Screening of sponge-associated bacteria to control vibriosis in vannamei shrimp (Litopenaeus vannamei)
##plugins.themes.bootstrap3.article.sidebar##
Issue
Section
Articles
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
##plugins.themes.bootstrap3.article.main##
SARJITO SARJITO
♥
ROSA AMALIA
https://orcid.org/0000-0003-4281-4064
ANINDITIA SABDANINGSIH
https://orcid.org/0000-0001-8822-5535
Abstract
Abstract. Sarjito S, Amalia R, Sabdaningsih A. 2022. Screening of sponge-associated bacteria to control vibriosis in vannamei shrimp (Litopenaeus vannamei). Biodiversitas 23: 5333-5341. An intensive shrimp culture with a high stocking density causes a higher chance of vannamei shrimp being infected with diseases. The most frequent disease is caused by Vibrio sp. Vibrio might cause a severe production loss in the shrimp culture, leading to larvae and mature stadium mortality at 50%. Therefore, a study on the alternative management of vibriosis disease using biocontrol agents is urgently needed. The sponge is a marine invertebrate that provides as a shelter for microbes to live and symbiosis with the animal. An evident ability of sponge-associated bacteria to produce antimicrobial compounds can be exploited as a biodegradable bio-agent, potentially as a solution to control vibriosis disease in a shrimp. This research aimed to isolate sponge-associated bacteria with vibriosis antibacterial potential. Sampling was done in Tulamben, Bali and Panjang island, Jepara, Indonesia with six sampling sites consisting of 15 sampling points. Moreover, vibriosis bacteria were provided by the laboratory of fish disease at Balai Besar Perikanan Budidaya Air Payau (BBPBAP) Jepara. Totally, 24 and 47 pure cultures were successfully isolated using Zobell 2216E agar medium from Tulamben, Bali and Panjang Island, Jepara respectively. The isolates were tested for antibacterial assay using plug agar diffusion methods. The top eight potential isolates were found in isolate B6.3C, B6.3D, B6.4E, B9.3C, PA.1, PA.4, PC.3, and PH.1 against Vibrio vulnificus, V. anguillarum, V. alginolyticus, V. parahaemolyticus, however there was no activity in V. harveyi. The molecular method was carried out to identify those potential isolates using universal primer 16S rRNA. The BLAST homology showed that all potential antibacterial isolates belong to the family Bacilllaceae, such as Bacillus cereus, Virgibacillus salarius, B. aerius, B. paramycoides, B. thuringiensis, and B. altitudinis. Further research will be carried out on microencapsulation and in vivo tests.
##plugins.themes.bootstrap3.article.details##
References
Altschul, S.F., Madden, T.L., Schaffer, A.A. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402. doi: 10.1093/nar/25.17.3389
Amalia, R., Ayuningrum, D., Sabdono, A., and Radjasa, O. K. (2021). Antipathogenic Activity of Acroporid Bacterial Symbionts Against Brown Band Disease-Associated Bacteria. Squalen Bulletin of Marine and Fisheries Postharvest and Biotechnology, 16(2). 65–74. https://doi.org/10.15578/squalen.536
Anteneh, Y. S., Yang, Q., Brown, M. H., and Franco, C. M. M. (2021). Antimicrobial activities of marine sponge-associated bacteria. Microorganisms, 9(1),1–19. https://doi.org/10.3390/microorganisms9010171
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. https://doi.org/10.1016/j.jpha.2015.11.005
Barman, P., Bandyopadhyay, P., Kati, A., Paul, T., Mandal, A. K., Mondal, K. C., & Mohapatra, P. K. das. (2018). Characterization and Strain Improvement of Aerobic Denitrifying EPS Producing Bacterium Bacillus cereus PB88 for Shrimp Water Quality Management. Waste and Biomass Valorization, 9(8), 1319–1330. https://doi.org/10.1007/s12649-017-9912-2
Barman, P., Kati, A., Mandal, A. K., Bandyopadhyay, P., & Mohapatra, P. K. das. (2017). Biopotentiality of Bacillus cereus PB45 for nitrogenous waste detoxification in ex situ model. Aquaculture International, 25(3), 1167–1183. https://doi.org/10.1007/s10499-016-0105-y
Bayer, K., Kamke, J., and Hentschel, U. 2014. Quantification of bacterial and archaeal symbionts in high and low microbial abundance sponges using real-time PCR. FEMS Microbiology Ecology, 89(3), 679–690. https://doi.org/10.1111/1574-6941.12369.
