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Potential of fascaplysin and palauolide from Fascaplysinopsis cf reticulata to reduce the risk of bacterial infection in fish farming

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Marine natural products isolated from the sponge Fascaplysinopsis cf reticulata, in French Polynesia, were investigated as an alternative to antibiotics to control pathogens in aquaculture. The overuse of antibiotics in aquaculture is largely considered to be an environmental pollution, because it supports the transfer of antibiotic resistance genes within the aquatic environment. One environmentally friendly alternative to antibiotics is the use of quorum sensing inhibitors (QSIs). Quorum sensing (QS) is a regulatory mechanism in bacteria which control virulence factors through the secretion of autoinducers (AIs), such as acyl-homoserine lactone (AHL) in gramnegative bacteria. Vibrio harveyi QS is controlled through three parallel pathways: HAI-1, AI-2, and CAI-1. Bioassayguided purification of F. cf reticulata extract was conducted on two bacterial species, i.e., Tenacibaculum maritimum and V. harveyi for antibiotic and QS inhibition bioactivities. Toxicity bioassay of fractions was also evaluated on the freshwater fish Poecilia reticulata and the marine fish Acanthurus triostegus. Cyclohexanic and dichloromethane fractions of F. cf reticulata exhibited QS inhibition on V. harveyi and antibiotic bioactivities on V. harveyi and T. maritimum, respectively. Palauolide (1) and fascaplysin (2) were purified as major molecules from the cyclohexanic and dichloromethane fractions, respectively. Palauolide inhibited QS of V. harveyi through HAI-1 QS pathway at 50 μg ml–1 (26 μM), while fascaplysin affected the bacterial growth of V. harveyi (50 μg ml–1) and T. maritimum (0.25 μg). The toxicity of fascaplysin-enriched fraction (FEF) was evaluated and exhibited a toxic effect against fish at 50 μg ml–1. This study demonstrated for the first time the QSI potential of palauolide (1). Future research may assess the toxicity of both the cyclohexanic fraction of the sponge and palauolide (1) on fish, to confirm their potential as alternative to antibiotics in fish farming.

Abstract

Marine natural products isolated from the sponge Fascaplysinopsis cf reticulata, in French Polynesia, were investigated as an alternative to antibiotics to control pathogens in aquaculture. The overuse of antibiotics in aquaculture is largely considered to be an environmental pollution, because it supports the transfer of antibiotic resistance genes within the aquatic environment. One environmentally friendly alternative to antibiotics is the use of quorum sensing inhibitors (QSIs). Quorum sensing (QS) is a regulatory mechanism in bacteria which control virulence factors through the secretion of autoinducers (AIs), such as acyl-homoserine lactone (AHL) in gramnegative bacteria. Vibrio harveyi QS is controlled through three parallel pathways: HAI-1, AI-2, and CAI-1. Bioassayguided purification of F. cf reticulata extract was conducted on two bacterial species, i.e., Tenacibaculum maritimum and V. harveyi for antibiotic and QS inhibition bioactivities. Toxicity bioassay of fractions was also evaluated on the freshwater fish Poecilia reticulata and the marine fish Acanthurus triostegus. Cyclohexanic and dichloromethane fractions of F. cf reticulata exhibited QS inhibition on V. harveyi and antibiotic bioactivities on V. harveyi and T. maritimum, respectively. Palauolide (1) and fascaplysin (2) were purified as major molecules from the cyclohexanic and dichloromethane fractions, respectively. Palauolide inhibited QS of V. harveyi through HAI-1 QS pathway at 50 μg ml–1 (26 μM), while fascaplysin affected the bacterial growth of V. harveyi (50 μg ml–1) and T. maritimum (0.25 μg). The toxicity of fascaplysin-enriched fraction (FEF) was evaluated and exhibited a toxic effect against fish at 50 μg ml–1. This study demonstrated for the first time the QSI potential of palauolide (1). Future research may assess the toxicity of both the cyclohexanic fraction of the sponge and palauolide (1) on fish, to confirm their potential as alternative to antibiotics in fish farming.

