiu, Z., Zou, L., ... Li, Y. (2019). Study on antibacterial and quorum sensing inhibition activities of Cinnamomum camphora leaf essential oil. Molecules, 24(20), 3792. doi:10.3390/molecules24203792.

Waturangi, D. E., Bunardi, Y. A., & Magdalena, S. (2011). Antibiofilm activity of bacteria isolated from marine environment in Indonesia against Vibrio cholerae. Research Journal of Microbiology, 6(12), 926-930. doi: 10.3923/jm.2011.926.930.

Waturangi, D. E., Hariyanto, J. P., Lois, W., Hutagalung, R. A., & Hwang, J. K. (2017). Inhibition of marine biofouling by aquatic Actinobacteria and coral-associated marine bacteria. Malaysian Journal of Microbiology, 13(2), 92-99. doi: 10.21161/mjm.86016.

Woo, J. H., Kitamura, E., Myouga, H., & Kamei, Y. (2002). An antifungal protein from the marine bacterium Streptomyces sp. strain AP77 is specific for Pythium porphyrae, a causative agent of red rot disease in Porphyra spp. Applied and Environmental Microbiology, 68(6), 2666-2675. doi: 10.1128/AEM.68.6.2666-2675.2002.

Wu, S., Liu, G., Jin, W., Xiu, P., & Sun, C. (2016). Antibiofilm and anti-infection of a marine bacterial exopolysaccharide against Pseudomonas aeruginosa. Frontiers in Microbiology, 7, 102. doi: 10.3389/fmicb.2016.00102.

Yarwood, J. M., Bartels, D. J., Volper, E. M., & Greenberg, E. P. (2004). Quorum sensing in Staphylococcus aureus biofilms. Journal of Bacteriology, 186(6), 1838-1850. doi: 10.1128/JB.186.6.1838-1850.2004.

Yunos, Y. N. M., Tan, W. S., Mohamad, N. I., Tan, P. W., Adrian, T. G. S., Yin, W. F., & Chan, K. G. (2014). Quorum sensing activity of a Kluyvera sp. isolated from a Malaysian waterfall. Sensors, 14(5), 8305-8312. doi: 10.3390/s140508305.




DOI: https://doi.org/10.15408/kauniyah.v13i2.14926 Abstract - 0 PDF - 0

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