Cappuccino,JG, and Sherman,N. (1987). Microbiology: A Laboratory Manual. The Benjamin or Cummings Publishing Company,Inc. Clifornia. DOI : 10.12691/ajmr-1-4-6.
Chandrakala, N., & Priya, S. (2017). Vibriosis in Shrimp Aquaculture A Review. International Journal of Scientific Research in Science, Engineering and Technology, 3, 27– 23.
Chin-Fa Hwang, Yi-An Chen, Chen Luo, Wen-Dee Chiang. Antioxidant and antibacterial activities of peptide fractions from flaxseed protein hydrolysed by protease from Bacillus altitudinis HK02. 51(3): 681-689. doi.org/10.1111/ijfs.13030.
Chythanya, R., Karunasagar, I., & Karunasagar, I. (2002). Inhibition of Shrimp Pathogenic Vibrios by a Marine Pseudomonas I-2 Strain. Aquaculture, 208, 1–10. https://doi.org/10.1016/S0044-8486(01)00714-1
Colin, P. L., and Arneson, C. 1995. Tropical Pacific Invertebrates: A Field Guide to the Marine Invertebrates Occurring on Tropical Pacific Coral Reefs, Seagrass Beds and Mangroves. The Coral Reef Press.
Crespo-Piazuelo, D., Lawlor, P.G., Ranjitkar, S. et al. 2021. Intestinal microbiota modulation and improved growth in pigs with post-weaning antibiotic and ZnO supplementation but only subtle microbiota effects with Bacillus altitudinis. Sci Rep 11, 23304 (2021). https://doi.org/10.1038/s41598-021-01826-x.
de Voogd, N. J. 2004. Callyspongia (Euplacella) biru spec. nov. (Porifera: Demospongiae: Haplosclerida) from Indonesia. Zoologische Mededelingen, 78(18–28), 477. http://www.repository.naturalis.nl/record/214454.
de Voogd, N. J. 2005. Indonesian sponges : biodiversity and mariculture potential [PhD Thesis, University of Amsterdam]. https://dare.uva.nl.
Diah Ayuningrum, Sakti Imam Muchlissin, Agus Trianto, Ocky Karna Radjasa, Agus Sabdono. 2020. Crude extract from a hardcoral-associated bacterium Virgibacillus salariusPHC-44-04 inhibiting growth of Multidrug-Resistant Enterobacter aerogeneshuman pathogen. Biofarmasi J Nat Prod Biochem. 18(2): 82-87. DOI: 10.13057/biofar/f180205.
Elma Laura Salazar-Marroquín, Luis J. Galán-Wong, Víctor Ricardo Moreno-Medina, Miguel Ángel Reyes-López, Benito Pereyra-Alférez. 2016. Bacteriocins synthesized by Bacillus thuringiensis: generalities and potential applications. Rev Med Microbiol. 27(3): 95–101. doi: 10.1097/MRM.0000000000000076.
Feliatra, F., Batubara, U. M., Nurulita, Y., Lukistyowati, I., & Setiaji, J. (2021). The potentials of secondary metabolites from Bacillus cereus SN7 and Vagococcus fluvialis CT21 against fish pathogenic bacteria. Microbial Pathogenesis, 158(July 2020), 105062. https://doi.org/10.1016/j.micpath.2021.105062.
Giles, E. C., Kamke, J., Moitinho-Silva, L., Taylor, M. W., Hentschel, U., Ravasi, T., and Schmitt, S. 2013. Bacterial community profiles in low microbial abundance sponges. FEMS Microbiology Ecology, 83(1), 232–241. https://doi.org/10.1111/j.1574-6941.2012.01467.x
Gloeckner, V., Wehrl, M., Moitinho-Silva, L., Gernert, C., Hentschel, U., Schupp, P., Pawlik, J. R., Lindquist, N. L., Erpenbeck, D., Wörheide, G., and Wörheide, G. 2014. The HMA-LMA dichotomy revisited: An electron microscopical survey of 56 sponge species. Biological Bulletin, 227(1), 78–88. https://doi.org/10.1086/BBLv227n1p78
Gopal, S., Otta, S.K., Kumar, S., Karunasagar, I., Nishibuchi, M., & Karunasagar, I. (2005). The Occurrence of Vibrio Species in Tropical Shrimp Culture Environments; Implications for Food Safety. International Journal of Food Microbiology, 102, 151–159. https://doi.org/10.1016/j.ijfoodmicro.2004.12.011.
