Candida Albicans and Streptococcus Mutans Biofilms Suppression by Bioactive Compounds Isolated from Ruta Angustifolia

Shafa Noer, Abinawanto, Boy M. Bachtiar, Anom Bowolaksono, Sofa Fajriah

Abstract

Ruta angustifolia is one of the species of Ruta genus that is widely used in Asia as traditional natural medicine, but scientific research related to this plant is still limited. Several studies have stated that this plant has an antimicrobial effect, but no studies have discussed the antibiofilm effect of bioactive compounds isolated from R. angustifolia. This study is the first to address this issue. This study aims to see whether the bioactive compounds isolated from R. angustifolia can inhibit the formation of biofilms on oral microbes that play the most important role in the construction of dental caries, namely Candida albicans and Streptococcus mutans. Isolation and identification of bioactive compounds is achieved through Thin Layer Chromatography, Liquid Chromatography with tandem mass spectrometry, and proton nuclear magnetic resonance, respectively. Crystal Violet (CV) method is used to see the total biomass of biofilm, and 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyl tetrazolium bromide (MTT) method is used for the viability test. The morphological visualization of C. albicans has also been carried out using a light microscope and a scanning electron microscope. Three compounds that have been isolated are kokusaginine, chalepin, and lindelofine. The CV and MTT data were compared with the control data using an analysis of variance test followed by the Tukey honestly significant difference test, while the morphological data is qualitatively analyzed. From the results of the biofilm test, it was concluded that the three compounds could significantly inhibit the formation of biofilms produced by C. albicans and S. mutans in mixed species cultures.

 

Keywords: Ruta angustifolia, biofilm, Candida albicans, Streptococcus mutans, bioactive compounds.

 

https://doi.org/10.55463/issn.1674-2974.49.1.25

 


Full Text:

PDF


References


WORLD HEALTH ORGANIZATION. Oral Health, 2020. https://www.who.int/news-room/fact-sheets/detail/oral-health

SALEHI B., KREGIEL D., MAHADY G., SHARIFI-RAD J., MARTINS N., and RODRIGUES C. F. Management of Streptococcus mutans-Candida spp. oral biofilms infections: paving the way for effective clinical interventions. Journal of Clinical Medicine, 2020, 9(2): 517. https://doi.org/10.3390/jcm9020517

EIDT G., DE ANDRADE C. G., DE CÁSSIA NEGRINI T., and ARTHUR R. A. Role of Candida albicans on enamel demineralization and on acidogenic potential of Streptococcus mutans in vitro biofilms. Journal of Applied Oral Science, 2019, 27: 1–8. https://doi.org/10.1590/1678-7757-2018-0593

CAVALHEIRO M., & TEIXEIRA M. C. Candida Biofilms: Threats, challenges, and promising strategies. Frontiers in Medicine, 2018, 5: 28. https://doi.org/10.3389/fmed.2018.00028

TALAPKO J., JUZBAŠIC M., MATIJEVIC T., PUSTIJANAC E., BEKIĆ S., KOTRIS I., and ŠKRLEC I. Candida albicans—The Virulence Factors and Clinical Manifestations of Infection. Journal of Fungi, 2021, 7(2): 79. https://doi.org/10.3390/jof7020079

LOBO C. I. V., RINALDI T. B., CHRISTIANO C. M. S., DE SALES LEITE L., BARBUGLI P. A., and KLEIN M. I. Dual-species biofilms of Streptococcus mutans and Candida albicans exhibit more biomass and are mutually beneficial compared with single-species biofilms. Journal of Oral Microbiology, 2019, 11(1): 1581520. https://doi.org/10.1080/20002297.2019.1581520

LU L., HU W., TIAN Z., YUAN D., YI G., ZHOU Y., CHENG Q., ZHU J., and LI M. Developing natural products as potential anti-biofilm agents. Chinese Medicine, 2019, 14(1): 11. https://doi.org/10.1186/s13020-019-0232-2

COIMBRA A. T., FERREIRA S., and DUARTE A. P. Genus Ruta: A natural source of high value products with biological and pharmacological properties. Journal of Ethnopharmacology, 2020, 260: 1-81. https://doi.org/10.1016/j.jep.2020.113076

RICHARDSON J. S. M., AMINUDIN N., and MALEK S. N. A. Chalepin: a compound from Ruta angustifolia L. Pers exhibits cell cycle arrest at S phase, suppresses nuclear factor-kappa B (NF-κB) pathway, signal transducer and activation of transcription 3 (STAT3) phosphorylation and extrinsic apoptotic pathway in non-small cell lung cancer carcinoma (A549). Pharmacognosy Magazine, 2017, 13(51): S489–S498. https://doi.org/10.4103/pm.pm_13_17

DUTTA K., KARMAKAR A., JANA D., BALLAV S., SHITYAKOV S., PANDA A. K., and GHOSH C. Benzyl isocyanate isolated from the leaves of Psidium guajava inhibits Staphylococcus aureus biofilm formation. Biofouling, 2020, 36(8): 1000–1017. https://doi.org/10.1080/08927014.2020.1842877

XIAO J., HARA A. T., KIM D., ZERO D. T., KOO H., and HWANG G. Biofilm three-dimensional architecture influences in situ pH distribution pattern on the human enamel surface. International Journal of Oral Science, 2017, 9(2): 74–79. https://doi.org/10.1038/ijos.2017.8

BARBOSA J. O., ROSSONI R. D., VILELA S. F. G., DE ALVARENGA J. A., DOS SANTOS VELLOSO M., DE AZEVEDO PRATA M. C., JORGE A. O. C., and JUNQUEIRA J. C. Streptococcus mutans can modulate biofilm formation and attenuate the virulence of Candida albicans. PLoS ONE, 2016, 11(3): e0150457. https://doi.org/10.1371/journal.pone.0150457

