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Isolation, Identification, and Pathogenicity of Potential Probiotics Isolated from Intestinal Coconut Crab (Birgus latro Linnaeus, 1767)
Corresponding Author(s) : Muhammad Aris
Jurnal Ilmiah Perikanan dan Kelautan,
Vol. 16 No. 1 (2024): JURNAL ILMIAH PERIKANAN DAN KELAUTAN
Abstract
Abstract
The supply of coconut crabs (Birgus latro Linnaeus, 1767) has been sourced from capture in the wild. Development efforts in aquaculture have succeeded in producing eggs. However, further development with larval maintenance failed because it was constrained by a low survival rate. This study aimed to identify the potential probiotic bacteria in coconut crabs. Coconut crab samples were collected from Moor Island, South Patani District, Central Halmahera Regency, North Maluku Province, Indonesia. The intestines of coconut crabs were taken as much as 1 g, then ground on a porcelain dish and added to Tri-Salt. The scouring liquid was taken in 0.1 ml and spread on a petri dish containing Nutrient Agar. The isolated used were marked with BL1, BL2, BL3, BL4, and BL5. Molecular identification was performed with sequencing and then analyzed using the Basic Local Alignment Search Tool (BLAST). The selection of isolates from the gastrointestinal tract of coconut crabs showed that the bacteria obtained were Enterobacter tabaci (BL1), Enterobacter hormaechei (BL2), Bacillus horneckiae (BL3), Pseudomonas stutzeri (BL4), and Acinetobacter variabilis (BL5). Further testing revealed that the bacteria A. variabilis (BL5) is a probiotic isolate in coconut crabs.
Highlight Research
- The intestinal bacteria from coconut crabs identified were E. tabaci, E. hormaechei, B. horneckiae, P. stutzeri, and A. variabilis.
- The E. tabaci strain BL1, E. hormaechei strain BL2, B. Horneckiae strain BL3, and P. stutzeri strain BL4 are pathogenic bacteria.
- The A. variabilis strain BL5 is potential probiotics bacteria.
- The A. variabilis strain BL5 showed a better survival rate than other isolates.
Keywords
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- Altaff, K. (2020). Indigenous live feed for aqua hatchery larval rearing of finfish and shellfish: A review. International Journal of Zoological Investigations, 6(1):162-173.
- Anokyewaa, M. A., Amoah, K., Li, Y., Lu, Y., Kuebutornye, F. K., Asiedu, B., & Seidu, I. (2021). Prevalence of virulence genes and antibiotic susceptibility of Bacillus used in commercial aquaculture probiotics in China. Aquaculture Reports, 21:100784.
- Bunnoy, A., Na-Nakorn, U., & Srisapoome, P. (2019). Probiotic effects of a novel strain, Acinetobacter KU011TH, on the growth performance, immune responses, and resistance against Aeromonas hydrophila of bighead catfish (Clarias macrocephalus Günther, 1864). Microorganisms, 7(12):613.
- Chiu, S. T., Chu, T. W., Simangunsong, T., Ballantyne, R., Chiu, C. S., & Liu, C. H. (2021). Probiotic, Lactobacillus pentosus BD6 boost the growth and health status of white shrimp, Litopenaeus vannamei via oral administration. Fish & Shellfish Immunology, 117:124-135.
- Dong, J., Zhang, L., Zhou, S., Xu, N., Yang, Q., Liu, Y., & Ai, X. (2020). Identification of a multi-resistant Enterobacter cloacae strain from diseased crayfish (Procambarus clarkii). Aquaculture Reports, 17:100405.
- Drew, M. M., Harzsch, S., Stensmyr, M., Erland, S., & Hansson, B. S. (2010). A review of the biology and ecology of the robber crab, Birgus latro (Linnaeus, 1767) (Anomura: Coenobitidae). Zoologischer Anzeiger - A Journal of Comparative Zoology, 249(1):45-67.
- Hamasaki, K., Yamashita, S., Ishiyama, N., & Kitada, S. (2013). Effects of water availability and migration timing from sea to land on survival and moulting in megalopae and juveniles of the coconut crab, Birgus latro: Implications for mass production of juveniles. Journal of Crustacean Biology, 33(5):627-632.