참고문헌 (68)

  1. Salah Mesalhy Aly, "Antimicrobials Use in Aquaculture and their Public Health Impact", Journal of Aquaculture Research & Development, 5(4) (2014), OMICS Publishing Group[DOI]
  2. Caio Rodrigo Dias Assis, "Comparative effect of pesticides on brain acetylcholinesterase in tropical fish", Science of The Total Environment, 441, pp.141~150 (2012), Elsevier BV[DOI]
  3. Bassler BL, "Cross-species induction of luminescence in the quorum-sensing bacterium Vibrio harveyi", J Bacteriol, 179(12), pp.4043~4045 (1997)
  4. Bauer A, "Antibiotic susceptibility testing by a standardized single disk method", Am J Clin Pathol, 45(4), pp.493~496 (1966)
  5. Sandip B. Bharate, "Total synthesis and anti-cholinesterase activity of marine-derived bis-indole alkaloid fascaplysin", MedChemComm, 3(9), pp.1098~ (2012), Royal Society of Chemistry (RSC)[DOI]
  6. Jessica M. A. Blair, "Molecular mechanisms of antibiotic resistance", Nature Reviews Microbiology, 13(1), pp.42~51 (2015), Springer Science and Business Media LLC[DOI]
  7. Blair WM, "The Vibrio harveyi bioassay used routinely to detect AI-2 quorum sensing inhibition is confounded by inconsistent normalization across marine matrices", J Microbiol Methods, 92, pp.250~252 (2013)
  8. John W. Blunt, "Marine natural products", Natural Product Reports, 22(1), pp.15~ (2005), Royal Society of Chemistry (RSC)[DOI]
  9. Bocquené G, "Les marqueurs biologiques des effets polluants: l’acétylcholinestérase" (2004), Ifremer
  10. Gilles Brackman, "Quorum Sensing Inhibitors Increase the Susceptibility of Bacterial Biofilms to Antibiotics In Vitro and In Vivo", Antimicrobial Agents and Chemotherapy, 55(6), pp.2655~2661 (2011), American Society for Microbiology[DOI]
  11. Gilles Brackman, "Cinnamaldehyde and cinnamaldehyde derivatives reduce virulence in Vibrio spp. by decreasing the DNA-binding activity of the quorum sensing response regulator LuxR", BMC Microbiology, 8(1), pp.149~ (2008), Springer Science and Business Media LLC[DOI]
  12. Suresh Kumar, "Fascaplysin Induces Caspase Mediated Crosstalk Between Apoptosis and Autophagy Through the Inhibition of PI3K", AKT, Journal of Cellular Biochemistry, pp.2015, 116(6)[DOI]
  13. Romila D. Charan, "Thorectandrols C, D, and E, New Sesterterpenes from the Marine Sponge Thorectandra sp.", Journal of Natural Products, 65(4), pp.492~495 (2002), American Chemical Society (ACS)[DOI]
  14. Xin Chen, "Quorum sensing inhibitors: a patent review (2014–2018)", Expert Opinion on Therapeutic Patents, 28(12), pp.849~865 (2018), Informa UK Limited[DOI]
  15. Debitus C. TUAM, "http:", https:, doi.org[DOI]
  16. Sergey Dobretsov, "Inhibition of marine biofouling by bacterial quorum sensing inhibitors", Biofouling, 27(8), pp.893~905 (2011), Informa UK Limited[DOI]
  17. Editorials, "The antibiotic alarm", Nature, 495, pp.141~ (2013)
  18. Amr El-Demerdash, "Bioactive Bromotyrosine-Derived Alkaloids from the Polynesian Sponge Suberea ianthelliformis", Marine Drugs, 16(5), pp.146~ (2018), MDPI AG[DOI]
  19. Dan qing Feng, "Antifouling activities of hymenialdisine and debromohymenialdisine from the sponge Axinella sp.", International Biodeterioration & Biodegradation, 85, pp.359~364 (2013), Elsevier BV[DOI]
  20. Freeman J, "A genetic analysis of the function of LuxO, a twocomponent response regulator involved in quorum sensing in Vibrio harveyi", Mol Microbiol, 31(2), pp.665~677 (1999)
  21. Sonja Gamby, "Altering the Communication Networks of Multispecies Microbial Systems Using a Diverse Toolbox of AI-2 Analogues", ACS Chemical Biology, 7(6), pp.1023~1030 (2012), American Chemical Society (ACS)[DOI]
  22. Givskov M, "Eukaryotic interference with homoserine lactonemediated prokaryotic signalling", J Bacteriol, 178(22), pp.6618~6622 (1996)
  23. Gerhard Hamilton, "Cytotoxic Effects of Fascaplysin against Small Cell Lung Cancer Cell Lines", Marine Drugs, 12(3), pp.1377~1389 (2014), MDPI AG[DOI]
  24. Stephen M. Hatosy, "The Ocean as a Global Reservoir of Antibiotic Resistance Genes", Applied and Environmental Microbiology, 81(21), pp.7593~7599 (2015), American Society for Microbiology[DOI]
