Abstract
Endophytes associated with medicinal plants are a potential source of valuable natural products. This study aimed to evaluate the antibacterial and antibiofilm activities of endophytic bacteria from Archidendron pauciflorum against multidrug-resistant (MDR) strains. A total of 24 endophytic bacteria were isolated from the leaf, root, and stem of A. pauciflorum. Seven isolates showed antibacterial activity with different spectra against four MDR strains. Extracts derived from four selected isolates (1 mg/mL) also displayed antibacterial activity. Among four selected isolates, DJ4 and DJ9 isolates exhibited the strongest antibacterial activity against P. aeruginosa strain M18, as indicated by the lowest minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) (DJ4 and DJ9 MIC: 7.81 µg/mL; DJ4 and DJ9 MBC: 31.25 µg/mL). 2 × MIC of DJ4 and DJ9 extracts was found to be the most effective concentration to inhibit more than 52% of biofilm formation and eradicate more than 42% of established biofilm against all MDR strains. 16S rRNA-based identification revealed four selected isolates belong to the genus Bacillus. DJ9 isolate possessed nonribosomal peptide synthetase (NRPS) gene, and DJ4 isolate possessed NRPS and polyketide synthase type I (PKS I) gene. Both these genes are commonly responsible for secondary metabolites synthesis. Several antimicrobial compounds, including 1,4-dihydroxy-2-methyl-anthraquinone and paenilamicin A1, were detected in the bacterial extracts. This study highlights endophytic bacteria isolated from A. pauciflorum provide a great source of novel antibacterial compounds.
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References
World Health Organization. (2020). The top 10 causes of death. Available from: https://www.who.int/news-room/fact-sheets/detail/the-top-10-causes-of-death. Accessed on August 27, 2021.
Inggraini, M., Nurfajriah, S., Priyanto, J. A., & Ilsan, N. A. (2021). Antimicrobial susceptibility and molecular species identification of clinical carbapenem-resistant bacteria. Biodiversitas., 22(2), 555–562. https://doi.org/10.13057/biodiv/d220206
Bunawan, H., Dusik, L., Bunawan, S. N., & Amin, N. M. (2013). Botany, traditional uses, phytochemistry and pharmacology of Archidendron jiringa: A review. Global Journal of Pharmacology, 7(4), 474–478. https://doi.org/10.5829/idosi.gjp.2013.7.4.824
Nasution, H. M., Yuniarti, R., Rani, Z., & Nursyafira, A. (2022). Phytochemical screening and antibacterial activity test of ethanol extract of jengkol leaves (Archidendron pauciflorum Benth.) I.C. Nielsen against Staphylococcus epidermidis and Propionibacterium acnes. International Journal of Scientific & Technology Management, 3(3), 647–653. https://doi.org/10.46729/ijstm.v3i3.509
Hidayati, R. A., Kristijono, A., & Muadifah, A. (2021). Antibacterial activity test for gel hand sanitizer of jengkol rind (Archidendron pauciflorum (Benth.) Nielsen) extract against Escherichia coli bacteria. Jurnal Sains dan Kesehatan [Indonesian], 3(2), 165–176.
Anggraini, T., Novendra, V., & Novelina. (2018). Antioxidant activity of Archidendron pauciflorum, Syzygium oleana, Mangifera indica, Theobroma cacao and Cinnamomum burmannii young leaves and their application as jelly drink colourants. Pakistan Journal of Nutrition, 17, 492–499. https://doi.org/10.3923/pjn.2018.492.499
Sihombing, J. R., Sidabutar, C. A. B. S., Fachrial, E., Almahdy, A., Chaidir, Z., & Dharma, A. (2017). Utilization of fruit peel extracts of Persea mericana, Cyphomandra betacea, Mangifera odorata and Archidendron pauciflorum as antidiabetic in experimental rats. Research Journal of Pharmaceutical, Biological and Chemical Sciences, 8(1), 1407–1410.
