Bacterial isolates from bryozoan Pleurocodonellina sp.: Diversity and antimicrobial potential against pathogenic bacteria
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MEEZAN ARDHANU ASAGABALDAN
♥
https://orcid.org/0000-0002-3340-6707
GILLES BEDOUX
NATHALIE BOURGOUGNON
RHESI KRISTIANA
DIAH AYUNINGRUM
AGUS SABDONO
AGUS TRIANTO
OCKY KARNA RADJASA
Abstract
Abstract. Asagabaldan MA, Bedoux G, Bourgougnon N, Kristiana R, Ayuningrum D, Sabdono A, Trianto A, Radjasa OK. 2019. Bacterial isolates from bryozoan Pleurocodonellina sp.: Diversity and antimicrobial potential against pathogenic bacteria. Biodiversitas 20: 2528-2535. There is an urgent need to discover new compounds with antibacterial activity, which can be developed into lead structures for the treatment of human disease caused by multidrug-resistant (MDR) bacteria. In this study, we focussed on bryozoan-associated bacteria to screen them toward antibacterial activities, since the microbiome of these organisms can still be regarded as under-investigated. Most of the few publications about bryozoan-associated bacteria focused on taxonomy and the potential as producers of antibacterial natural products were neglected. Four specimens of bryozoan Pleurocodonellina sp. were collected from Teluk Awur, Jepara in Java Sea, Indonesia. Therefrom, 56 bacterial strains were isolated, and 17 displayed antibacterial activities against MDR bacteria Pseudomonas aruginosa, Klebsiella pneumoniae, Acinetobacter baumannii, Enterobacter cloacae, and methicillin-resistant Staphylococcus aureus (MRSA). Taxonomic identification of the bacteria by 16S rRNA gene sequencing revealed them belonging to the genera Virgibacillus, Pseudoalteromonas, Halomonas, and Bacillus. Most interestingly, the genus Virgibacillus was dominantly obtained from the Pleurocodonellina sp. specimens, i.e., 12 active isolates. Nevertheless, the best activities against MDR bacteria (both Gram-positive and Gram-negative) were contributed to isolates showing >99% identity to Pseudoalteromonas. The results further suggest adding the genus Virgibacillus as bacteria associated with bryozoan, since to the best of our knowledge there were no reports of this genus isolated from bryozoan.
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References
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Ayuningrum, D., Kristiana, R., Asagabaldan, M.A., Sabdono, A., Radjasa, O.K. & Nuryadi, H. 2017. Isolation, characterisation and antagonistic activity of bacteria symbionts hardcoral Pavona sp. isolated from Panjang Island, Jepara against infectious multi-drug resistant (MDR) bacteria. IOP Conference Series: Earth and Environmental Science 55: 012029.
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Harmer, S.F. 1926. The Polyzoa of the Siboga Expedition. Part 2. Cheilostomata Anasca. Siboga Expedition Reports 28b: 183–501, pls 13–34.
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Harmer, S.F. 1957. The Polyzoa of the Siboga Expedition. Part 4. Cheilostomata Ascophora, II. Siboga Expedition Reports 28d: 641–1147, pls 42–74.
Heindl, H., Wiese, J., Thiel, V. & Imhoff, J.F. 2010. Phylogenetic diversity and antimicrobial activities of bryozoan-associated bacteria isolated from Mediterranean and Baltic Sea habitats. Systematic and Applied Microbiology 33: 94–104.
Heindl, H., Thiel, V., Wiese, J., & Imhoff, J.F. 2012. Bacterial isolates from the bryozoan Membranipora membranacea: Influence of culture media on isolation and antimicrobial activity. International Microbiology 15:17–32.
Kaselowsky, J., Scholz, J., Mawatari, S.F., Probert, P.K., Gerdes, G., Kadagies, N., & Hillmer, G. 2005. Bryozoans and microbial communities of cool-temperate to subtropical latitudes-paleoecological implications - I. Growth morphologies of shallow-water bryozoans settling on bivalve shells (Japan and New Zealand). Facies 50: 349–361.
