PERTANIKA JOURNAL OF SCIENCE AND TECHNOLOGY

The success rate of aquaculture is highly influenced by several factors, including optimum water quality, feed management, and microorganism control. Several microorganisms interfere with the quality of media and fish culture, i.e., fish growth. Aeromonas and Vibrio are the main pathogenic bacteria that disrupt fish growth and cause mortality. Sidr leaf (Ziziphus spina-christi) extract contains phytochemicals that have antibacterial properties. This study aimed to identify the phytochemical components and analyze the effect of Sidr leaf extract on the growth of aquaculture-based pathogenic bacteria. Sidr leaf extract was obtained using ethanol and tested via phytochemical analysis, chemical analysis, prediction of activity spectra for substances (PASS) examination, and inhibition capability against Aeromonas hydrophila, Aeromonas caviae, Aeromonas sobria, Pseudomonas putida, Pseudomonas aeruginosa, Streptococcus agalactiae, Vibrio vulnificus, Vibrio harveyi, Vibrio parahaemolyticus, and Vibrio alginolyticus. The results showed that Sidr leaf extract contained phytochemicals, namely, flavonoids, alkaloids, saponins, tannins, and steroids. Gas chromatography-mass spectrometry analyses showed that the Sidr leaf extract contained 30 compounds with antiseborrheic effects. PASS analysis demonstrated that 15 compounds (64.51% level) have potential as antibacterial, with a probability activity value of more than 0.300. The inhibition test showed that the Sidr leaf extract exhibited moderate-to-strong inhibition against pathogenic bacterial growth, except for V. vulnificus, for which it produced a weak inhibition. The results indicate that Sidr leaf extract can be used as a natural herb to control bacterial pathogens in fish cultivation.

• Ababutain, I. M. (2019). Antimicrobial activity and gas chromatography-mass spectrometry (GC-MS) analysis of Saudi Arabian Ocimum basilicum leaves extracts. Journal of Pure and Applied Microbiology, 13(2), 823–833. https://doi.org/10.22207/JPAM.13.2.17

• Abdel-Fatah, M. A., Hussein, N. H., Hawash, S. I., & Shaarawy, H. H. (2016). Investigation of using Sidr leave extracts in nano-silver preparation. ARPN Journal of Engineering and Applied Sciences, 11(19), 11649–11654.

• Abu-raghif, A. R., Jasim, G. A., & Hanoon, M. M. (2017). Anti-proliferative activity of Zizyphus spina-christi leaves methanol extract against rhabdomyosarcoma (RD) cell line. International Journal of Pharmacy and Pharmaceutical Sciences, 9(2), 279–282. https://doi.org/10.22159/ijpps.2017v9i2.15013

• Adamczak, A., Ożarowski, M., & Karpiński, T. M. (2020). Antibacterial activity of some flavonoids and organic acids widely distributed in plants. Journal of Clinical Medicine, 9(1), 109. https://doi.org/10.3390/jcm9010109

• Ads, E. N., Rajendrasozhan, S., Hassan, S. I., Sharawy, S. M. S., & Humaidi, J. R. (2017). Phytochemical, antimicrobial and cytotoxic evaluation of Ziziphus spina-christi (L.) stem bark. Biomedical Research, 28(15), 6646–6653.

• Algammal, A. M., Mohamed, M. F., Tawfiek, B. A., Hozzein, W. N., Kazzaz, W. M. E., & Mabrok, M. (2020). Molecular typing, antibiogram and PCR-RFLP based detection of Aeromonas hydrophila complex isolated from Oreochromis niloticus. Pathogens, 9(3), 238. https://doi.org/10.3390/pathogens9030238

• Alhassan, K. A., Indabawa, A. S., & Shah, M. M. (2019). Phytochemical analysis, proximate composition and antibacterial activities of Ziziphus species (Z. jujube and Z. spina christi). Journal of Applied and Advanced Research, 4(1), 42–46. https://doi.org/10.21839/jaar.2019.v4i1.262

• Al-Mutairi, M. H., Ali, S., Aly, S. M., & Aldebasi, Y. (2016). Antibacterial activity of Sidr (Ziziphus spina-christi), leaves extract against selected pathogenic bacteria. European Journal of Pharmaceutical and Medical Research, 3(5), 138–144.