Rahim, A. R., Malini, D. M., & Hermawan, W. (2018). Antihyperlipidemic activity of Archidendron pauciflorum fruit peel extract in streptozotocin-induced diabetes female wistar rats. IOP IOP Conference Series: Earth and Environmental Science, 166(2018), 1–8. https://doi.org/10.1088/1755-1315/166/1/012015
Fouda, A., Eid, A. M., Elsaied, A., El-Belely, E. F., Barghoth, M. G., Azab, E., Gobouri, A. A., & Hassan, S. E. D. (2021). Plant growth promoting endophytic bacterial community inhabiting the leaves of Pulicaria incisa (Lam.) DC inherent to arid regions. Plants, 10(76), 2–22. https://doi.org/10.3390/plants10010076
Chaouachi, M., Marzouk, T., Jallouli, S., Elkahoui, S., Gentzbittel, L., Ben, C., & Djébali, N. (2021). Activity assessment of tomato endophytic bacteria bioactive compounds for the postharvest biocontrol of Botrytis cinerea. Postharvest Biology and Technology, 172(11389), 1–18. https://doi.org/10.1016/j.postharvbio.2020.111389
Beiranvand, M., Amin, M., Hashemi-Shahraki, A., Romani, B., Yaghoubi, S., & Sadeghi, P. (2017). Antimicrobial activity of endophytic bacterial populations isolated from medical plants of Iran. Iranian Journal of Microbiology, 9(1), 11–18.
Myo, E. M., Maung, C. E. H., Mya, K. M., & Khai, A. A. (2020). Characterization of bacterial endophytes from Myanmar medicinal plants for antimicrobial activity against human and plant pathogens. Brazilian Journal of Pharmaceutical Sciences, 56(e17705), 1–8. https://doi.org/10.1590/s2175-97902019000317705
Aljuraifani, A., Aldosary, S., & Ababutain, I. (2019). In vitro antimicrobial activity of endophytes, isolated from Moringa peregrina growing in eastern region of Saudi Arabia. National Academy Science Letters, 42(1), 75–80. https://doi.org/10.1007/s40009-018-0739-6
Golinska, P., Wypij, M., Agarkar, G., Rathod, D., Dahm, H., & Rai, M. (2015). Endophytic actinobacteria of medicinal plants: Diversity and bioactivity. Antonie van Leeuwenhoek, 108, 267–289. https://doi.org/10.1007/s10482-015-0502-7
Ding, L., Armin, M., Heinz-Herbert, F., Wen-Han, L., & Christian, H. (2011). A family of multi-cyclic indolosesquiterpenes from a bacterial endophyte. Organic & Biomolecular Chemistry, 9(11), 4029–4031. https://doi.org/10.1039/c1ob05283g
Castillo, U., Harper, J. K., Strobel, G. A., Sears, J., Alesi, K., Ford, E., Lin, J., Hunter, M., Maranta, M., Ge, H., Yaver, D., Jensen, J. B., Porter, H., Robison, R., Millar, D., Hess, W. M., Condron, M., & Teplow, D. (2003). Kakadumycins, novel antibiotics from Streptomyces sp NRRL 30566, an endophyte of Grevillea pteridifolia. FEMS Microbiology Letters, 224(2), 183–190. https://doi.org/10.1016/S0378-1097(03)00426-9
Ezra, D., Castillo, U. F., Strobel, G. A., Hess, W. M., Porter, H., Jensen, J. B., Condron, M. A. M., Teplow, D. B., Sears, J., Maranta, M., Hunter, M., Weber, B., & Yaver, D. (2004). Coronamycins, peptide antibiotics produced by a verticillate Streptomyces sp. (MSU-2110) endophytic on Monstera sp. Microbiology., 150(04), 785–793. https://doi.org/10.1099/mic.0.26645-0
Singh, R., Pandey, K. D., Singh, M., Singh, S. K., Hasem, A., Al-ArjaniAbdAllah, A. B. F. E. F., Singh, P. K., & Kumar, A. (2021). Isolation and characterization of endophytes bacterial strains of Momordica charantia L. and their possible approach in stress management. Microorganisms, 10(290), 1–14. https://doi.org/10.3390/microorganisms10020290
Rini, A. F., Yuhana, M., & Wahyudi, A. T. (2017). Potency of sponge-associated bacteria producing bioactive compounds as biological control of vibriosis on shrimp. Jurnal Akuakultur Indonesia, 16(1), 41–50. https://doi.org/10.19027/jai.16.1.41-50
Priyanto, J. A., Pujiyanto, S., & Rukmi, I. (2014). Flavonoids production capability test of tea mistletoe (Scurrula atropurpurea BL. Dans) endophytic bacteria isolates. Jurnal Sains dan Matematika, 22(4), 89–96.