Kerr, K.G., Snelling, A.M. 2009. Pseudomonas aeruginosa: a formidable and ever-present adversary. The Journal of Hospital Infection 73: 338–344
König, G.M., Kehraus, S., Seibert, S.F, Abdel-Lateef, A. & Müller, D. 2006. Natural products from marine organisms and their associated microbes. ChemBioChem 7: 229–238
Kristiana, R., Sibero, M.T., Farisa, M.Y., Ayuningrum, D., Dirgantara D., Hanafi, M., Radjasa, O.K., Sabdono, A. & Trianto, A. 2019. Antibacterial potential of nudibranch-associated bacteria from Saparua and Nusa Laut Islands, Indonesia. Biodiversitas 20 (7): 1811¬¬¬–1819.
Kristiana, R., Ayuningrum, D., Asagabaldan, M.A., Nuryadi, H., Sabdono, A. & Radjasa, O.K. 2017. Isolation and partial characterization of bacteria activity associated with gorgonian Euplexaura sp. against methicillin-resistant Staphylococcus aureus (MRSA). IOP Conference Series: Earth and Environmental Science: 55, 012056.
Lane, D.L. 1991. 16S/23S rRNA sequencing. In: Stackebrandt, E. (Ed.) Nucleic acid Techniques in Bacterial Systematics. Wiley, New York, pp. 115–175.
Lister, P.D., Wolter, D.J., & Hanson, N.D. 2009. Antibacterial-resistant Pseudomonas aeruginosa: Clinical impact and complex regulation of chromosomally encoded resistance mechanisms. Clinical Microbiology Reviews 22: 582–610.
Lopanik, N., Gustafson, K.R., & Lindquist, N. 2004. Structure of bryostatin 20: A symbiont-produced chemical defense for larvae of the host bryozoan, Bugula neritina. Journal of Natural Products 67: 1412–1414.
Madigan, M. T., Martinko, J. M., Bender, K. S., Buckley, D. H., & Stahl, D. A. 2015. Brock biology of microorganisms (Fourteenth edition.). Boston: Pearson.
Massard, J.A., Geimer, G. 2008. Global diversity of bryozoans (Bryozoa or Ectoprocta) in freshwater. Hydrobiologia 595: 93–99.
Mauldin, P.D., Salgado, C.D., Hansen, I.S., Durup, D.T., & Bosso, J.A. 2010. Attributable hospital cost and length of stay associated with health care-associated infections caused by antibiotic-resistant gram-negative bacteria. Antimicrobial Agents and Chemotherapy 54:109–115.
Mohan, G., Thipparamalai, T.A.K., & Ramasamy, B. (2016) Antimicrobial activities of secondary metabolites and phylogenetic study of sponge endosymbiotic bacteria, Bacillus sp. at Agatti Island, Lakshadweep Archipelago. Biotechnology Reports 11: 44–52.
Mondol, M.A., Shin, H.J., & Islam, M.T. 2013. Diversity of secondary metabolites from marine Bacillus species: chemistry and biological activity. Marine Drugs 11(8): 2846–72.
Nogales, B., Lanfranconi, M.P., Piña-Villalonga, J.M. & Bosch, R. 2011. Anthropogenic perturbations in marinemicrobial communities. FEMS Microbiology Reviews 358: 275–298.
Offret, C., Desriac, F., Le Chevalier, P., Mounier, J., Jegou, C. & Fleury, Y. 2016. Spotlight on Antimicrobial Metabolites from the Marine Bacteria Pseudoalteromonas: Chemodiversity and Ecological Significance. Marine Drugs 14(7).
Peters, L., König, G.M., Terlau, H. & Wright, A.D. 2002. Four new bromotryptamine derivatives from the marine bryozoan Flustra foliacea. Journal of Natural Products 65: 1633–1637.
Pettit, G.R., Herald, C.L., Doubek D.L., Herald, D.L., Arnold, E. & Clardy, J. 1982. Isolation and Structure of Bryostatin 1. Journal of the American Chemical Society 104: 6846–6848.
Pukall, R., Kramer, I., Rohde, M. & Stackebrandt, E. 2001. Microbial diversity of cultivatable bacteria associated with the North Sea bryozoan Flustra foliacea. Systematic and Applied Microbiology 24: 623–633.
Ryland, J.S. 2005. Bryozoa: an introductory overview. Pages 9-20 in: Moostiere (Bryozoa). E. R. Wöss, ed., vol. 16.
