ENDOPHYTIC BACTERIA DIVERSITY FROM ZINGIBERACEAE AND ANTICANDIDAL CHARACTERIZATION PRODUCED BY Pseudomonas helmanticensis

Authors

  • Tri Ratna Sulistiyani Research Center for Biology, Indonesian Institute of Sciences, Jl. Raya Jakarta-Bogor Km. 46, Cibinong Science Center, Cibinong 16911, Indonesia https://orcid.org/0000-0002-2307-6863
  • Masrukhin Research Center for Biology, Indonesian Institute of Sciences, Jl. Raya Jakarta-Bogor Km. 46, Cibinong Science Center, Cibinong 16911, Indonesia https://orcid.org/0000-0001-8853-6034
  • Ismu Purnaningsih Research Center for Biology, Indonesian Institute of Sciences, Jl. Raya Jakarta-Bogor Km. 46, Cibinong Science Center, Cibinong 16911, Indonesia
  • Toga Pangihotan Napitupulu Research Center for Biology, Indonesian Institute of Sciences, Jl. Raya Jakarta-Bogor Km. 46, Cibinong Science Center, Cibinong 16911, Indonesia https://orcid.org/0000-0002-4219-6211
  • Agus Budiyanto Indonesian Center for Agricultural Post Harvest Research and Development Jl. Tentara Pelajar No. 12 Cimanggu, Agricultural Research Campus, Indonesia
  • Atit Kanti Research Center for Biology, Indonesian Institute of Sciences, Jl. Raya Jakarta-Bogor Km. 46, Cibinong Science Center, Cibinong 16911, Indonesia
  • I Made Sudiana Research Center for Biology, Indonesian Institute of Sciences, Jl. Raya Jakarta-Bogor Km. 46, Cibinong Science Center, Cibinong 16911, Indonesia

DOI:

https://doi.org/10.11113/jurnalteknologi.v83.15014

Keywords:

Anticandidal, diversity, endophytic, identification, Zingiberaceae

Abstract

Endophytic microbes are sources for the novel antibiotic. We isolated endophytic bacteria from Zingiberaceae collected from West Sulawesi, Indonesia, and investigated their anticandidal activity. Molecular identification of the isolates was done using 16S rRNA gene sequence analysis. The antimicrobial activity was tested against four bacteria and one yeast. The anticandidal compound of selected bacteria was extracted using three different solvents (chloroform, ethyl acetate, and methanol), and each fraction was tested for their anticandidal activity. Anticandidal minimum inhibitory concentration (MIC) was determined with concentration ranging from 300 to 18.75 μg/mL, and the morphology of the Candida cells after treatment was confirmed by scanning electron microscope (SEM). The identification of anticandidal compounds was conducted using GC-MS. A total of 24 isolates were collected from Zingiberaceae plants. There were 14 genera and 19 species belonging to Gammaproteobacteria (66.67%), Alphaproteobacteria (25.00%), Actinobacteria (4.17%), Bacteriodetes (4.17%), and a new record for Lelliottia aquatilis as an endophytic bacteria. One of 24 isolates identified as Pseudomonas helmanticensis isolated from Alpinia melichroa showed anticandidal activity. Ethyl acetate was the appropriate solvent to extract the anticandidal compounds. Diisooctyl phthalate was found as the most abundant compound in the extract for the anticandidal activity. An increase in extract concentration did not reduce the Candida cell number. The extract treatment showed membrane disruption of Candida albicans cells. We propose that active compounds from P. helmanticensis are potential as anticandidal sources and could be explored more for the pharmaceutical industry. 

References

References

George, V., Mathew, J., Sabulal, B., Dan, M. and Shiburaj, S. 2006. Chemical composition and antimicrobial activity of essential oil from the rhizomes of Amomum cannicarpum. Fitoterapia. 77: 392–394.

DOI: https://doi.org/10.1016/j.fitote.2006.04.003

Yang, Y., Yan, R., Cai, X., Zheng, Z. and Zou, G. 2008. Chemical composition and antimicrobial activity of the essential oil of Amomum tsao-ko. Journal of the Science of Food and Agriculture. 88(12): 2111–2116.