Diale, M. O., Aswa, E. U., & Serepa-Dlamini, M. H. (2018). The antibacterial activity of bacterial endophytes isolated from Combretum mole. African Journal of Biotechnology, 17(8), 255–262. https://doi.org/10.5897/AJB2017.16349
NCCLS (National Committee for Clinical Laboratory Standard). (2020). Performance standard for antimicrobial susceptibility testing. Ninth informational supplement. 30th ed., NCCLS, Malvern, PA, 40 (1), 1–294.
Wintachai, P., Paosen, S., Yupanqui, C. T., & Voravuthikunchai, S. P. (2019). Silver nanoparticles synthesized with Eucalyptus critriodora ethanol leaf extract stimulate antibacterial activity against clinically multidrug-resistant Acinetobacter baumannii isolated from pneumonia patients. Microbial Pathogenesis, 126, 245–257. https://doi.org/10.1016/j.micpath.2018.11.018
Marchesi, J. R., Sato, T., Weightman, A. J., Martin, A. T., Fry, J. C., Hiom, S. J., Dymock, D., & 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. https://doi.org/10.1128/AEM.64.2.795-799.1998
Ayuso-Sacido, A., & Genilloud, O. (2004). New PCR primers for the screening of NRPS and PKS-I systems in actinomycetes: Detection and distribution of these biosynthetic gene sequences in major taxonomic groups. Microbial Ecology, 49, 10–24. https://doi.org/10.1007/s00248-004-0249-6
Schirmer, A., Gadkari, R., Reeves, C. D., Ibrahim, F., DeLong, E. F., & Hutchinson, C. R. (2005). Metagenomic analysis reveals diverse polyketide synthase gene clusters in microorganisms associated with the marine sponge Discodermia dissolute. Applied and Environmental Microbiology, 71(8), 4840–4849. https://doi.org/10.1128/AEM.71.8.4840-4849.2005
Metsä-Ketelä, M., Salo, V., Halo, L., Hautala, A., Hakala, J., Mäntsälä, P., & Ylihonko, K. (1999). An efficient approach for screening minimal PKS genes from Streptomyces. FEMS Microbiology Letters, 180, 1–6. https://doi.org/10.1111/j.1574-6968.1999.tb08770.x
Septama, A. W., Tasfiyati, A. N., Kristiana, R., & Jaisi, A. (2022). Chemical profiles of essential oil from Javanese turmeric (Curcuma xanthorrhiza Roxb.): Evaluation of its antibacterial and antibiofilm activities against selected clinical isolates. South+A1443 African Journal of Botany, 146, 728–734. https://doi.org/10.1016/j.sajb.2021.12.017
Innocenti, G., Dall’Acqua, S., Viola, G., & Loi, M. C. (2006). Cytotoxic constituents from Anagyris foetida leaves. Fitotropia, 77(7), 595–597. https://doi.org/10.1016/j.fitote.2006.06.012
Ifaya, M., Musfiroh, I., Sahidin, & Susilawati, Y. (2021). Potential antidiabetic activities of fractions from purified extract of Lawsonia inermis leaves in alloxan–induced diabetic mice. International Journal of Applied Pharmaceutics, 13(4), 89–94. https://doi.org/10.22159/ijap.2021.v13s4.43824
Hu, H., Wang, S., Zhang, C., Wang, L., Ding, L., Zhang, J., & Wu, Q. (2010). Synthesis and in vitro inhibitory activity of matrine derivatives towards pro-inflammatory cytokines. Bioorganic & Medicinal Chemistry Letters, 20(24), 7537–7539.
Badr, J. M. (2008). Antioxidant and antimicrobial constituents of Crucianella maritima L. Natural Product Sciences, 14(4), 227–232.