  25. Henke JM, "Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi", J Bacteriol, 186(20), pp.6902~6914 (2004)[DOI]
  26. Henke JM, "Quorum sensing regulates type III secretion in Vibrio harveyi and Vibrio parahaemolyticus", J Bacteriol, 186(12), pp.3794~3805 (2004)[DOI]
  27. Johnson FH, "An interesting new species of luminous bacteria", J Bacteriol, 31(6), pp.585~593 (1936)
  28. Vipin Chandra Kalia, "Quorum sensing inhibitors: An overview", Biotechnology Advances, 31(2), pp.224~245 (2013), Elsevier BV[DOI]
  29. I. Karunasagar, "Mass mortality of Penaeus monodon larvae due to antibiotic-resistant Vibrio harveyi infection", Aquaculture, 128(3-4), pp.203~209 (1994), Elsevier BV[DOI]
  30. Kingsland S, "The refractory model : the logistic curve and the history of population ecology", Quaterly Rev Biol, 57, pp.29~52 (1982)
  31. Suresh Kumar, "Fascaplysin Induces Caspase Mediated Crosstalk Between Apoptosis and Autophagy Through the Inhibition of PI3K", AKT, Journal of Cellular Biochemistry, pp.2015, 116(6)[DOI]
  32. Lecchini D, "Estimating the patch size of larval fishes during colonization on coral reefs", J Fish Biol, 65, pp.1142~1146 (2004)[DOI]
  33. Ronald Lulijwa, "Antibiotic use in aquaculture, policies and regulation, health and environmental risks: a review of the top 15 major producers", Reviews in Aquaculture (2019), Wiley[DOI]
  34. T. Mai, "Quorum sensing inhibitors from Leucetta chagosensis Dendy, 1863", Letters in Applied Microbiology, 61(4), pp.311~317 (2015), Wiley[DOI]
  35. Sudhakar Manda, "Discovery of a marine-derived bis-indole alkaloid fascaplysin, as a new class of potent P-glycoprotein inducer and establishment of its structure–activity relationship", European Journal of Medicinal Chemistry, 107, pp.1~11 (2016), Elsevier BV[DOI]
  36. Manefield M, "Inhibition of luminescence and virulence in the black tiger prawn(Penaeus monodon)pathogen Vibrio harveyi by intercellular signal antagonists", Appl Environ Microbiol, 66(5), pp.2079~2084 (2000)[DOI]
  37. Jose Luis Martinez, "Environmental pollution by antibiotics and by antibiotic resistance determinants", Environmental Pollution, 157(11), pp.2893~2902 (2009), Elsevier BV[DOI]
  38. Kathya A. Modesto, "Roundup® causes oxidative stress in liver and inhibits acetylcholinesterase in muscle and brain of the fish Prochilodus lineatus", Chemosphere, 78(3), pp.294~299 (2010), Elsevier BV[DOI]
  39. Mark G. Moloney, "Natural Products as a Source for Novel Antibiotics", Trends in Pharmacological Sciences, 37(8), pp.689~701 (2016), Elsevier BV[DOI]
  40. Werner E. G. Müller, "Principles of Biofouling Protection in Marine Sponges: A Model for the Design of Novel Biomimetic and Bio-inspired Coatings in the Marine Environment?", Marine Biotechnology, 15(4), pp.375~398 (2013), Springer Science and Business Media LLC[DOI]
  41. Zeena E. Nackerdien, "Quorum Sensing Influences Vibrio harveyi Growth Rates in a Manner Not Fully Accounted For by the Marker Effect of Bioluminescence", PLoS ONE, 3(2), pp.e1671~ (2008), Public Library of Science (PLoS)[DOI]
  42. F.M.I. Natrah, "Effects of micro-algae commonly used in aquaculture on acyl-homoserine lactone quorum sensing", Aquaculture, 317(1-4), pp.53~57 (2011), Elsevier BV[DOI]
  43. Gde Sasmita Julyantoro Pande, "Quorum sensing-disrupting compounds protect larvae of the giant freshwater prawn Macrobrachium rosenbergii from Vibrio harveyi infection", Aquaculture, 406-407, pp.121~124 (2013), Elsevier BV[DOI]
  44. Tania Pérez-Sánchez, "Biological Approaches for Disease Control in Aquaculture: Advantages, Limitations and Challenges", Trends in Microbiology, 26(11), pp.896~903 (2018), Elsevier BV[DOI]
  45. Peters L, "Secondary metabolites of Flustra foliace and their influence on bacteria", Appl Environ Microbiol, 69(6), pp.3469~3475 (2003)[DOI]
  46. chemical communication in sponges and corals, "Chemical defense", pp.2014, Quévrain E
  47. Maria Rasch, "An Inhibitor of Bacterial Quorum Sensing Reduces Mortalities Caused by Vibriosis in Rainbow Trout (Oncorhynchus mykiss, Walbaum)", Systematic and Applied Microbiology, 27(3), pp.350~359 (2004), Elsevier BV[DOI]