Sabuda, D.M., Laupland, K., Pitout, J., Dalton, B., Rabin, H., Louie, T. & Conly, J. 2008. Utilization of colistin for treatment of multidrug-resistant Pseudomonas aeruginosa. Canadian Journal of Infectious Diseases and Medical Microbiology 19: 413–418
Schaufelberger, D.E., Koleck, M.P., Beutler, J.A., Vatakis, A.M., Alvarado, A.B., Andrews, P., Marzo, L.V., Muschik, G.M., Roach, J. & Ross, J.T. 1991. The large-Scale isolation of bryostatin 1 from Bugula neritina following current good manufacturing practices. Journal of Natural Products 54: 1265–1270.
Sharp, J.H., Winson, M.K. & Porter, J.S. 2007. Bryozoan metabolites: An ecological perspective. Natural Product Reports 24: 659–673.
Sibero, M.T., Bachtiarini, T.U., Trianto, A., Lupita, A.H., Sari, D.P., Igarashi, Y., Harunari, E., Sharma, A.R., Radjasa, O.K. & Sabdono, A. 2019. Characterization of a yellow pigmented coral-associated bacterium exhibiting antibacterial activity against Multidrug-Resistant (MDR) Organism. Egyptian Journal of Aquatic Research 45(1): 81–87.
Thakur, N.L., Thakur, A.N., Müller, W.E.G. 2005. Marine Natural Products Drug Discovery. Biotechnology 4: 471–477
Tilbrook, K.J. 2006. Cheilostomatous Bryozoa from the Solomon Islands. Santa Barbara Museum of Natural History, Monographs 4 (Studies in Biodiversity Number 3), 4, 1–386.
Tumbarello, M., Repetto, E., Trecarichi, E.M. & Bernardini, C. 2011. Multidrug-resistant Pseudomonas aeruginosa bloodstream infections: risk factors and mortality. Epidemiology & Infection 139: 1740–1749.
Walls, J.T., Blackman, A.J., Ritz, D.A. 1995. Localisation of the amathamide alkaloids in surface bacteria of Amathia wilsoni Kirkpatrick, 1888 (Bryozoa: Ctenostomata). Hydrobiologia 297: 163–172.
Winston, J.E. & Heimberg, B.F. 1986. Bryozoans from Bali, Lombok, and Komodo. American Museum Novitates 2847: 1–49.
Yu, H.B., Yang, F., Li, Y.Y., Gan, J.H., Jiao, W.H. & Lin, H.W. 2015. Cytotoxic bryostatin derivatives from the South China sea bryozoan Bugula neritina. Journal of Natural Products 78: 1169–1173.
Almeida, A.C.S., Souza, F.B.C., Farias, J., Alves, O.F.S. & Vieira, L.M. 2018. Bryozoa on disarticulated bivalve shells from Todos os Santos Bay, northeastern Brazil, with the description of two new species. Zootaxa 4434 (3): 401–428.
Almeida, AC.S., Souza, F.B.C., Menegola, C. & Vieira, L.M. 2017. Diversity of marine bryozoans inhabiting demosponges in Northeastern Brazil. Zootaxa 4290 (2): 281–323.
Anthoni, U., Nielsen, P.H., Pereira, M., & Christophersen, C. 1990. Bryozoan secondary metabolites: A chemotaxonomical challenge. Comparative Biochemistry and Physiology - Part B: Biochemistry & Molecular Biology 96: 431–437.
Arunachalam, K., Amirtham Jacob Appadorai R. 2013. Antioxidant potential and biochemical evaluation of metabolites from the marine bacteria Virgibacillus sp. associated with the sponge Callyspongia diffusa. Free Radicals and Antioxidants, 3(1): 47–51.
Asagabaldan, M.A., Ayuningrum, D., Kristiana, R., Sabdono, A., Radjasa, O.K. & Trianto, A. 2017. Identification and antibacterial activity of bacteria isolated from marine sponge Haliclona (Reniera) sp. against multi-drug resistant human pathogen. IOP Conference Series: Earth and Environmental Science 55: 012019.