Duraipandiyan, V., Al-Dhabi, N. A., & Ignacimuthu, S. (2016). New antimicrobial anthraquinone 6,61-bis (1,5,7-trihydroxy-3-hydroxymethylanthraquinone) isolated from Streptomyces sp. isolate ERI-26. Saudi Journal of Biological Sciences, 23(6), 731–735. https://doi.org/10.1016/j.sjbs.2016.02.008
Garcia-Gonzalez, E., Müller, S., Hertlein, G., Heid, N., Süssmuth, R. D., & Genersch, E. (2014). Biological effects of paenilamicin, a secondary metabolite antibiotic produced by the honey bee pathogenic bacterium Paenibacillus larvae. Microbiology Open, 3(5), 642–656. https://doi.org/10.1002/mbo3.195
Handayani, S., & Arty, I. S. (2008). Synthesis of hydroxyl radical scavengers from benzalacetone and its derivatives. Journal of Physical Science, 19(2), 61–68.
Morales-Cedeno, L. R., OrozcoMosqueda, M. D. C., Loeza-Lara, P. D., Parra-Cota, F. I., Santos-Villalobos, S. D. L., & Santoyo, G. (2021). Plant growth-promoting bacterial endophytes as biocontrol agents of pre- and post-harvest diseases: Fundamentals, methods of application and future perspectives. Microbiological Research, 242(2021), 1–12. https://doi.org/10.1016/j.micres.2020.126612
Gouda, S., Das, G., Sen, S. K., Shin, H. S., & Patra, J. K. (2016). Endophytes: A treasure house of bioactive compounds of medicinal importance. Frontiers in Microbiology, 7(1538), 1–8. https://doi.org/10.3389/fmicb.2016.01538
Nxumalo, C. I., Ngidi, L. S., Shandu, J. S. E., & Maliehe, T. S. (2020). Isolation of endophytic bacteria from the leaves of Anredera cordifolia CIX1 for metabolites and their biological activities. BMC Complementary Medicine and Therapies, 20(1), 1–11. https://doi.org/10.1186/s12906-020-03095-z
Xin, L. Y., Min, T. H., Zin, P. N. L. M., Pulingam, T., Appaturi, J. N., & Parumasivam, T. (2021). Antibacterial potential of Malaysian ethnomedicinal plants against methicillin-susceptible Staphylococcus aureus (MSSA) and methicillin-resistant Staphylococcus aureus (MRSA). Saudi Journal of Biological Sciences, 28(10), 5884–5889.
Bakar, R. A., Ahmad, I., & Sulaiman, S. F. (2012). Effect of Pithecellobium jiringa as antimicrobial agent. Bangladesh Journal of Pharmacology, 7, 131–134. https://doi.org/10.3329/bjp.v7i2.10973
Lebeaux, D., Ghigo, J. M., & Beloin, C. (2014). Biofilm-related infections: Bridging the gap between clinical management and fundamental aspects of recalcitrance toward antibiotics. Microbiology and Molecular Biology Reviews, 78(3), 510–543. https://doi.org/10.1128/MMBR.00013-14
Nadar, S., Khan, T., Patching, S. G., & Omri, A. (2022). Development of antibiofilm therapeutics strategies to overcome antimicrobial drug resistance. Microorganisms, 10(303), 1–28. https://doi.org/10.3390/microorganisms10020303
Khan, F., Oloketuyi, S. F., & Kim, Y. M. (2019). Diversity of bacteria and bacterial products as antibiofilm and antiquorum sensing drugs against pathogenic bacteria. Current Drug Targets, 20(11), 1156–1179. https://doi.org/10.2174/1389450120666190423161249
Ansary, W. R., Prince, F. R. K., Haque, E., Sultana, F., West, H. M., Rahman, M. M., Mondol, A. M., Akanda, A. M., Rahman, M., Clarke, M. L., & Islam, M. T. (2018). Endophytic Bacillus spp. from medicinal plants inhibit mycelial growth of Sclerotinia sclerotiorum and promote plant growth. Zeitschrift fuer Naturforschung, C: Journal of Biosciences, 73, 1–10. https://doi.org/10.1515/znc-2018-0002
Islam, T., Rabbee, M. F., Choi, J., & Baek, K. H. (2022). Biosynthesis, molecular regulation, and application of bacilysin produced by Bacillus species. Metabolites, 12(397), 1–13. https://doi.org/10.3390/metabo12050397