• Aparna, V., Dileep, K. V., Mandal, P. K., Karthe, P., Sadasivan, C., & Haridas, M. (2012). Anti-inflammatory property of n-hexadecanoic acid: Structural evidence and kinetic assessment. Chemical Biology and Drug Design, 80(3), 434–439. https://doi.org/10.1111/j.1747-0285.2012.01418.x

• Asgarpanah, J., & Haghighat, E. (2012). Phytochemistry and pharmacologic properties of Ziziphus spina christi (L.) Willd. African Journal of Pharmacy and Pharmacology, 6(31), 2332–2339. https://doi.org/10.5897/ajpp12.509

• Atujona, D., Cai, S., & Amenyogbe, E. (2018). Mini review on Vibrio infection - A case study on Vibrio harveyi clade. Fisheries and Aquaculture Journal, 9(4), 1000258. https://doi.org/10.4172/2150-3508.1000258

• Awang-Jamil, Z., Aminuddin, M. F., Zaidi, B. Q., Basri, A. M., Ahmad, N., & Taha, H. (2021). Phytochemicals and antimicrobial analysis of selected medicinal plants from Brunei Darussalam. Biodiversitas, 22(2), 601–606. https://doi.org/10.13057/biodiv/d220211

• Baba, E., Acar, Ü., Öntaş, C., Kesbiç, O. S., & Yilmaz, S. (2016). The use of Avena sativa extract against Aeromonas hydrophila and its effect on growth performance, hematological and immunological parameters in common carp (Cyprinus carpio). Italian Journal of Animal Science, 15(2), 325–333. https://doi.org/10.1080/1828051X.2016.1185977

• Bentzon-Tilia, M., Sonnenschein, E. C., & Gram, L. (2016). Monitoring and managing microbes in aquaculture – Towards a sustainable industry. Microbial Biotechnology, 9(5), 576–584. https://doi.org/10.1111/1751-7915.12392

• Boussaada, O., Ammar, S., Saidana, D., Chriaa, J., Chraif, I., Daami, M., Helal, A. N., & Mighri, Z. (2008). Chemical composition and antimicrobial activity of volatile components from capitula and aerial parts of Rhaponticum acaule DC growing wild in Tunisia. Microbiological Research, 163(1), 87–95. https://doi.org/10.1016/j.micres.2007.02.010

• Bouyahya, A., Abrini, J., Dakka, N., & Bakri, Y. (2019). Essential oils of Origanum compactum increase membrane permeability, disturb cell membrane integrity, and suppress quorum-sensing phenotype in bacteria. Journal of Pharmaceutical Analysis, 9(5), 301-311. https://doi.org/10.1016/j.jpha.2019.03.001

• Brito, S. M. O., Coutinho, H. D. M., Talvani, A., Coronel, C., Barbosa, A. G. R., Vega, C., Figueredo, F. G., Tintino, S. R., Lima, L. F., Boligon, A. A., Athayde, M. L., & Menezes, I. R. A. (2015). Analysis of bioactivities and chemical composition of Ziziphus joazeiro Mart. using HPLC-DAD. Food Chemistry, 186, 185–191. https://doi.org/10.1016/j.foodchem.2014.10.031

• Chen, H. B., Zhang, J., Yu, H. X., & Hu, Q. L. (2007). In vitro study on the antibacterial of a medicinal intermediate, solanesol. Qilu Pharmaceutical Affairs, 26, 558–559.

• Dangoggo, S. M., Hassan, L. G., Sadiq, I. S., & Manga, S. B. (2012). Phytochemical analysis and antibacterial screening of leaves of Diospyros mespiliformis and Ziziphus spina-christi. Chemical Engineering Journal, 1(1), 31–37.