Ayuningrum, D., Kristiana, R., Asagabaldan, M.A., Sabdono, A., Radjasa, O.K. & Nuryadi, H. 2017. Isolation, characterisation and antagonistic activity of bacteria symbionts hardcoral Pavona sp. isolated from Panjang Island, Jepara against infectious multi-drug resistant (MDR) bacteria. IOP Conference Series: Earth and Environmental Science 55: 012029.
Ayuningrum, D., liu, Y., Riyanti, Sibero, M.T., Kristiana, R., Asagabaldan, M.A., Wuisan, Z.G., Trianto, A., Radjasa, O.K., Sabdono, A. & Schaeberle, T.F. 2019. Tunicate-associated bacteria show a great potential for the discovery of antimicrobial compounds. PLOS ONE 14(3): 1–14
Bitzer, J., Grosse, T., Wang, L., Lang, S., & Beil, W.A.Z. 2006. New aminophenoxazinones from a marine Halomonas sp.: fermentation, structure elucidation, and biological activity. The Journal of Antibiotics 59(2) :7.
Blunt, J.W., Copp, B.R., Keyzers, R.A., Munro, M.H.G. & Prinsep, M.R. 2015. Marine natural products. Natural Product Reports 32: 116–211.
Blunt, J.W., Copp, B.R., Munro MHG, Northcote, P.T. & Prinsep, M.R. 2010. Marine natural products. Natural Product Reports 27: 165.
Bowman, J.P. 2007. Bioactive Compound Synthetic Capacity and Ecological Significance of Marine Bacterial Genus Pseudoalteromonas. Marine Drugs 5: 220–241.
CDC. 2013. Antibiotic resistance threats in the United States, 2013. Current 114.
Crain, C.M., Kroeker, K. & Halpern, B. 2008. Interactive and cumulative effects of multiple human stressors in marine systems. Ecology Letter 11: 1304–1315.
Davidson, S.K., Allen, S.W., Lim, G.E., Anderson, C.M., Haygood, M.G. 2001. Evidence for the Biosynthesis of Bryostatins by the Bacterial Symbiont “Candidatus Endobugula sertula” of the Bryozoan Bugula neritina. Applied and Environmental Microbiology 67: 4531–4537.
Di Martino E, Taylor PD. 2018. Early Pleistocene and Holocene bryozoans from Indonesia. Zootaxa 4419: 1–70.
Di Martino, E. & Taylor, P.D. 2014. Miocene Bryozoa from East Kalimantan, Indonesia. Part I: Cyclostomata and “Anascan” Cheilostomata. Scripta Geologica 146: 17–126.
Di Martino, E. & Taylor, P.D. 2015. Miocene Bryozoa from East Kalimantan, Indonesia. Part II: “Ascophoran” Cheilostomata. Scripta Geologica 148: 1–142.
Di Martino, E., Taylor, P.D. & Johnson, K.G. 2015. Bryozoan Diversity in the Miocene of the Kutai Basin, East Kalimantan, Indonesia. Palaios 30: 109–115.
Dick, M.H. & Grischenko, A.V. 2017. Rocky-intertidal cheilostome bryozoans from the vicinity of the Sesoko Biological Station, west-central Okinawa, Japan. Journal of Natural History 51: 141–266.
Gerdes, G., Kadagies, N., Kaselowsky, J., Lauer, A., & Scholz, J. 2005. Bryozoans and microbial communities of cool-temperate to subtropical latitudes-paleoecological implications—II. Diversity of microbial fouling on laminar shallow marine bryozoans of Japan and New Zealand. Facies 50: 363–389.
Guiton, P.S., Hung, C.S., Hancock, L.E., Caparon, M.G. & Hultgren, S.J. 2010. Enterococcal biofilm formation and virulence in an optimized murine model of foreign body-associated urinary tract infections. Infection and Immunity 78: 4166–4175.
Harmer, S.F. 1915. The Polyzoa of the Siboga Expedition. Part 1. Entoprocta, Ctenostomata and Cyclostomata. Siboga Expedition Reports 28a: 1–180, pls 1–12.
Harmer, S.F. 1926. The Polyzoa of the Siboga Expedition. Part 2. Cheilostomata Anasca. Siboga Expedition Reports 28b: 183–501, pls 13–34.