- He, R. Z., Li, Z. C., Li, S. Y., & Li, A. X. (2021). Development of an immersion challenge model for Streptococcus agalactiae in Nile tilapia (Oreochromis niloticus). Aquaculture, 531:735877.
- Hindu, S. V., Chandrasekaran, N., Mukherjee, A., & Thomas, J. (2018). Effect of dietary supplementation of novel probiotic bacteria Bacillus vireti 01 on antioxidant defence system of freshwater prawn challenged with Pseudomonas aeruginosa. Probiotics and Antimicrobial Proteins, 10:356-366.
- Jefri, M., Satyantini, W. H., Sahidu, A. M., & Nindarwi, D. D. (2020). Application of Probiotics for Organic Matter and Enhancement of Growth Performance in White Shrimp (Litopenaeus vannamei). Jurnal Ilmiah Perikanan Dan Kelautan, 12(1):97-104.
- Lee, C., Kim, S., Shin, J., Kim, M. G., Gunathilaka, B. E., Kim, S. H., Kim, J. E., Ji, S. C., Han, J. E., & Lee, K. J. (2021). Dietary supplementations of Bacillus probiotic improve digestibility, growth performance, innate immunity, and water ammonia level for Pacific white shrimp, Litopenaeus vannamei. Aquaculture International, 29(6):2463-2475.
- Ma, R., Wang, Y., Zhao, L., Zhou, J., Zhao, S., Li, X., Dai, X., & Fang, W. (2020). Exploration of the death causes in zoea stages of Macrobrachium rosenbergii based on microbial diversity analysis. Aquaculture, 519:734710.
- Maas, R. M., Deng, Y., Dersjant-Li, Y., Petit, J., Verdegem, M. C., Schrama, J. W., & Kokou, F. (2021). Exogenous enzymes and probiotics alter digestion kinetics, volatile fatty acid content and microbial interactions in the gut of Nile tilapia. Scientific Reports, 11(1):1-16.
- Mohamad, N., Manan, H., Sallehhuddin, M., Musa, N., & Ikhwanuddin, M. (2020). Screening of Lactic Acid Bacteria isolated from giant freshwater prawn (Macrobrachium rosenbergii) as potential probiotics. Aquaculture Reports, 18:100523.
- Muttharasi, C., Gayathri, V., Muralisankar, T., Mohan, K., Uthayakumar, V., Radhakrishnan, S., Kumar, P., & Palanisamy, M. (2021). Growth performance, digestive enzymes and antioxidants activities in the shrimp Litopenaeus vannamei fed with Amphiroa fragilissima crude polysaccharides encapsulated Artemia nauplii. Aquaculture, 545:737263.
- Nimrat, S., Khaopong, W., Sangsong, J., Boonthai, T., & Vuthiphandchai, V. (2021). Dietary administration of Bacillus and yeast probiotics improves the growth, survival, and microbial community of juvenile whiteleg shrimp, Litopenaeus vannamei. Journal of Applied Aquaculture, 33(1):15-31.
- Ninwichian, P., Phuwan, N., & Limlek, P. (2022). Effects of tank color on the growth, survival rate, stress response, and skin color of juvenile hybrid catfish (Clarias macrocephalus x Clarias gariepinus). Aquaculture, 554:738129.
- Nuidate, T., Kuaphiriyakul, A., Surachat, K., & Mittraparp-Arthorn, P. (2021). Induction and genome analysis of HY01, a newly reported prophage from an emerging shrimp pathogen Vibrio campbellii. Microorganisms, 9(2):400.
- Oliveira, R. V., Oliveira, M. C., & Pelli, A. (2017). Disease infection by Enterobacteriaceae family in fishes: a review. Journal of Microbiology & Experimentation, 4(5):00128.
- Osman, K. M., da Silva Pires, Á., Franco, O. L., Saad, A., Hamed, M., Naim, H., Ali, A. H. M., & Elbehiry, A. (2021). Nile tilapia (Oreochromis niloticus) as an aquatic vector for Pseudomonas species of medical importance: Antibiotic resistance association with biofilm formation, quorum sensing and virulence. Aquaculture, 532:736068.