• Doğan, A., Otlu, S., Çelebİ, Ö, Aksu Kiliçle, P., Gülmez Sağlam, A., Doğan, A. N. C., & Mutlu, N. (2017). An investigation of antibacterial effects of steroids. Turkish Journal of Veterinary and Animal Sciences, 41(2), 302–305. https://doi.org/10.3906/vet-1510-24

• Ermias, R., Tukue, M. & Bahlbi, A. (2011). Phytochemical screening of Ziziphus spina-christi and Piper nigrum. Journal of Atoms and Molecules, 1(1), 41–47.

• Filimonov, D. A., Lagunin, A. A., Gloriozova, T. A., Rudik, A. V., Druzhilovskii, D. S., Pogodin, P. V., & Poroikov, V. V. (2014). Prediction of the biological activity spectra of organic compounds using the pass online web resource. Chemistry of Heterocyclic Compounds, 50(3), 444–457. https://doi.org/10.1007/s10593-014-1496-1

• Gull, J., Sultana, B., Anwar, F., Naseer, R., Ashraf, M., & Ashrafuzzaman, M. (2012). Variation in antioxidant attributes at three ripening stages of guava (Psidium guajava L.) fruit from different geographical regions of Pakistan. Molecules, 17(3), 3165–3180. https://doi.org/10.3390/molecules17033165

• Haniffa, M. A., & Kavitha, K. (2012). Antibacterial activity of medicinal herbs against the fish pathogen Aeromonas hydrophila. Journal of Agricultural Technology, 8(1), 205–211.

• Huang, F., Kong, J., Ju, J., Zhang, Y., Guo, Y., Cheng, Y., Qian, H., Xie, Y., & Yao, W. (2019). Membrane damage mechanism contributes to inhibition of trans-cinnamaldehyde on Penicillium italicum using Surface-Enhanced Raman Spectroscopy (SERS). Scientific Reports, 9(1), 490. https://doi.org/10.1038/s41598-018-36989-7

• Ibrahim, J. A., Egharevba, H. O., Nnamdi, R. A., & Kunle, O. F. (2015). Comparative pharmacognostic and phytochemical analysis of Ziziphus spina-christi (L.) Desf. and Ziziphus abyssinica Hochst. ex A. Rich. International Journal of Pharmacognosy and Phytochemical Research, 7(6), 1160–1166.

• Igbinosa, I. H., Beshiru, A., & Igbinosa, E. O. (2017). Antibiotic resistance profile of Pseudomonas aeruginosa isolated from aquaculture and abattoir environments in urban communities. Asian Pacific Journal of Tropical Disease, 7(1), 47–52. https://doi.org/10.12980/apjtd.7.2017D6-363

• Inbathamizh, L., & Padmini, E. (2013). Effect of geographical properties on the phytochemical composition and antioxidant potential of Moringa oleifera flowers. BioMed Research International, 1(3), 239–247.

• Joshua, W. J., & Zulperi, Z. (2020). Effects of Spirulina platensis and Chlorella vulgaris on the immune system and reproduction of fish. Pertanika Journal of Tropical Agricultural Science, 43(4), 429–444. https://doi.org/10.47836/pjtas.43.4.01

• Khaleel, S. M., Jaran, A. S., & Al-Deeb, T. M. F. (2019). Antimicrobial and lipid peroxidation inhibition potential of Ziziphus spina-christi (Sedr), a Jordanian medicinal plant. Journal of Biological Sciences, 19(2), 131–136. https://doi.org/10.3923/jbs.2019.131.136

• Kinnunen, P. K., Kaarniranta, K., & Mahalka, A. K. (2012). Protein-oxidized phospholipid interactions in cellular signaling for cell death: From biophysics to clinical correlations. Biochimica et Biophysica Acta-Biomembranes, 1818(10), 2446-2455. https://doi.org/10.1016/j.bbamem.2012.04.008

• Kumar, D. G., & Rajakumar R. (2016). Gas chromatography mass spectrometry analysis of bioactive components from the ethanol extract of Avicennia marina leaves. Innovare Journal of Science, 4(4), 9-12.