DOI: https://doi.org/10.1002/jsfa.3321

Tijjani, M. A., Dimari, G. A., Buba, S. W. and Khan, I. Z. 2012. In-vitro antibacterial properties and pre-liminary phtytochemical analysis of Amomum subulatum Roxburg ( Large Cardamom ). Journal of Applied Pharmaceutical Science. 02(05): 69–73.

DOI: https://doi.org/10.7324/JAPS.2012.2511

Chan, E. W. C., Lim, Y. Y. and Omar, M. 2007. Antioxidant and antibacterial activity of leaves of Etlingera species ( Zingiberaceae ) in Peninsular Malaysia. Food Chemistry. 104:(4) 1586–1593.

DOI:https://doi.org/10.1016/j.foodchem.2007.03.023

Ghasemzadeh, A., Jaafar, H. Z. E., Rahmat, A. and Ashkani, S. 2015. Secondary metabolites constituents and antioxidant , anticancer and antibacterial activities of Etlingera elatior ( Jack ) R . M . Sm grown in different locations of Malaysia. BMC Complementary and Alternative Medicine. 15(335): 1–10.

DOI: https://doi.org/10.1186/s12906-015-0838-6

Tan, R. X. and Zou, W. X. 2001. Endophytes: a rich source of functional metabolites. Natural product reports. 18(4): 448–459.

DOI: https://doi.org/10.1039/b100918o

Pimentel, M. R., Molina, G., Dion, A. P. and Pastore, M. 2011. The use of endophytes to obtain bioactive compounds and their application in biotransformation process. Biotechnology Research International. 2011: 1–11.

DOI: https://doi.org/10.4061/2011/576286

Das, I., Panda, M. K., Rath, C. C. and Tayung, K. 2017. Bioactivities of bacterial endophytes isolated from leaf tissues of Hyptis suaveolens against some clinically significant pathogens. Journal of Applied Pharmaceutical Science. 7(8): 131–136.

DOI: https://doi.org/10.7324/JAPS.2017.70818

Alvin, A., Miller, K. I. and Neilan, B. A. 2014. Exploring the potential of endophytes from medicinal plants as sources of antimycobacterial compounds. Microbiological Research. 169(7–8): 483–495.

DOI: https://doi.org/10.1016/j.micres.2013.12.009

Miller, K. I., Qing, C., Sze, D. M. Y., Roufogalis, B. D. and Neilan, B. A. 2012. Culturable endophytes of medicinal plants and the genetic basis for their boactivity. Microbial Ecology. 64(2): 431–449.

DOI: https://doi.org/10.1007/s00248-012-0044-8

Strobel, G. and Daisy, B. 2003. Bioprospecting for microbial endophytes and their natural products. Microbiology and molecular biology reviews : MMBR. 67(4): 491–502.

DOI: https://doi.org/10.1128/MMBR.67.4.491-502.2003

Gouda, S., Das, G., Sen, S. K. and Shin, H. 2016. Endophytes : A treasure house of bioactive compounds of medicinal importance. Frontiers in Microbiology. 7: 1–8.

DOI: https://doi.org/10.3389/fmicb.2016.01538

Hamby, K. A., Hernández, A., Boundy-mills, K. and Zalom, F. G. 2012. Associations of yeasts with spotted-wing Drosophila ( Drosophila suzukii ; Diptera : Drosophilidae ) in cherries and raspberries. Applied and Environmental Microbiology. 78(14): 4869–4873.

DOI: https://doi.org/10.1128/AEM.00841-12

Li, H., Qing, C., Zhang, Y. and Zhao, Z. 2005. Screening for endophytic fungi with antitumour and antifungal activities from Chinese medicinal plants. World Journal of Microbiology & Biotechnology. 21: 1515–1519.

DOI: https://doi.org/10.1007/s11274-005-7381-4

Zida, A., Bamba, S., Yacouba, A. and Guiguemdé, R. T. 2016. Anti- Candida albicans natural products , sources of new antifungal drugs : A review. Journal de Mycologie Medicale.

DOI: https://doi.org/10.1016/j.mycmed.2016.10.002

Arau, W. L., Marcon, J., Maccheroni, W., Elsas, J. D. Van and Vuurde, J. W. L. Van. 2002. Diversity of endophytic bacterial populations and their interaction with Xylella fastidiosa in citrus plants. Applied and Environmental Microbiology. 68(10): 4906–4914.