- Poupin, J., Zubia, M., Gravier-Bonnet, N., Chabanet, P., & Duhec, A. (2013). Crustacea Decapoda of Glorieuses Islands, with notes on the distribution of the coconut crab (Birgus latro) in the Western Indian Ocean. Marine Biodiversity Records, 6:1-12.
- Ramírez, C., Rojas, R., & Romero, J. (2020). Partial evaluation of autochthonous probiotic potential of the gut microbiota of Seriola lalandi. Probiotics and Antimicrobial Proteins, 12:672-682.
- Restrepo, L., Domínguez-Borbor, C., Bajaña, L., Betancourt, I., Rodríguez, J., Bayot, B., & Reyes, A. (2021). Microbial community characterization of shrimp survivors to AHPND challenge test treated with an effective shrimp probiotic (Vibrio diabolicus). Microbiome, 9(88):1-20.
- Ringø, E., Van Doan, H., Lee, S. H., Soltani, M., Hoseinifar, S. H., Harikrishnan, R., & Song, S. K. (2020). Probiotics, lactic acid bacteria and bacilli: interesting supplementation for aquaculture. Journal of Applied Microbiology, 129(1):116-136.
- Riyaz, S. U. M., Inbakandan, D., Manikandan, D., Bhavadharani, P., Elson, J., Prabhu, N. S., Dhas, T. S., Nalini, S., Latha, M. B., & Simal-Gandara, J. (2021). Microbiome in the ice-ice disease of the farmed red algae Kappaphycus alvarezii and degradation of extracted food carrageenan. Food Bioscience, 42:101138.
- Riyaz, S. U. M., Prabhu, N. S., Nalini, S., Tejaswini, G., Christy, H. J., & Inbakandan, D. (2020). Microbiome identification from ice ice disease infected Kappaphycus alvarezii using 16S rRNA gene sequence analysis and in silico docking studies against carrageenan degrading bacteria. Biocatalysis and Agricultural Biotechnology, 27:101707.
- Serosero, R., Sulistiono, Riani, E., & Butet, N. A. (2020). Reproduction of coconut crabs (Birgus latro) in Daeo District, Morotai Island, North Maluku, Indonesia. AACL Bioflux, 13(4):2002-2013.
- Sineva, E. V., Andreeva-Kovalevskaya, Z. I., Shadrin, A. M., Gerasimov, Y. L., Ternovsky, V. I., Teplova, V. V., Yurkova, T. V., & Solonin, A. S. (2009). Expression of Bacillus cereus hemolysin II in Bacillus subtilis renders the bacteria pathogenic for the crustacean Daphnia magna. FEMS Microbiology Letters, 299(1):110-119.
- Sugizaki, M., Hamasaki, K., Dan, S., & Kitada, S. (2010). Growth and morphogenesis of larvae reared at different temperatures, and mass culture of larvae in the coconut crab Birgus latro (Decapod, Coenobitidae). Aquaculture Science, 58(1):135-142.
- Sukenda, S., Gardenia, L., Zairin Jr, M., Lusiastuti, A., & Alimudin, A. (2020). Identification of giant gourami iridovirus (GGIV): A new infectious spleen and kidney necrosis virus (ISKNV) from natural outbreak in cultured Osphronemus goramy. Aquaculture International, 28:1069-1082.
- Sulistiono, Ridwan, Jusadi, D., Samson, S., & Serosero, R. (2019). Study on the coconut crab (Birgus latro) in-situ rearing in Derawan Islands, Indonesia: Feeding artificial food (part 1). AACL Bioflux, 12(5):1918-1928.
- Velmurugan, S., Palanikumar, P., Velayuthani, P., Donio, M. B. S., Babu, M. M., Lelin, C., Sudhakar, S., & Citarasu, T. (2015). Bacterial white patch disease caused by Bacillus cereus, a new emerging disease in semi-intensive culture of Litopenaeus vannamei. Aquaculture, 444:49-54.