  48. Miriam Reverter, "Effects of local Polynesian plants and algae on growth and expression of two immune-related genes in orbicular batfish ( Platax orbicularis )", Fish & Shellfish Immunology, 58, pp.82~88 (2016), Elsevier BV[DOI]
  49. Deborah M. Roll, "Fascaplysin, an unusual antimicrobial pigment from the marine sponge Fascaplysinopsis sp", The Journal of Organic Chemistry, 53(14), pp.3276~3278 (1988), American Chemical Society (ACS)[DOI]
  50. Kumar Saurav, "Quorum Sensing Inhibitors from the Sea Discovered Using Bacterial N-acyl-homoserine Lactone-Based Biosensors", Marine Drugs, 15(3), pp.53~ (2017), MDPI AG[DOI]
  51. Jonas Schluter, "The Evolution of Quorum Sensing as a Mechanism to Infer Kinship", PLOS Computational Biology, 12(4), pp.e1004848~ (2016), Public Library of Science (PLoS)[DOI]
  52. Schneider L, "A critical review of cholinesterase inhibitors as a treatment modality in Alzheimer’s disease", Dialogues Clin Neurosci, 2(2), pp.111~128 (2000)
  53. Segraves NL, "Comparison of fascaplysin and related alkaloids : a study of structures, cytotoxicities, and sources", J Nat Prod, 67, pp.783~792 (2004)[DOI]
  54. Muhammad Imtiaz Shafiq, "FASCAPLYSIN as a Specific Inhibitor for CDK4: Insights from Molecular Modelling", PLoS ONE, 7(8), pp.e42612~ (2012), Public Library of Science (PLoS)[DOI]
  55. Syed Q. A. Shah, "Antimicrobial resistance and antimicrobial resistance genes in marine bacteria from salmon aquaculture and non-aquaculture sites", Environmental Microbiology, 16(5), pp.1310~1320 (2014), Wiley[DOI]
  56. Poojan Shrestha, "Enumerating the economic cost of antimicrobial resistance per antibiotic consumed to inform the evaluation of interventions affecting their use", Antimicrobial Resistance & Infection Control, 7(98), pp.1~9 (2018), Springer Science and Business Media LLC[DOI]
  57. Mette Elena Skindersoe, "Quorum Sensing Antagonism from Marine Organisms", Marine Biotechnology, 10(1), pp.56~63 (2008), Springer Science and Business Media LLC[DOI]
  58. Spellberg B, "The future of antibiotics and resistance: a tribute to a career of leadership by John Bartlett", Clin Infect Dis, 59, pp.S71~S75 (2014)[DOI]
  59. Hans P. Steenackers, "Structure–activity relationship of brominated 3-alkyl-5-methylene-2(5H)-furanones and alkylmaleic anhydrides as inhibitors of Salmonella biofilm formation and quorum sensing regulated bioluminescence in Vibrio harveyi", Bioorganic & Medicinal Chemistry, 18(14), pp.5224~5233 (2010), Elsevier BV[DOI]
  60. Sullivan B, "An antibacterial sesterterpene from a palauan sponge", Tetrahedron Lett, 23, pp.907~910 (1982)[DOI]
  61. Lee R. Swem, "Deducing Receptor Signaling Parameters from In Vivo Analysis: LuxN", AI-1 Quorum Sensing in Vibrio harveyi, 2008, pp.134(3), 461~473[DOI]
  62. M. E. Teasdale, "Secondary Metabolites Produced by the Marine Bacterium Halobacillus salinus That Inhibit Quorum Sensing-Controlled Phenotypes in Gram-Negative Bacteria", Applied and Environmental Microbiology, 75(3), pp.567~572 (2009), American Society for Microbiology[DOI]
  63. Edisson Tello, "Synthesis of cembranoid analogues and evaluation of their potential as quorum sensing inhibitors", Bioorganic & Medicinal Chemistry, 21(1), pp.242~256 (2013), Elsevier BV[DOI]
  64. Torsten Thomas, "Diversity, structure and convergent evolution of the global sponge microbiome", Nature Communications, 7(1) (2016), Springer Science and Business Media LLC[DOI]
  65. Christopher M. Waters, "QUORUM SENSING: Cell-to-Cell Communication in Bacteria", Annual Review of Cell and Developmental Biology, 21(1), pp.319~346 (2005), Annual Reviews[DOI]
  66. P. W. Wester, "Toxicological pathology in laboratory fish: an evaluation with two species and various environmental contaminants", Ecotoxicology, 3(1), pp.21~44 (1994), Springer Science and Business Media LLC[DOI]
  67. WHO, "Antimicrobial use in aquaculture and antimicrobial resistance" (2006), WHO press
  68. Q. Yang, "Detection of quorum sensing signal molecules in the family Vibrionaceae", Journal of Applied Microbiology, 110(6), pp.1438~1448 (2011), Wiley[DOI]

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