DOI: https://doi.org/10.1128/AEM.68.10.4906-4914.2002

Packeiser, H., Lim, C., Balagurunathan, B., Wu, J. and Zhao, H. 2013. An extremely simple and effective colony PCR procedure for bacteria, yeasts and microalgae. Applied Biochemistry and Biotechnology. 169(2): 695–700.

DOI: https://doi.org/10.1007/s12010-012-0043-8

Palaniappan, P., Chauhan, P. S., Saravanan, V. S., Anandham, R. and Sa, T. 2010. Isolation and characterization of plant growth promoting endophytic bacterial isolates from root nodule of Lespedeza sp. Biology and Fertility of Soils. 46(8): 807–816.

DOI: https://doi.org/10.1007/s00374-010-0485-5

Yoon, S., Ha, S., Kwon, S., Lim, J., Kim, Y., Seo, H. and Chun, J. 2017. Introducing EzBioCloud : a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. International Journal of Systematic and Evolutionary Microbiology. 67: 1613–1617.

DOI: https://doi.org/10.1099/ijsem.0.001755

Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. 2013. MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution. 30(12): 2725–2729.

DOI: https://doi.org/10.1093/molbev/mst197

Balouiri, M., Sadiki, M. and Ibnsouda, S. K. 2016. Methods for in vitro evaluating antimicrobial activity : A review. Journal of Pharmaceutical Analysis. 6(2): 71–79.

DOI: https://doi.org/10.1016/j.jpha.2015.11.005

Deveau, A., Gross, H., Palin, B., Mehnaz, S., Schnepf, M., Leblond, P., Dorrestein, P. C. and Aigle, B. 2016. Role of secondary metabolites in the interaction between Pseudomonas fluorescens and soil microorganisms under iron-limited conditions. FEMS Microbiology Ecology. 92(8): 1–11.

DOI: https://doi.org/10.1093/femsec/fiw107

Arunachalam, C. and Gayathri, P. 2010. Studies on bioprospecting of endophytic bacteria from the medicinal plant of Andrographis paniculata for their antimicrobial activity and antibiotic susceptibility pattern. International Journal of Current Pharmaceutical Research. 2(4): 63–68.

Matsubara, V. H., Wang, Y., Bandara, H. M. H. N., Pinto, M., Mayer, A. and Samaranayake, L. P. 2016. Probiotic lactobacilli inhibit early stages of Candida albicans biofilm development by reducing their growth , cell adhesion and filamentation. Applied Microbiology and Biotechnology.

DOI: https://doi.org/10.1007/s00253-016-7527-3

Li, Y., Huang, W., Huang, S., Du, J. and Huang, C. 2012. Screening of anti-cancer agent using zebrafish : comparison with the MTT assay. Biochemical and Biophysical Research Communications. 422(1): 85–90.

DOI: https://doi.org/10.1016/j.bbrc.2012.04.110

Jalgaonwala, R. E. and Mahajan, R. T. 2011. Evaluation of hydrolytic enzyme activities of endophytes from. Biotechnology Advances. 7(6): 1733–1741.

Yulia E, Shipton, W. A. 2008. Fungal leaf mycota of selected aromatic plants in North Queensland. Australasian Mycologist. 27(1).

Kumar, A., Singh, R., Yadav, A. and Singh, D. D. G. P. K. 2016. Isolation and characterization of bacterial endophytes of Curcuma longa L . 3 Biotech. 6(1): 1–8.

DOI: https://doi.org/10.1007/s13205-016-0393-y

Chowdhury, E. K., Jeon, J., Rim, S. O., Park, Y. and Lee, S. K. 2017. Composition , diversity and bioactivity of culturable bacterial endophytes in mountain-cultivated ginseng in Korea. Scientific Reports. 7:10098.

DOI: https://doi.org/10.1038/s41598-017-10280-7

Park, Y., Lee, S., Ahn, D. J., Kwon, T. R., Park, S. U., Lim, H. and Bae, H. 2012. Diversity of fungal endophytes in various tissues of Panax ginseng Meyer cultivated in Korea. Journal of Ginseng Research. 36(2): 211–217.