- Widiyanti, S. E., Marsoedi, S., & Setyohadi, D. (2015). Resource management of coconut crab (Birgus latro) in Liwo Island, North Maluku of Indonesia. Journal of Biodiversity and Environmental Sciences, 6(5):343-351.
- Xu, L., Yuan, J., Chen, X., Zhang, S., Xie, M., Chen, C., & Wu, Z. (2021). Screening of intestinal probiotics and the effects of feeding probiotics on the digestive enzyme activity, immune, intestinal flora and WSSV resistance of Procambarus clarkii. Aquaculture, 540:736748.
- Yang, J., Kim, Y. K., Kang, T. S., Jee, Y. K., & Kim, Y. Y. (2017). Importance of indoor dust biological ultrafine particles in the pathogenesis of chronic inflammatory lung diseases. Environmental Health and Toxicology, 32:e2017021.
- Yorisue, T., Iguchi, A., Yasuda, N., Yoshioka, Y., Sato, T., & Fujita, Y. (2020). Evaluating the effect of overharvesting on genetic diversity and genetic population structure of the coconut crab. Scientific Reports, 10(10026):1¬-9.
References
Altaff, K. (2020). Indigenous live feed for aqua hatchery larval rearing of finfish and shellfish: A review. International Journal of Zoological Investigations, 6(1):162-173.
Anokyewaa, M. A., Amoah, K., Li, Y., Lu, Y., Kuebutornye, F. K., Asiedu, B., & Seidu, I. (2021). Prevalence of virulence genes and antibiotic susceptibility of Bacillus used in commercial aquaculture probiotics in China. Aquaculture Reports, 21:100784.
Bunnoy, A., Na-Nakorn, U., & Srisapoome, P. (2019). Probiotic effects of a novel strain, Acinetobacter KU011TH, on the growth performance, immune responses, and resistance against Aeromonas hydrophila of bighead catfish (Clarias macrocephalus Günther, 1864). Microorganisms, 7(12):613.
Chiu, S. T., Chu, T. W., Simangunsong, T., Ballantyne, R., Chiu, C. S., & Liu, C. H. (2021). Probiotic, Lactobacillus pentosus BD6 boost the growth and health status of white shrimp, Litopenaeus vannamei via oral administration. Fish & Shellfish Immunology, 117:124-135.
Dong, J., Zhang, L., Zhou, S., Xu, N., Yang, Q., Liu, Y., & Ai, X. (2020). Identification of a multi-resistant Enterobacter cloacae strain from diseased crayfish (Procambarus clarkii). Aquaculture Reports, 17:100405.
Drew, M. M., Harzsch, S., Stensmyr, M., Erland, S., & Hansson, B. S. (2010). A review of the biology and ecology of the robber crab, Birgus latro (Linnaeus, 1767) (Anomura: Coenobitidae). Zoologischer Anzeiger - A Journal of Comparative Zoology, 249(1):45-67.
Hamasaki, K., Yamashita, S., Ishiyama, N., & Kitada, S. (2013). Effects of water availability and migration timing from sea to land on survival and moulting in megalopae and juveniles of the coconut crab, Birgus latro: Implications for mass production of juveniles. Journal of Crustacean Biology, 33(5):627-632.
He, R. Z., Li, Z. C., Li, S. Y., & Li, A. X. (2021). Development of an immersion challenge model for Streptococcus agalactiae in Nile tilapia (Oreochromis niloticus). Aquaculture, 531:735877.
Hindu, S. V., Chandrasekaran, N., Mukherjee, A., & Thomas, J. (2018). Effect of dietary supplementation of novel probiotic bacteria Bacillus vireti 01 on antioxidant defence system of freshwater prawn challenged with Pseudomonas aeruginosa. Probiotics and Antimicrobial Proteins, 10:356-366.
Jefri, M., Satyantini, W. H., Sahidu, A. M., & Nindarwi, D. D. (2020). Application of Probiotics for Organic Matter and Enhancement of Growth Performance in White Shrimp (Litopenaeus vannamei). Jurnal Ilmiah Perikanan Dan Kelautan, 12(1):97-104.