Hameed, A.S.S. (1993). A Study of the Aerobic Heterotrophic Bacterial Flora of Hatchery-Reared Eggs, Larvae and Postlarvae of Penaeus. DOI: 10.1016/0044-8486(93)90319-T.
Hamza, A., Fdhila, K., Zouiten, D., & Masmoudi, A. S. (2016). Virgibacillus proomii and Bacillus mojavensis as probiotics in sea bass (Dicentrarchus labrax) larvae: effects on growth performance and digestive enzyme activities. Fish Physiology and Biochemistry, 42(2), 495–507. https://doi.org/10.1007/s10695-015-0154-6
Hardoim, C. C. P., and Costa, R. 2014. Microbial communities and bioactive compounds in marine sponges of the family irciniidae-A review. Marine Drugs, 12(10), 5089–5122. https://doi.org/10.3390/md12105089.
Hooper, J. N. A. 2003. ‘Sponguide’. Guide To Sponge Collection and Identification.
Hooper, J. N. A., Soest, R. W. M. van., and Willenz, Philippe. 2002. Systema Porifera?: a guide to the classification of sponges. Kluwer Academic/Plenum Publishers.
Jung, W.J. Mabood, Fazli; Souleimanov, Alfred; Zhou, Xiaomin. Jaoua, Samir; Kamoun, Fakher; Smith, Donald L. 2008. Stability and Antibacterial Activity of Bacteriocins Produced by Bacillus thuringiensis and Bacillus thuringiensis ssp. Kurstaki. Journal of Microbiology and Biotechnology. 18(11): 1836-1840. DOI: 10.4014/jmb.0800.120
Kelly, J. B., Carlson, D. E., Low, J. S., Rice, T., and Thacker, R. W. 2021. The Relationship Between Microbiomes and Selective Regimes in the Sponge Genus Ircinia. Frontiers in Microbiology, 12(March), 1–16. https://doi.org/10.3389/fmicb.2021.607289
Khan, S. T., Takagi, M., and Shin-Ya, K. 2011. Actinobacteria associated with the marine sponges Cinachyra sp., Petrosia sp., and Ulosa sp. and their culturability. Microbes and Environments, 27(1), 99–104. https://doi.org/10.1264/jsme2.ME11270.
Kumar, B.K., Deekshit, V.K., Raj, R.M., Rai, P., Shivanagowda, B.M., and Karunasagar, I. 2014. The Diversity of Vibrio parahaemolyticus Associated with Disease Outbreak Among Cultured Litopenaeus vannamei (Pacific White Shrimp) in India. Aquaculture, 433, 247–251. https://doi.org/10.1016/j.aquaculture.2014.06.016.
Kumar, S., Stecher, G., Li, M., Knyaz, C., dan Tamura, K. (2018). Mega X: Molecular Evolutionary Genetics Analysis Across Computing Platforms. Molecular Biology and Evolution, 35(6), 1547–1549. https://doi.org/10.1093/molbev/msy096.
Lightner, D.V., 1996. A Handbook of pathology and diagnostic Procedures for Diseases of Penaeid Shrimp. Baton Rouge, LA, USA: World Aquaculture Society.
Meidong R, Khotchanalekha K, Doolgindachbaporn S, Nagasawa T, Nakao M, Sakai K, Tongpim S. 2018. Evaluation of probiotic Bacillus aerius B81e isolated from healthy hybrid catfish on growth, disease resistance and innate immunity of Pla-mong Pangasius bocourti. Fish Shellfish Immunol. 73:1-10. doi: 10.1016/j.fsi.2017.11.032.
Miller RA, Beno SM, Kent DJ, Carroll LM, Martin NH, Boor KJ, Kovac J. 2016. Bacillus wiedmannii sp. nov., a psychrotolerant and cytotoxic Bacillus cereus group species isolated from dairy foods and dairy environments. Int J Syst Evol Microbiol. 66(11):4744-4753. doi: 10.1099/ijsem.0.001421.