FAKAI M. I., ABD MALEK S. N., and KARSANI S. A. Induction of apoptosis by chalepin through phosphatidylserine externalisations and DNA fragmentation in breast cancer cells (MCF7). Life Sciences, 2019, 220: 186–193. https://doi.org/10.1016/j.lfs.2019.01.029

NAHAR L., AL-MAJMAIE S., AL-GROSHI A., RASUL A., and SARKER S. D. Chalepin and chalepensin: Occurrence, biosynthesis and therapeutic potential. Molecules, 2021, 26(6): 1609. https://doi.org/10.3390/molecules26061609

LASKAR M. A., & CHOUDHURY M. D. Search for therapeutics against COVID 19 targeting SARS-CoV-2 papain-like protease: an in silico study. Research Square, 2020, 1–28. https://doi.org/10.21203/rs.3.rs-33294/v1

RAUT J. S., & KARUPPAYIL S. M. Phytochemicals as Inhibitors of Candida Biofilm. Current Pharmaceutical Design, 2016, 22: 1–24. https://doi.org/10.2174/1381612822666160601

RICHARDSON J. S. M., SETHI G., LEE G. S., and MALEK S. N. A. Chalepin: isolated from Ruta angustifolia L . Pers induces mitochondrial mediated apoptosis in lung carcinoma cells. BMC Complementary and Alternative Medicine, 2016, 16: 389. https://doi.org/10.1186/s12906-016-1368-6

KHAMENEH B., IRANSHAHY M., SOHEILI V., and BAZZAZ B. S. F. Review on plant antimicrobials: a mechanistic viewpoint. Antimicrobial Resistance and Infection Control, 2019, 8: 118. https://doi.org/10.1186/s13756-019-0559-6

THAWABTEH A., JUMA S., BADER M., KARAMAN D., SCRANO L., BUFO S. A., and KARAMAN R. The biological activity of natural alkaloids against herbivores, cancerous cells and pathogens. Toxins, 2019, 11(11): 656. https://doi.org/10.3390/toxins11110656

EFSA PANEL ON CONTAMINANTS IN THE FOOD CHAIN (CONTAM), KNUTSEN H. K., ALEXANDER J., BARREGÅRD L., BIGNAMI M., BRÜSCHWEILER B., CECCATELLI S., COTTRILL B., DINOVI M., EDLER L., GRASL-KRAUPP B., HOGSTRAND C., HOOGENBOOM L. (R.), NEBBIA C. S., OSWALD I. P., PETERSEN A., ROSE M., ROUDOT A.-C., SCHWERDTLE T., VLEMINCKX C., VOLLMER G., WALLACE H., RUIZ J. A. G., and BINAGLIA M. Risks for human health related to the presence of pyrrolizidine alkaloids in honey, tea, herbal infusions and food supplements. EFSA Journal, 2017, 15(7): e04908. https://doi.org/10.2903/j.efsa.2017.4908

NOER S., & PRATIWI R. D. Uji kualitatif fitokimia daun Ruta angustifolia (Qualitative test of phytochemicals of Ruta angustifolia leaves). Faktor Exacta, 2016, 9(3): 200-206. http://dx.doi.org/10.30998/faktorexacta.v9i3.879

KAMAL L. Z. M., HASSAN N. M., TAIB N. M., and SOE M. K. Graveoline from Ruta angustifolia (L.) Pers. and its antimicrobial synergistic potential in erythromycin or vancomycin combinations. Sains Malaysiana, 2018, 47(10): 2429–2435. https://doi.org/10.17576/jsm-2018-4710-19

BOWEN W. H., BURNE R. A., WU H., and KOO H. Oral Biofilms: Pathogens, Matrix and Polymicrobial Interactions in Microenvironment. Trends in Microbiology, 2019, 26(3): 229–242. https://doi.org/10.1016/j.tim.2017.09.008

BACHTIAR E. W., & BACHTIAR B. M. Effect of cell-free spent media prepared from Aggregatibacter actinomycetemcomitans on the growth of Candida albicans and Streptococcus mutans in co-species biofilms. European Journal of Oral Sciences, 2020, 128(5): 395–404. https://doi.org/10.1111/eos.12725

NOER S., BACHTIAR B. M., and BOWOLAKSONO A. Inhibition of Candida albicans hypha formation in biofilm formation by Ruta angustifolia extract. AIP Conference Proceedings, 2021, 2331: 050003. https://doi.org/10.1063/5.0041682

WU R., TAO Y., CAO Y., ZHOU Y., and LIN H. Streptococcus mutans Membrane Vesicles Harboring Glucosyltransferases Augment Candida albicans Biofilm Development. Frontiers in Microbiology, 2020, 11: 581184. https://doi.org/10.3389/fmicb.2020.581184

IKONO R., VIBRIANI A., WIBOWO I., SAPUTRO K. E., MULIAWAN W., BACHTIAR B. M., MARDLIYATI E., BACHTIAR E. W., ROCHMAN N. T., KAGAMI H., XIANQI L., NAGAMURA-INOUE T., and TOJO A. Nanochitosan antimicrobial activity against Streptococcus mutans and Candida albicans dual-species biofilms. BMC Research Notes, 2019, 12(1): 383. https://doi.org/10.1186/s13104-019-4422-x

WIJAYA C. H., SEPTIANA S., BACHTIAR B. M., and YULIANA N. D. Cajuputs candy impairs Candida albicans and Streptococcus mutans mixed biofilm formation in vitro. F1000Research, 2020, 8: 1923. https://doi.org/10.12688/f1000research.20700.2


Refbacks

  • There are currently no refbacks.