DOI: http://dx.doi.org/10.5142/jgr.2012.36.2.211

Samonil, P., Valtera, M., Bek, S., Sebkova, B., Vrska, T. and Houska, J. 2011. Soil variability through spatial scales in a permanently disturbed natural spruce-fir-beech forest. European Journal of Forest Research. 130: 1075–1091.

DOI: https://doi.org/10.1007/s10342-011-0496-2

Chow, Y. and Ting, A. S. Y. 2015. Endophytic l-asparaginase-producing fungi from plants associated with anticancer properties. Journal of Advanced Research. 6(6): 869–876.

DOI: https://doi.org/10.1016/j.jare.2014.07.005

Putra, I. P., Rahayu, G. and Hidayat, I. 2015. Impact of domestication on the endophytic fungal diversity associated with wild zingiberaceae at Mount Halimun Salak National Park. HAYATI Journal of Biosciences. 22(4): 157–162.

DOI: https://doi.org/10.1016/j.hjb.2015.10.005

Sulistiyani, T. R., Lisdiyanti, P. and Lestari, Y. 2014. Population and diversity of endophytic bacteria associated with medicinal plant Curcuma zedoaria. Microbiology Indonesia. 8(2): 65–72.

DOI: https://doi.org/10.5454/mi.8.2.4

Kämpfer, P. and Glaeser, S. P. 2013. Prokaryote Characterization and Identification. In: Rosenberg, E., DeLong, E. F., Lory, S., Stackebrandt E., Thompson F. (eds) The Prokaryotes. Berlin: Springer-Verlag, Berlin, Heidelberg

DOI: https://doi.org/10.1007/978-3-642-30194-0_6

Vendan, R. T., Yu, Y. J., Lee, S. H. and Rhee, Y. H. 2010. Diversity of endophytic bacteria in ginseng and their potential for plant growth promotion. Journal of microbiology. 48(5): 559–565.

DOI: https://doi.org/10.1007/s12275-010-0082-1

Chen, I., Chang, C., Ng, C., Wang, C., Shyu, Y. and Chang, L. 2008. Antioxidant and antimicrobial activity of zingiberaceae plants in Taiwan. Plant Foods for Human Nutrition. 63: 15–20.

DOI: https://doi.org/10.1007/s11130-007-0063-7

Banisalam, B., Sani, W., Philip, K., Imdadul, H. and Khorasani, A. 2011. Comparison between in vitro and in vivo antibacterial activity of Curcuma zedoaria from Malaysia. African Journal of Biotechnology. 10(55): 11676–11681.

DOI: https://doi.org/10.5897/AJB10.962

Sharp, N. J., Newman, M. F., Santika, Y., Gufrin and Poulsen, A. D. 2012. The enigmatic ginger Alpinia melichroa rediscovered in southeast Sulawesi. Nordic Journal of Botany. 30(2): 163–167.

DOI: https://doi.org/10.1111/j.1756-1051.2011.01122.x

Sasidharan, S., Chen, Y., Saravanan, D., Sundram, K. M., Latha, L. Y. 2011. Extraction, isolation and characterization of boactive compounds from plants' extracts. African Journal of Traditional, Complementary and Alternative Medicines. 8(1): 1–10.

Khule, P. K., Gilhotra, R. M., Nitalikar, M. M. and More, V. V. 2019. Formulation and evaluation of itraconazole emulgel for various fungal infections. Asian Journal of Pharmaceutics. 13(1): 19–22.

Lucena, P. A., Nascimento, T. L., Gaeti, M. P. N., De Ãvila, R. I., Mendes, L. P., Vieira, M. S., Fabrini, D., Amaral, A. C. and Lima, E. M. 2018. In vivo vaginal fungal load reduction after treatment with itraconazole-loaded polycaprolactone-nanoparticles. Journal of Biomedical Nanotechnology. 14(7): 1347–1358.

DOI: https://doi.org/10.1166/jbn.2018.2574

Saag, M. S. and Dismukes, W. E. 1988. Azole antifungal agents: Emphasis on new triazoles. Antimicrobial Agents and Chemotherapy. 32(1): 1–8.

DOI: https://doi.org/10.1128/AAC.32.1.1

Lestner, J. and Hope, W. W. 2013. Itraconazole: An update on pharmacology and clinical use for treatment of invasive and allergic fungal infections. Expert Opinion on Drug Metabolism and Toxicology. 9(7): 911–926.