Mingqi Sun, Shuhong Ye, Zhichao Xu, Lu Wan & Yuguang Zhao. 2021. Endophytic Bacillus altitudinis Q7 from Ginkgo biloba inhibits the growth of Alternaria alternata in vitro and its inhibition mode of action, Biotechnology & Biotechnological Equipment, 35:1, 880-894, DOI: 10.1080/13102818.2021.1936639.
Mondol, M. A. M., Shin, H. J., & Islam, M. T. (2013). Diversity of secondary metabolites from marine bacillus species: Chemistry and biological activity. Marine Drugs, 11(8), 2846–2872. https://doi.org/10.3390/md11082846
Motta, A. S., Flores, F. S., Souto, A. A., & Brandelli, A. (2008). Antibacterial activity of a bacteriocin-like substance produced by Bacillus sp. P34 that targets the bacterial cell envelope. Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology, 93(3), 275–284. https://doi.org/10.1007/s10482-007-9202-2
Oscáriz, J. C., and Pisabarro, A. G. (2000). Characterization and mechanism of action of cerein 7, a bacteriocin produced by Bacillus cereus Bc7. Journal of Applied Microbiology, 89(2), 361–369. https://doi.org/10.1046/j.1365-2672.2000.01123.x
Panigrahi, A., Das, R. R., Sivakumar, M. R., Saravanan, A., Saranya, C., Sudheer, N. S., Kumaraguru Vasagam, K. P., Mahalakshmi, P., Kannappan, S., & Gopikrishna, G. (2020). Bio-augmentation of heterotrophic bacteria in biofloc system improves growth, survival, and immunity of Indian white shrimp Penaeus indicus. Fish and Shellfish Immunology, 98(January), 477–487. https://doi.org/10.1016/j.fsi.2020.01.021
Poppell, E., Weisz, J., Spicer, L., Massaro, A., Hill, A., and Hill, M. 2014. Sponge heterotrophic capacity and bacterial community structure in high- and low-microbial abundance sponges. Marine Ecology, 35(4), 414–424. https://doi.org/10.1111/maec.12098.
Prokof’eva, N. G., Kalinovskaya, N. I., Luk’yanov, P. A., Shentsova, E. B., & Kuznetsova, T. A. (n.d.). The membranotropic activity of cyclic acyldepsipeptides from bacterium Bacillus pumilus, associated with the marine sponge Ircinia sp.
Ravi, A. v., Musthafa, K. S., Jegathammbal, G., Kathiresan, K., & Pandian, S. K. (2007). Screening and evaluation of probiotics as a biocontrol agent against pathogenic Vibrios in marine aquaculture. In Letters in Applied Microbiology (Vol. 45, Issue 2, pp. 219–223). https://doi.org/10.1111/j.1472-765X.2007.02180.x
Rivka Cahan, Hen Friman, Yeshayahu Nitzan. 2008. Antibacterial activity of Cyt1Aa from Bacillus thuringiensis subsp. Israelensis. Microbiology, 154, 3529–3536. DOI 10.1099/mic.0.2008/020784-0.
Roets-Dlamini, Y., Lalloo, R., Moonsamy, G., Kumari, S., Nasr, M., Ramchuran, S., & Bux, F. (2022). Development of Bacillus spp. consortium for one-step “Aerobic Nitrification-Denitrification” in a fluidized-bed reactor. Bioresource Technology Reports, 17(September 2021), 100922. https://doi.org/10.1016/j.biteb.2021.100922
Ruangpan, L., and Kitao, T. (1991). Vibrio Bacteria Isolated From Black Tiger Shrimp, Penaeus monodon Fabricius. Journal of Fish diseases, 14(3), 383-388. DOI:10.1111/j.1365-2761.1991.tb00836.x
Sabdaningsih, A., Liu Y., Mettal, U., Heep, J., Riyanti, Wang, L., Cristianawatio, O., Nuryadi, H., Triandala Sibero, M., Marner, M., Radjasa, O.K., Sabdono, A., Trianto, A., Schaberle, T.F. 2020. A New Citrinin Derivative from the Indonesian Marine Sponge-Associated Fungus Penicillium Citrinum. Marine Drugs. 18(4): 227. Doi: 10.3390/MD18040227.
Saitou, Naruya and Masatoshi Nei (1987) The Neighbor-Joining Method: A New Method For Reconstructing Phylogenetic Trees. Molecular Biology and Evolution, vol. 4, pp. 406-425. DOI : 10.1093/oxfordjournals.molbev.a040454.