Qin, Y., Wang, Y., He, Y., Zhang, Y., She, Q., Chai, Y., Li, P., & Shang, Q. (2019). Characterization of subtilin l-q11, a novel class i bacteriocin synthesized by Bacillus subtilis L-Q11 isolated from orchard soil. Frontiers in Microbiology, 10, 1–11. https://doi.org/10.3389/fmicb.2019.00484
Tang, H. L., Sun, C. H., Hu, X. X., You, X. F., Wang, M., & Liu, S. W. (2016). Damxungmacin A and B, two new amicoumacins with rare heterocyclic cores isolated from Bacillus subtilis XZ-7. Molecules, 21(11), 1–10. https://doi.org/10.3390/molecules21111601
Cai, D., Zhang, B., Zhu, J., Xu, H., Liu, P., Wang, Z., Li, J., Yang, Z., Ma, X., & Chen, S. (2020). Enhanced bacitracin production by systematically engineering s-adenosylmethionine supply modules in Bacillus licheniformis. Frontiers in Bioengineering and Biotechnology, 8(305), 1–12. https://doi.org/10.3389/fbioe.2020.00305
Song, L., Jenner, M., Masschelein, J., Jones, C., Bull, M. J., Harris, S. R., Hartkoorn, R. C., Vocat, A., Romero-Canelon, I., Coupland, P., Webster, G., Dunn, M., Weiser, R., Paisey, C., Cole, S. T., Parkhill, J., Mahenthiralingam, E., & Challis, G. L. (2017). Discovery and biosynthesis of gladiolin: A Burkholderia gladioli antibiotic with promising activity against Mycobacterium tuberculosis. Journal of the American Chemical Society, 139(23), 7974–7981. https://doi.org/10.1021/jacs.7b03382
Mizuno, C. M., Kimes, N. E., López-Pérez, M., Ausó, E., Rodriguez-Valera, F., & Ghai, R. (2013). A hybrid NRPS-PKS gene cluster related to the bleomycin family of antitumor antibiotics in Alteromonas macleodii strains. PlosOne., 8(9), 1–12. https://doi.org/10.1371/journal.pone.0076021
Courtial, J., Helesbeux, J. J., Oudart, H., Aligon, S., Bahut, M., Hamon, B., N’Guyen, G., Pigné, S., Hussain, A. G., Pascouau, C., Bataillé-Simoneau, N., Collemare, J., Berruyer, R., & Poupard, P. (2022). Characterization of NRPS and PKS genes involved in the biosynthesis of SMs in Alternaria dauci including the phytotoxic polyketide aldaulactone. Science and Reports, 12(1), 1–20. https://doi.org/10.1038/s41598-022-11896-0
Miller, K. I., Qing, C., Sze, D. M. Y., & Neilan, B. A. (2012). Investigation of the biosynthetic potential of endophytes in traditional Chinese anticancer herbs. PlosOne, 7(5), 1–12. https://doi.org/10.1371/journal.pone.0035953
Caulier, S., Nannan, C., Gillis, A., Licciardi, F., Bragard, C., & Mahillon, J. (2019). Overview of the antimicrobial compounds produced by members of the Bacillus subtilis Group. Frontiers in Microbiology, 10(302), 1–19. https://doi.org/10.3389/fmicb.2019.00302
Acknowledgements
The authors would like to thank Dr. Tjandrawati Mozef from The Research Center for Pharmaceutical Ingredients and Traditional Medicine, National Research and Innovation Agency (BRIN), for the detailed discussion during the research.
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This study was funded by The Institution of Research and Community Services, IPB University, Indonesia, through “Penelitian Dosen Muda” Program under grant number 2881/IT3.L1/PT.01.03/M/T/2022, which was awarded to Jepri Agung Priyanto.
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JAP, MEP, and RIA contributed to the experimental design. JAP, MEP, and RK were involved in laboratory work and data analysis. JAP, MEP, and RIA confirmed and interpreted all research data and contributed to paper writing.
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Priyanto, J.A., Prastya, M.E., Astuti, R.I. et al. The Antibacterial and Antibiofilm Activities of the Endophytic Bacteria Associated with Archidendron pauciflorum against Multidrug-Resistant Strains. Appl Biochem Biotechnol 195, 6653–6674 (2023). https://doi.org/10.1007/s12010-023-04382-4
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DOI: https://doi.org/10.1007/s12010-023-04382-4