• Mazumder, K., Nabila, A., Aktar, A., & Farahnaky, A. (2020). Bioactive variability and in vitro and in vivo antioxidant activity of unprocessed and processed flour of nine cultivars of Australian lupin species: A comprehensive substantiation. Antioxidants, 9(4), 282. https://doi.org/10.3390/antiox9040282

• Mbunde, M., Mdegela, R. H., Laswai, H. S., & Mabiki, F. P. (2018). Quantification of phenolics, flavonoids and antioxidant activity of Tamarindus indica from selected areas in Tanzania. Biofarmasi Journal of Natural Product Biochemistry, 16(1), 22–28. https://doi.org/10.13057/biofar/f160103

• Mensah-Agyei, G. O., Ayeni, K. I., & Ezeamagu, C. O. (2020). GC-MS analysis of bioactive compounds and evaluation of antimicrobial activity of the extracts of Daedalea elegans: A Nigerian mushroom. African Journal of Microbiology Research, 14(6), 204–210. https://doi.org/10.5897/ajmr2019.9120

• Monteiro, S. H., Andrade, G. M., Garcia, F., & Pilarski, F. (2018). Antibiotic residues and resistant bacteria in aquaculture. The Pharmaceutical and Chemical Journal, 5(4), 127–147.

• Motamedi, H., Seyyednejad, S. M., Hasannejad, Z., & Fariba Dehghani, F. (2014). A comparative study on the effects of Ziziphus spina-christi alcoholic extracts on growth and structural integrity of bacterial pathogens. Iranian Journal of Pharmaceutical Sciences, 10(2), 1- 10.

• Moustafa, M. F., Hesham, A. E. L., Quraishi, M. S., & Alrumman, S. A. (2016). Variations in genetic and chemical constituents of Ziziphus spina-christi L. populations grown at various altitudinal zonation up to 2227 m height. Journal of Genetic Engineering and Biotechnology, 14(2), 349–362. https://doi.org/10.1016/j.jgeb.2016.09.001

• Mulyani, S., Adriani, M., & Wirjatmadi, B. (2021). Antibacterial activity of extract ethanol bidara leaves (Ziziphus spina-christi L.) on Enteropathogenic coli. Indian Journal of Forensic Medicine and Toxicology, 15(1), 1589–1595. https://doi.org/10.37506/ijfmt.v15i1.13638

• Novriadi, R. (2016). Vibriosis in aquaculture. Omni-Akuatika, 12(1), 24. https://doi.org/10.20884/1.oa.2016.12.1.24

• Orhan, I., Özçelik, B., & Şener, B. (2011). Evaluation of antibacterial, antifungal, antiviral, and antioxidant potentials of some edible oils and their fatty acid profiles. Turkish Journal of Biology, 35(2), 251–258. https://doi.org/10.3906/biy-0907-107

• Pan, C. Y., Tsai, T. Y., Su, B. C., Hui, C. F., & Chen, J. Y. (2017). Study of the antimicrobial activity of tilapia piscidin 3 (TP3) and TP4 and their effects on immune functions in hybrid tilapia (Oreochromis spp.). PLOS One, 12(1), e0169678. https://doi.org/10.1371/journal.pone.0169678

• Parasuraman, S. (2011). Prediction of activity spectra for substances. Journal of Pharmacology and Pharmacotherapeutics, 2(1), 52–53. https://doi.org/10.4103/0976-500X.77119

• Pargaputri, A. F., Munadziroh, E., & Indrawati, R. (2016). Antibacterial effects of Pluchea indica Less. leaf extract on E. faecalis and Fusobacterium nucleatum (in vitro). Dental Journal, 49(2), 93–98. https://doi.org/10.20473/j.djmkg.v49.i2.p93-98