Sarjito, Haditomo, A.H.C., Djunaedi, A., and Prayitno, S.B. 2018. The Diversity of Vibrios Associated with Vibriosis in Pacific White Shrimp (Litopenaeus vannamei) from Extensive Shrimp Pond in Kendal District, Indonesia. IOP Conference Series: Earth and Environmental Science, 116. https://doi.org/10.1088/1755-1315/116/1/012011.
Sarjito, S.B. Prayitno, M.Y. Farisa, R.T.C. Nast, R. Kristiana, A. Sabdaningsih, and A. Sabdono. Exploration of Bacteria Associated with Nudribranchs to Control Vibrio spp. IOP Conf. Series: Earth and Environmental Science, 530: 012031. DOI: 10.1088/ 1755-1315/530/1/012031.
Sarjito and Sabdono, A. 2021. Associated Vibrio Species in Shrimp Vibriosis from Traditional Brackish Water Pond in the North Coastal of Central Java, Indonesia. Genetics of Aquatic Organism, 5(2): 45-54. DOI: 10.4194/2459-1831-v5_2_01.
Setiaji, J., Feliatra, F., Teruna, H. Y., Lukistyowati, I., Suharman, I., Muchlisin, Z. A., & Johan, T. I. (2020). Antibacterial activity in secondary metabolite extracts of heterotrophic bacteria against Vibrio alginolyticus, Aeromonas hydrophila, and Pseudomonas aeruginosa. F1000Research, 9, 1–11. https://doi.org/10.12688/f1000research.26215.1
Shivaji S, Chaturvedi P, Suresh K, Reddy GSN, Dutt CBS, Wainwright M, Narlikar JV, Bhargava PM. 2006. Bacillus aerius sp. nov., Bacillus aerophilus sp. nov., Bacillus stratosphericus sp. nov. and Bacillus altitudinis sp. nov., isolated from cryogenic tubes used for collecting air samples from high altitudes. Int J Syst Evol Microbiol. 56(Pt 7):1465-1473. doi: 10.1099/ijs.0.64029-0.
Sibero, M.T., Radjasa, O.K., Sabdono, A., Trianto, A., Triningsih, D.W. and Hutagaol, I.D. 2018. Antibacterial activity of indonesian sponge associated fungi against clinical pathogenic multidrug resistant bacteria. Journal of Applied Pharmaceutical Science 8(2): 88-94. DOI: 10.7324/JAPS.20 18.8214.
Singh, B.I. 1986. Studies on the Bacteria Associated with Penaeus indicus in a Culture System. Ph.D. Thesis. Cochin University of Science and Technology, Cochin, India, 230 pp.
Stalin N, Srinivasan P. Efficacy of potential phage cocktails against Vibrio harveyi and closely related Vibrio species isolated from shrimp aquaculture environment in the south east coast of India. Vet Microbiol. 2017 Aug;207:83-96. doi: 10.1016/j.vetmic.2017.06.006. Epub 2017 Jun 9. PMID: 28757045.
Steinert, G., Taylor, M. W., Deines, P., Simister, R. L., de Voogd, N. J., Hoggard, M., and Schupp, P. J. 2016. In four shallow and mesophotic tropical reef sponges from Guam the microbial community largely depends on host identity. PeerJ, 2016(4). https://doi.org/10.7717/peerj.1936.
Sulistiyani, S.A. Nugraheni, Miftahuddin Majid Khoeri, Agus Sabdono, and Ocky Karna Radjasa. 2010. Antibacterial Activity of Bacterial Symbionts of Softcoral Sinularia sp. Against Pathogenic Resistant Bacteria. Journal of Coastal Development. 13(2): 113-118. ISSN : 1410-5217.
Sumi, C. D., Yang, B. W., Yeo, I. C., & Hahm, Y. T. (2015). Antimicrobial peptides of the genus Bacillus: A new era for antibiotics. Canadian Journal of Microbiology, 61(2), 93–103. https://doi.org/10.1139/cjm-2014-0613
Susilowati, Ragil, Sabdono, Agus and Widowati, Ita. 2015. Isolation and Characterization of Bacteria Associated with Brown Algae Sargassum spp. from Panjang Island and their Antibacterial Activities. Procedia Environmental Sciences. 23. 10.1016/j.proenv.2015.01.036.