DOI: https://doi.org/10.1517/17425255.2013.794785

Seyedjavadi, S. S., Khani, S., Eslamifar, A., Ajdary, S., Goudarzi, M., Halabian, R., Akbari, R., Zare-Zardini, H., Fooladi, A. A. I., Amani, J., Razzaghi-Abyaneh, M. 2020. The antifungal peptide MCh-AMP1 derived from Matricaria chamomilla inhibits Candida albicans growth via inducing ROS generation and altering fungal cell membrane permeability. Frontiers in Microbiology. 10: 1–10.

DOI: https://doi.org/10.3389/fmicb.2019.03150

Ortiz, A. and Sansinenea, E. 2018. Di-2-ethylhexylphthalate may be a natural product, rather than a pollutant. Journal of Chemistry. 2018.

DOI: https://doi.org/10.1155/2018/6040814

Zhang, H., Hua, Y., Chen, J., Li, X., Bai, X. and Wang, H. 2018. Organism-derived phthalate derivatives as bioactive natural products. Journal of Environmental Science and Health, Part C. 36(3): 125–144.

DOI: https://doi.org/10.1080/10590501.2018.1490512

Afifah, N., Ibrahim, D., Sulaiman, S. F. and Zakaria, N. A. 2012. Inhibition of Klebsiella pneumoniae ATCC 13883 cells by hexane extract of Halimeda discoidea ( Decaisne ) and the identification of its potential bioactive compounds. Journal of Microbiology and Biotechnology. 22(6): 872–881.

Priya, A. M. and Jayachandran, S. 2012. Induction of apoptosis and cell cycle arrest by Bis ( 2-ethylhexyl ) phthalate produced by marine Bacillus pumilus MB 40. Chemico-Biological Interactions. 195(2): 133–143.

DOI: https://doi.org/10.1016/j.cbi.2011.11.005

Rajamanikyam, M., Vadlapudi, V., Parvathaneni, S. P., Koude, D., Sriapadi, P., Misra, S., Amanchy, R., Upadhyayula, S. M. 2017. Isolation and characterization of phthalates from Brevibacterium mcbrellneri that cause cytotoxycity and cell cycle arrest. EXCLI Journal. 16: 375–387.

Abd-elnaby, H., Abo-elala, G., Abdel-raouf, U., Abd-, A. and Hamed, M. 2016. Antibacterial and anticancer activity of marine Streptomyces parvus : optimization and application. Biotechnology & Biotechnological Equipment. 30(1): 180–191.

DOI: https://doi.org/10.1080/13102818.2015.1086280

Ramya, B., Malarvili, T., Velavan, S. 2015. GC-MS analysis of bioactive compounds in Bryonopsis lacinosa fruit extract. International Journal of Pharmaceutical Sciences and Research. 6(8): 3375–3379.

DOI: https://doi.org/10.13040/IJPSR.0975-8232.6(8).3375-79

Hadi, M. Y., Mohammad, G. J. and Hameed, I. H. 2016. Analysis of bioactive chemical compounds of Nigella sativa using gas chromatography-mass spectrometry. Journal of Parmacognosy ad Phytotherapy. 8(2): 8–24.

DOI: https://doi.org/10.5897/JPP2015.0364

Igwe, O. U. and Okwunodulu, F. U. 2014. Investigation of bioactive phytochemical compounds from the chloroform extract of the leaves of Phyllanthus amarus by GC-MS. International Journal of Chemistry and Pharmaceutical Sciences. 2(1): 554–560.

Belakhdar, G., Benjouad, A. and Abdennebi, E. H. 2015. Determination of some bioactive chemical constituents from Thesium humile Vahl. Journal of Materials and Environmental Science. 6(10): 2778–2783.

Downloads

Published

2020-12-07

Issue

Section

Science and Engineering

How to Cite

ENDOPHYTIC BACTERIA DIVERSITY FROM ZINGIBERACEAE AND ANTICANDIDAL CHARACTERIZATION PRODUCED BY Pseudomonas helmanticensis. (2020). Jurnal Teknologi, 83(1), 7-17. https://doi.org/10.11113/jurnalteknologi.v83.15014