Harmer, S.F. 1934. The Polyzoa of the Siboga Expedition. Part 3. Cheilostomata Ascophora, I. Family Reteporidae. Siboga Expedition Reports 28c: 502–640, pls 35–41.
Harmer, S.F. 1957. The Polyzoa of the Siboga Expedition. Part 4. Cheilostomata Ascophora, II. Siboga Expedition Reports 28d: 641–1147, pls 42–74.
Heindl, H., Wiese, J., Thiel, V. & Imhoff, J.F. 2010. Phylogenetic diversity and antimicrobial activities of bryozoan-associated bacteria isolated from Mediterranean and Baltic Sea habitats. Systematic and Applied Microbiology 33: 94–104.
Heindl, H., Thiel, V., Wiese, J., & Imhoff, J.F. 2012. Bacterial isolates from the bryozoan Membranipora membranacea: Influence of culture media on isolation and antimicrobial activity. International Microbiology 15:17–32.
Kaselowsky, J., Scholz, J., Mawatari, S.F., Probert, P.K., Gerdes, G., Kadagies, N., & Hillmer, G. 2005. Bryozoans and microbial communities of cool-temperate to subtropical latitudes-paleoecological implications - I. Growth morphologies of shallow-water bryozoans settling on bivalve shells (Japan and New Zealand). Facies 50: 349–361.
Kerr, K.G., Snelling, A.M. 2009. Pseudomonas aeruginosa: a formidable and ever-present adversary. The Journal of Hospital Infection 73: 338–344
König, G.M., Kehraus, S., Seibert, S.F, Abdel-Lateef, A. & Müller, D. 2006. Natural products from marine organisms and their associated microbes. ChemBioChem 7: 229–238
Kristiana, R., Sibero, M.T., Farisa, M.Y., Ayuningrum, D., Dirgantara D., Hanafi, M., Radjasa, O.K., Sabdono, A. & Trianto, A. 2019. Antibacterial potential of nudibranch-associated bacteria from Saparua and Nusa Laut Islands, Indonesia. Biodiversitas 20 (7): 1811¬¬¬–1819.
Kristiana, R., Ayuningrum, D., Asagabaldan, M.A., Nuryadi, H., Sabdono, A. & Radjasa, O.K. 2017. Isolation and partial characterization of bacteria activity associated with gorgonian Euplexaura sp. against methicillin-resistant Staphylococcus aureus (MRSA). IOP Conference Series: Earth and Environmental Science: 55, 012056.
Lane, D.L. 1991. 16S/23S rRNA sequencing. In: Stackebrandt, E. (Ed.) Nucleic acid Techniques in Bacterial Systematics. Wiley, New York, pp. 115–175.
Lister, P.D., Wolter, D.J., & Hanson, N.D. 2009. Antibacterial-resistant Pseudomonas aeruginosa: Clinical impact and complex regulation of chromosomally encoded resistance mechanisms. Clinical Microbiology Reviews 22: 582–610.
Lopanik, N., Gustafson, K.R., & Lindquist, N. 2004. Structure of bryostatin 20: A symbiont-produced chemical defense for larvae of the host bryozoan, Bugula neritina. Journal of Natural Products 67: 1412–1414.
Madigan, M. T., Martinko, J. M., Bender, K. S., Buckley, D. H., & Stahl, D. A. 2015. Brock biology of microorganisms (Fourteenth edition.). Boston: Pearson.
Massard, J.A., Geimer, G. 2008. Global diversity of bryozoans (Bryozoa or Ectoprocta) in freshwater. Hydrobiologia 595: 93–99.
Mauldin, P.D., Salgado, C.D., Hansen, I.S., Durup, D.T., & Bosso, J.A. 2010. Attributable hospital cost and length of stay associated with health care-associated infections caused by antibiotic-resistant gram-negative bacteria. Antimicrobial Agents and Chemotherapy 54:109–115.
Mohan, G., Thipparamalai, T.A.K., & Ramasamy, B. (2016) Antimicrobial activities of secondary metabolites and phylogenetic study of sponge endosymbiotic bacteria, Bacillus sp. at Agatti Island, Lakshadweep Archipelago. Biotechnology Reports 11: 44–52.