Lee, C., Kim, S., Shin, J., Kim, M. G., Gunathilaka, B. E., Kim, S. H., Kim, J. E., Ji, S. C., Han, J. E., & Lee, K. J. (2021). Dietary supplementations of Bacillus probiotic improve digestibility, growth performance, innate immunity, and water ammonia level for Pacific white shrimp, Litopenaeus vannamei. Aquaculture International, 29(6):2463-2475.
Ma, R., Wang, Y., Zhao, L., Zhou, J., Zhao, S., Li, X., Dai, X., & Fang, W. (2020). Exploration of the death causes in zoea stages of Macrobrachium rosenbergii based on microbial diversity analysis. Aquaculture, 519:734710.
Maas, R. M., Deng, Y., Dersjant-Li, Y., Petit, J., Verdegem, M. C., Schrama, J. W., & Kokou, F. (2021). Exogenous enzymes and probiotics alter digestion kinetics, volatile fatty acid content and microbial interactions in the gut of Nile tilapia. Scientific Reports, 11(1):1-16.
Mohamad, N., Manan, H., Sallehhuddin, M., Musa, N., & Ikhwanuddin, M. (2020). Screening of Lactic Acid Bacteria isolated from giant freshwater prawn (Macrobrachium rosenbergii) as potential probiotics. Aquaculture Reports, 18:100523.
Muttharasi, C., Gayathri, V., Muralisankar, T., Mohan, K., Uthayakumar, V., Radhakrishnan, S., Kumar, P., & Palanisamy, M. (2021). Growth performance, digestive enzymes and antioxidants activities in the shrimp Litopenaeus vannamei fed with Amphiroa fragilissima crude polysaccharides encapsulated Artemia nauplii. Aquaculture, 545:737263.
Nimrat, S., Khaopong, W., Sangsong, J., Boonthai, T., & Vuthiphandchai, V. (2021). Dietary administration of Bacillus and yeast probiotics improves the growth, survival, and microbial community of juvenile whiteleg shrimp, Litopenaeus vannamei. Journal of Applied Aquaculture, 33(1):15-31.
Ninwichian, P., Phuwan, N., & Limlek, P. (2022). Effects of tank color on the growth, survival rate, stress response, and skin color of juvenile hybrid catfish (Clarias macrocephalus x Clarias gariepinus). Aquaculture, 554:738129.
Nuidate, T., Kuaphiriyakul, A., Surachat, K., & Mittraparp-Arthorn, P. (2021). Induction and genome analysis of HY01, a newly reported prophage from an emerging shrimp pathogen Vibrio campbellii. Microorganisms, 9(2):400.
Oliveira, R. V., Oliveira, M. C., & Pelli, A. (2017). Disease infection by Enterobacteriaceae family in fishes: a review. Journal of Microbiology & Experimentation, 4(5):00128.
Osman, K. M., da Silva Pires, Á., Franco, O. L., Saad, A., Hamed, M., Naim, H., Ali, A. H. M., & Elbehiry, A. (2021). Nile tilapia (Oreochromis niloticus) as an aquatic vector for Pseudomonas species of medical importance: Antibiotic resistance association with biofilm formation, quorum sensing and virulence. Aquaculture, 532:736068.
Poupin, J., Zubia, M., Gravier-Bonnet, N., Chabanet, P., & Duhec, A. (2013). Crustacea Decapoda of Glorieuses Islands, with notes on the distribution of the coconut crab (Birgus latro) in the Western Indian Ocean. Marine Biodiversity Records, 6:1-12.
Ramírez, C., Rojas, R., & Romero, J. (2020). Partial evaluation of autochthonous probiotic potential of the gut microbiota of Seriola lalandi. Probiotics and Antimicrobial Proteins, 12:672-682.
Restrepo, L., Domínguez-Borbor, C., Bajaña, L., Betancourt, I., Rodríguez, J., Bayot, B., & Reyes, A. (2021). Microbial community characterization of shrimp survivors to AHPND challenge test treated with an effective shrimp probiotic (Vibrio diabolicus). Microbiome, 9(88):1-20.