Teplitski, M., & Ritchie, K. (2009). How feasible is the biological control of coral diseases?. Trend in Ecology and Evolution, 24(7), 378-385. doi: 10.1016/j.tree.2009.02.008.
Thakur, N. L., & Anil, A. C. (2000). Antibacterial activity of the sponge Ircinia ramosa: Importance of its surface-associated bacteria. Journal of Chemical Ecology, 26(1), 57–71. https://doi.org/10.1023/A:1005485310488
Thakur, N.L., & Müller, W.E. 2004. Biotechnological Potential of Marine Sponges. J. Current Science. 86 (11): 1506–1512.
Thakur, N.L., Thakur A.N, dan Muller W.E. (2005). Marine Natural Product in Drug Discovery. Natural Product Radiance. 4 (6): 471 – 478.
Thomas, T., Lucas M.S., Miguel, L., Johannes, R.B., Cole, E., Carmen A.G., Julie, B.O., Patrick, M.E., Susanna, L.L., Heidi, L., Andia, C.F., Rodrigo, C., Peter, J.S., Laura, S., Dirk, E., Jack, G., Rob, K., Gail, A., Jose, V.L., Michael, W.T., Robert, W.T., Jose, M.M., Ute, H., and Nicole, S.W. Diversity, Structure and Convergent Evolution of The Global Sponge Microbiome. 7:11870. Doi: 10.1038/ncomms11870.
Trianto, A., Radjasa, O. K., Sabdono, A., Muchlissin, S. I., Afriyanto, R., Sulistiowati, McCauley, E. (2019). Exploration culturable bacterial symbionts of sponges from ternate islands, Indonesia. Biodiversitas, 20(3), 776–782. https://doi.org/10.13057/biodiv/d200323
Turon, M., and Uriz, M. J. 2020. New Insights Into the Archaeal Consortium of Tropical Sponges. Frontiers in Marine Science, 6. https://doi.org/10.3389/fmars.2019.00789
Turon, M., Cáliz, J., Garate, L., Casamayor, E. O., and Uriz, M. J. 2018. Showcasing the role of seawater in bacteria recruitment and microbiome stability in sponges. Scientific Reports, 8(1). https://doi.org/10.1038/s41598-018-33545-1
van Soest, R. W. M. 1989. The Indonesian sponge fauna: A status report. Netherlands Journal of Sea Research, 23(2), 223–230. https://doi.org/10.1016/0077-7579(89)90016-1.
Wang, J., Zhang, L., Teng, K., Sun, S., Sun, Z., & Zhong, J. (2014). Cerecidins, novel lantibiotics from bacillus cereus with potent antimicrobial activity. Applied and Environmental Microbiology, 80(8), 2633–2643. https://doi.org/10.1128/AEM.03751-13
Most read articles by the same author(s)
- DIAH AYUNINGRUM, ANINDITIA SABDANINGSIH, OKTAVIANTO EKO JATI, Screening of actinobacteria-producing amylolytic enzyme in sediment from Litopenaeus vannamei (Boone, 1931) ponds in Rembang District, Central Java, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 22 No. 4 (2021)
- DESRINA, BudiSLAMET B. PRAYITNO, ALFABETIAN HARJUNO CONDRO HADITOMO, RUSTHESA LATRITIANI, SARJITO SARJITO, Detection of Enterocytozoon hepatopenaei (EHP) DNA in the polychaetes from shrimp ponds suffering white feces syndrome outbreaks , Biodiversitas Journal of Biological Diversity: Vol. 21 No. 1 (2020)
- ROSA AMALIA, SRI REJEKI, LESTARI LAKSHMI WIDOWATI, RESTIANA WISNU ARIYATI , The growth of tiger shrimp (Penaeus monodon) and its dynamics of water quality in integrated culture , Biodiversitas Journal of Biological Diversity: Vol. 23 No. 1 (2022)
- OLVI CRISTIANAWATI, ANINDITIA SABDANINGSIH, LEONTINE ELISABETH BECKING, MIFTAHUDIN MAJID KHOERI, HANDUNG NURYADI, AGUS SABDONO, AGUS TRIANTO, OCKY KARNA RADJASA, Biological activity of sponge-associated fungi from Karimunjawa Islands, Indonesia against pathogenic Streptococcus pneumoniae , Biodiversitas Journal of Biological Diversity: Vol. 20 No. 8 (2019)