• Pohlmann, J., Lampe, T., Shimada, M., Nell, P. G., Pernerstorfer, J., Svenstrup, N., Brunner, N. A., Schiffer, G., & Freiberg, C. (2005). Pyrrolidinedione derivatives as antibacterial agents with a novel mode of action. Bioorganic and Medicinal Chemistry Letters, 15(4), 1189–1192. https:/doi.org/10.1016/j.bmcl.2004.12.002

• Potocki, L., Oklejewicz, B., Kuna, E , Szpyrka, E., Duda, M., & Zuczek, J. (2021). Application of green algal Planktochlorella nurekis biomasses to modulate growth of selected microbial species. Molecules, 26(13), 4038. https://doi.org/10.3390/molecules26134038

• Prabu, E., Felix, S., Felix, N., Ahilan, B., & Ruby, P. (2017). An overview on significance of fish nutrition in aquaculture industry. International Journal of Fisheries and Aquatic Studies, 5(6), 349–355.

• Praja, R. K., & Safnurbaiti, D. P. (2018). The infection of Vibrio parahaemolythicus in shrimp and human. Oceana Biomedicina Journal, 1(1), 44–58. http://doi.org/10.30649/obj.v1i1.6

• Raman, V., Samuel, L., Saradhi, P., Rao, N., Krishna, N. V., Sudhakar, M., & Radhakrishnan, T. (2012). Antibacterial, antioxidant activity and GC-MS analysis of Eupatorium odoratum. Asian Journal of Pharmaceutical and Clinical Research, 5(2), 99–106.

• Ravi, L., Manasvi V., & Praveena Lakshmi, B. (2016). Antibacterial and antioxidant activity of saponin from Abutilon indicum leaves. Asian Journal of Pharmaceutical and Clinical Research, 9(3), 344–347. https://doi.org/10.22159/ajpcr.2016.v9s3.15064

• Riyadi, P. H., Romadhon R., Anggo A. D., Herawati V. E., & Setyastuti A. I. (2020). PASS and ADMET analyses for eight compounds from Nile tilapia (Oreochromis niloticus) viscera waste hydrolysate as anti-inflammatory nutraceutical. AACL Bioflux, 13(5), 2630–2638.

• Sarjito, Haditomo, A. H. C., Desrina, Ariyati R. W., & Prayitno, S. B. (2018a). The diversity of causative agent associated with bacterial diseases on catfish (Clarias gariepinus) with molecular based from Demak, Indonesia. Omni-Akuatika, 14(2), 100–106.

• Sarjito, Haditomo, A. H. C., Desrina, Djunaedi, A., & Prayitno, S. B. (2018b). The bacterial diversity associated with bacterial diseases on mud crab (Scylla serrata Fab.) from Pemalang Coast, Indonesia. In Journal of Physics: Conference Series (Vol. 1025, No. 1, p. 012076). IOP Publishing. https:/doi.org/10.1088/1742-6596/1025/1/012076

• Sarjito, Radjasa O. K, Prayitno, S. B., & Hutabarat, S. (2009). Phylogenetic diversity of the causative agents of vibriosis associated with groupers fish from Karimunjawa Islands, Indonesia. Current Research in Bacteriology, 2(1), 14-21. https://doi.org/10.3923/crb.2009.14.21

• Sarjito, Haditomo, A. H. C, Desrina, Djunaedi, A., & Prayitno S. B. (2018c). The diversity of vibrios associated with vibriosis in pacific white shrimp (Litopenaeus vannamei) from extensive shrimp pond in Kendal District, Indonesia. In IOP Conference Series: Earth and Environmental Science (Vol. 116, No. 1, p. 012011). IOP Publishing. https://doi.org/10.1088/1755-1315/116/1/012011

• Sivakumar, S. R., Radhakrishnan, S., & Kulangiappar, K. (2017). Isolation of N-methyl formamide from red algae Portieria hornemannii (Lyngbye) P.C. Silva active against two plant pathogenic bacteria. American-Eurasian Journal of Agricultural and Environmental Sciences, 17(1), 99–106.