Ringø, E., Van Doan, H., Lee, S. H., Soltani, M., Hoseinifar, S. H., Harikrishnan, R., & Song, S. K. (2020). Probiotics, lactic acid bacteria and bacilli: interesting supplementation for aquaculture. Journal of Applied Microbiology, 129(1):116-136.
Riyaz, S. U. M., Inbakandan, D., Manikandan, D., Bhavadharani, P., Elson, J., Prabhu, N. S., Dhas, T. S., Nalini, S., Latha, M. B., & Simal-Gandara, J. (2021). Microbiome in the ice-ice disease of the farmed red algae Kappaphycus alvarezii and degradation of extracted food carrageenan. Food Bioscience, 42:101138.
Riyaz, S. U. M., Prabhu, N. S., Nalini, S., Tejaswini, G., Christy, H. J., & Inbakandan, D. (2020). Microbiome identification from ice ice disease infected Kappaphycus alvarezii using 16S rRNA gene sequence analysis and in silico docking studies against carrageenan degrading bacteria. Biocatalysis and Agricultural Biotechnology, 27:101707.
Serosero, R., Sulistiono, Riani, E., & Butet, N. A. (2020). Reproduction of coconut crabs (Birgus latro) in Daeo District, Morotai Island, North Maluku, Indonesia. AACL Bioflux, 13(4):2002-2013.
Sineva, E. V., Andreeva-Kovalevskaya, Z. I., Shadrin, A. M., Gerasimov, Y. L., Ternovsky, V. I., Teplova, V. V., Yurkova, T. V., & Solonin, A. S. (2009). Expression of Bacillus cereus hemolysin II in Bacillus subtilis renders the bacteria pathogenic for the crustacean Daphnia magna. FEMS Microbiology Letters, 299(1):110-119.
Sugizaki, M., Hamasaki, K., Dan, S., & Kitada, S. (2010). Growth and morphogenesis of larvae reared at different temperatures, and mass culture of larvae in the coconut crab Birgus latro (Decapod, Coenobitidae). Aquaculture Science, 58(1):135-142.
Sukenda, S., Gardenia, L., Zairin Jr, M., Lusiastuti, A., & Alimudin, A. (2020). Identification of giant gourami iridovirus (GGIV): A new infectious spleen and kidney necrosis virus (ISKNV) from natural outbreak in cultured Osphronemus goramy. Aquaculture International, 28:1069-1082.
Sulistiono, Ridwan, Jusadi, D., Samson, S., & Serosero, R. (2019). Study on the coconut crab (Birgus latro) in-situ rearing in Derawan Islands, Indonesia: Feeding artificial food (part 1). AACL Bioflux, 12(5):1918-1928.
Velmurugan, S., Palanikumar, P., Velayuthani, P., Donio, M. B. S., Babu, M. M., Lelin, C., Sudhakar, S., & Citarasu, T. (2015). Bacterial white patch disease caused by Bacillus cereus, a new emerging disease in semi-intensive culture of Litopenaeus vannamei. Aquaculture, 444:49-54.
Widiyanti, S. E., Marsoedi, S., & Setyohadi, D. (2015). Resource management of coconut crab (Birgus latro) in Liwo Island, North Maluku of Indonesia. Journal of Biodiversity and Environmental Sciences, 6(5):343-351.
Xu, L., Yuan, J., Chen, X., Zhang, S., Xie, M., Chen, C., & Wu, Z. (2021). Screening of intestinal probiotics and the effects of feeding probiotics on the digestive enzyme activity, immune, intestinal flora and WSSV resistance of Procambarus clarkii. Aquaculture, 540:736748.
Yang, J., Kim, Y. K., Kang, T. S., Jee, Y. K., & Kim, Y. Y. (2017). Importance of indoor dust biological ultrafine particles in the pathogenesis of chronic inflammatory lung diseases. Environmental Health and Toxicology, 32:e2017021.
Yorisue, T., Iguchi, A., Yasuda, N., Yoshioka, Y., Sato, T., & Fujita, Y. (2020). Evaluating the effect of overharvesting on genetic diversity and genetic population structure of the coconut crab. Scientific Reports, 10(10026):1¬-9.