Mondol, M.A., Shin, H.J., & Islam, M.T. 2013. Diversity of secondary metabolites from marine Bacillus species: chemistry and biological activity. Marine Drugs 11(8): 2846–72.
Nogales, B., Lanfranconi, M.P., Piña-Villalonga, J.M. & Bosch, R. 2011. Anthropogenic perturbations in marinemicrobial communities. FEMS Microbiology Reviews 358: 275–298.
Offret, C., Desriac, F., Le Chevalier, P., Mounier, J., Jegou, C. & Fleury, Y. 2016. Spotlight on Antimicrobial Metabolites from the Marine Bacteria Pseudoalteromonas: Chemodiversity and Ecological Significance. Marine Drugs 14(7).
Peters, L., König, G.M., Terlau, H. & Wright, A.D. 2002. Four new bromotryptamine derivatives from the marine bryozoan Flustra foliacea. Journal of Natural Products 65: 1633–1637.
Pettit, G.R., Herald, C.L., Doubek D.L., Herald, D.L., Arnold, E. & Clardy, J. 1982. Isolation and Structure of Bryostatin 1. Journal of the American Chemical Society 104: 6846–6848.
Pukall, R., Kramer, I., Rohde, M. & Stackebrandt, E. 2001. Microbial diversity of cultivatable bacteria associated with the North Sea bryozoan Flustra foliacea. Systematic and Applied Microbiology 24: 623–633.
Ryland, J.S. 2005. Bryozoa: an introductory overview. Pages 9-20 in: Moostiere (Bryozoa). E. R. Wöss, ed., vol. 16.
Sabuda, D.M., Laupland, K., Pitout, J., Dalton, B., Rabin, H., Louie, T. & Conly, J. 2008. Utilization of colistin for treatment of multidrug-resistant Pseudomonas aeruginosa. Canadian Journal of Infectious Diseases and Medical Microbiology 19: 413–418
Schaufelberger, D.E., Koleck, M.P., Beutler, J.A., Vatakis, A.M., Alvarado, A.B., Andrews, P., Marzo, L.V., Muschik, G.M., Roach, J. & Ross, J.T. 1991. The large-Scale isolation of bryostatin 1 from Bugula neritina following current good manufacturing practices. Journal of Natural Products 54: 1265–1270.
Sharp, J.H., Winson, M.K. & Porter, J.S. 2007. Bryozoan metabolites: An ecological perspective. Natural Product Reports 24: 659–673.
Sibero, M.T., Bachtiarini, T.U., Trianto, A., Lupita, A.H., Sari, D.P., Igarashi, Y., Harunari, E., Sharma, A.R., Radjasa, O.K. & Sabdono, A. 2019. Characterization of a yellow pigmented coral-associated bacterium exhibiting antibacterial activity against Multidrug-Resistant (MDR) Organism. Egyptian Journal of Aquatic Research 45(1): 81–87.
Thakur, N.L., Thakur, A.N., Müller, W.E.G. 2005. Marine Natural Products Drug Discovery. Biotechnology 4: 471–477
Tilbrook, K.J. 2006. Cheilostomatous Bryozoa from the Solomon Islands. Santa Barbara Museum of Natural History, Monographs 4 (Studies in Biodiversity Number 3), 4, 1–386.
Tumbarello, M., Repetto, E., Trecarichi, E.M. & Bernardini, C. 2011. Multidrug-resistant Pseudomonas aeruginosa bloodstream infections: risk factors and mortality. Epidemiology & Infection 139: 1740–1749.
Walls, J.T., Blackman, A.J., Ritz, D.A. 1995. Localisation of the amathamide alkaloids in surface bacteria of Amathia wilsoni Kirkpatrick, 1888 (Bryozoa: Ctenostomata). Hydrobiologia 297: 163–172.
Winston, J.E. & Heimberg, B.F. 1986. Bryozoans from Bali, Lombok, and Komodo. American Museum Novitates 2847: 1–49.
Yu, H.B., Yang, F., Li, Y.Y., Gan, J.H., Jiao, W.H. & Lin, H.W. 2015. Cytotoxic bryostatin derivatives from the South China sea bryozoan Bugula neritina. Journal of Natural Products 78: 1169–1173.
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