• Soni, H. & Malik, J.K. (2021). Phyto-pharmacological potential of Zizyphus jujube: A review. Scholars International Journal of Biochemistry, 4(2), 1–5. https://doi.org/10.36348/sijb.2021.v04i01.001

• Statistics Indonesia. (2020). Produksi perikanan budidaya menurut provinsi dan jenis budidaya, 2000-2018 [Aquaculture production by province and type of cultivation, 2000-2018]. https://www.bps.go.id/statictable/2009/10/05/1706/produksi-perikanan-budidaya-menurut-provinsi-dan-jenis-budidaya-2000-2017.html

• Stein, S. E., Mikaia, A., White, E., Zaikin, V., Zhu, D., Sparkman, O. D., Neta, P., & Zenkevich, I. (2014). NIST Standard Reference Database 1A. https://www.nist.gov/document/nist1aver22manpdf

• Suliman, M. B., & Mohammed, A. A. (2018). Preliminary phytochemical screening and antibacterial activity of ethanolic and aqueous extracts of Sudanese medicinal plant Ziziphus spina-christi L. leaves. Arabian Journal of Medicinal and Aromatic Plants, 4(1), 35–44.

• Swamy, M. K., Arumugam, G., Kaur, R., Ghasemzadeh, A., Yusoff, M. M., & Sinniah, U. R. (2017). GC-MS based metabolite profiling, antioxidant and antimicrobial properties of different solvent extracts of Malaysian Plectranthus amboinicus leaves. Evidence-Based Complementary and Alternative Medicine, 2017, 1517683. https://doi.org/10.1155/2017/1517683

• Taghipour, M. T., Nameni, R., Taghipour, M., & Ghorat, F. (2020). Phytochemical analysis and antimicrobial activity of Ziziphus spina-christi and Tamarix aphylla leaves’ extracts as effective treatment for Coronavirus Disease 2019 (COVID-19). Thrita, 9(2), e107776. https://doi.org/10.5812/thrita.107776

• Temerk, H. A., Salem, W. M., Sayed, W. F., & Hassan, F. S. (2017). Antibacterial effect of phytochemial extracts from Ziziphus spina-christi against some pathogenic bacteria. Egyptian Journal of Botany, 57(3), 595–604. https://doi.org/10.21608/ejbo.2017.665.1035

• Thawabteh, A., Juma, S., Bader, M., Karaman, D., Scrano, L., Bufo, S. A., & Karaman, R. (2019). The biological activity of natural alkaloids against herbivores, cancerous cells and pathogens. Toxins, 11(11), 656. https://doi.org/10.3390/toxins11110656

• Tran, N., Rodriguez, U. P., Chan, C. Y., Phillips, M. J., Mohan, C. V., Henriksson, P. J. G., Koeshendrajana, S., Suri, S., & Hall, S. (2017). Indonesian aquaculture futures: An analysis of fish supply and demand in Indonesia to 2030 and role of aquaculture using the AsiaFish model. Marine Policy, 79, 25–32. https://doi.org/10.1016/j.marpol.2017.02.002

• Ulanowska, K., Tkaczyk, A., Konopa, G., & Węgrzyn, G. (2006). Differential antibacterial activity of genistein arising from global inhibition of DNA, RNA and protein synthesis in some bacterial strains. Archives of Microbiology, 184(5), 271-278. https://doi.org/10.1007/s00203-005-0063-7

• Wu, Y., Bai, J., Zhong, K., Huang, Y., Qi, H., Jiang, Y., & Gao, H. (2016). Antibacterial activity and membrane-disruptive mechanism of 3-p-trans-coumaroyl-2-hydroxyquinic acid, a novel phenolic compound from pine needles of Cedrus deodara, against Staphylococcus aureus. Molecules, 21(8), 1084. https://doi.org/10.3390/molecules21081084

• Yoon, B. K., Jackman, J. A., Valle-Gonzalez, E. R., & Cho, N. J. (2018). Antibacterial free fatty acids and monoglycerides: Biological activities, experimental testing, and therapeutic applications. International Journal of Molecular Sciences, 19(4), 1114. https://doi.org/10.3390/ijms19041114