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Effects of chitin synthesis inhibitor treatment on Lepeophtheirus salmonis (Copepoda, Caligidae) larvae


Autoři: Hulda María Harðardóttir aff001;  Rune Male aff001;  Frank Nilsen aff001;  Sussie Dalvin aff001
Působiště autorů: Sea Lice Research Centre, Department of Biological Science, University of Bergen, Bergen, Norway aff001;  Sea Lice Research Centre, Institute of Marine Research, Bergen, Bergen, Norway aff002
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222520

Souhrn

The salmon louse (Lepeophtheirus salmonis) is an ectoparasite infecting Atlantic salmon (Salmo salar), which causes substantial problems to the salmon aquaculture and threatens wild salmon. Chitin synthesis inhibitors (CSIs) are used to control L. salmonis in aquaculture. CSIs act by interfering with chitin formation and molting. In the present study, we investigated the action of four CSIs: diflubenzuron (DFB), hexaflumuron (HX), lufenuron (LF), and teflubenzuron (TFB) on larval molt. As the mode of action of CSIs remains unknown, we selected key enzymes in chitin metabolism and investigated if CSI treatment influenced the transcriptional level of these genes. All four CSIs interfered with the nauplius II molt to copepodids in a dose-dependent manner. The EC50 values were 93.2 nM for diflubenzuron, 1.2 nM for hexaflumuron, 22.4 nM for lufenuron, and 11.7 nM for teflubenzuron. Of the investigated genes, only the transcriptional level of L. salmonis chitin synthase 1 decreased significantly in hexaflumuron and diflubenzuron-treated larvae. All the tested CSIs affected the molt of nauplius II L. salmonis larvae but at different concentrations. The larvae were most sensitive to hexaflumuron and less sensitive to diflubenzuron. None of the CSIs applied had a strong impact on the transcriptional level of chitin synthesis or chitinases genes in L. salmonis. Further research is necessary to get more knowledge of the nature of the inhibition of CSI and may require methods such as studies of protein structure and enzymological studies.

Klíčová slova:

Arthropoda – Crustaceans – DNA transcription – Genetic interference – chitin – Larvae – Molting – Exoskeleton


Zdroje

1. Hamre LA, Eichner C, Caipang CMA, Dalvin ST, Bron JE, Nilsen F, et al. The Salmon Louse Lepeophtheirus salmonis (Copepoda: Caligidae) Life Cycle Has Only Two Chalimus Stages. PLoS One. 2013;8(9): 1–9. doi: 10.1371/journal.pone.0073539 24069203

2. Costello MJ. The global economic cost of sea lice to the salmonid farming industry. Can Vet J. 2009;32(1): 54–56. doi: 10.1111/j.1365-2761.2008.01011.x 19245636

3. Sun R, Liu C, Zhang H, Wang Q. Benzoylurea Chitin Synthesis Inhibitors. J Agric Food Chem. 2015;63(31): 6847–6865. doi: 10.1021/acs.jafc.5b02460 26168369

4. Becker A, Schlöder P, Steele JE, Wegener G. The regulation of trehalose metabolism in insects. Experientia. 1996;52(5): 433–439. doi: 10.1007/bf01919312 8706810

5. Muthukrishnan S, Merzendorfer H, Arakane Y, Kramer KJ. Chitin Metabolism in Insects. Insect Molecular Biology and Biochemistry. 2012. doi: 10.1016/B978-0-12-384747-8.10007–8

6. Binnington KC. Ultrastructural changes in the cuticle of the sheep blowfly, Lucilia, induced by certain insecticides and biological inhibitors. Tissue Cell. 1985;17(1): 131–140. doi: 10.1016/0040-8166(85)90021-7 3923653

7. Gangishetti U, Breitenbach S, Zander M, Saheb SK, Müller U, Schwarz H, et al. Effects of benzoylphenylurea on chitin synthesis and orientation in the cuticle of the Drosophila larva. Eur J Cell Biol. 2009;88(3): 167–180. doi: 10.1016/j.ejcb.2008.09.002 18996617

8. Perez-Farinos G, Smagghe G, Marco V, Tirry L, Castañera P. Effects of Topical Application of Hexaflumuron on Adult Sugar Beet Weevil, Aubeonymus mariaefranciscae, on Embryonic Development: Pharmacokinetics in Adults and Embryos. Pestic Biochem Physiol. 1998;61(3): 169–182. doi: 10.1006/pest.1998.2356

9. Mommaerts V, Sterk G, Smagghe G. Hazards and uptake of chitin synthesis inhibitors in bumblebees Bombus terrestris. Pest Manag Sci. 2006;62(8): 752–758. doi: 10.1002/ps.1238 16786494

10. Van Leeuwen T, Demaeght P, Osborne EJ, Dermauw W, Gohlke S, Nauen R, et al. Population bulk segregant mapping uncovers resistance mutations and the mode of action of a chitin synthesis inhibitor in arthropods. Proc Natl Acad Sci USA. 2012;109(12): 4407–12. doi: 10.1073/pnas.1200068109 22393009

11. Douris V, Steinbach D, Panteleri R, Livadaras I, Pickett JA, Van Leeuwen T, et al. Resistance mutation conserved between insects and mites unravels the benzoylurea insecticide mode of action on chitin biosynthesis. Proc Natl Acad Sci. 2016;113(51): 14692–14697. doi: 10.1073/pnas.1618258113 27930336

12. Suzuki Y, Shiotsuki T, Jouraku A, Miura K, Minakuchi C. Benzoylurea resistance in western flower thrips Frankliniella occidentalis (Thysanoptera: Thripidae): the presence of a point mutation in chitin synthase 1. J Pestic Sci. 2017;42(3): 93–96. doi: 10.1584/jpestics.D17-023 30364015

13. Mayer RT, Chen AC, DeLoach JR. Chitin synthesis inhibiting insect growth regulators do not inhibit chitin synthase. Experientia. 1981;37(4): 337–338.

14. Zhang X, Yan Zhu K. Biochemical characterization of chitin synthase activity and inhibition in the African malaria mosquito, Anopheles gambiae. Insect Sci. 2013;20(2): 158–166. doi: 10.1111/j.1744-7917.2012.01568.x 23955856

15. Norwegian Veterinary Institute. Use of therapeutic agents against salmon lice in Norwegian Aquaculture. 2016; pp:6.

16. Aaen SM, Helgesen KO, Bakke MJ, Kaur K, Horsberg TE. Drug resistance in sea lice: A threat to salmonid aquaculture. Trends Parasitol. 2015;31(2): 72–81. doi: 10.1016/j.pt.2014.12.006 25639521

17. Poley JD, Braden LM, Messmer AM, Igboeli OO, Whyte SK, Macdonald A, et al. High level efficacy of lufenuron against sea lice (Lepeophtheirus salmonis) linked to rapid impact on moulting processes. Int J Parasitol Drugs Drug Resist. 2018;8(2): 174–188. doi: 10.1016/j.ijpddr.2018.02.007 29627513

18. Skilbrei OT, Espedal PG, Nilsen F, Perez Garcia E, Glover KA. Evaluation of emamectin benzoate and substance EX against salmon lice in sea-ranched Atlantic salmon smolts. Dis Aquat Organ. 2015;113(3): 187–194. doi: 10.3354/dao02832 25850396

19. Olsvik PA, Samuelsen OB, Agnalt A-L, Lunestad BT. Transcriptional responses to teflubenzuron exposure in European lobster (Homarus gammarus). Aquat Toxicol. 2015;167: 143–156. doi: 10.1016/j.aquatox.2015.07.008 26318677

20. Harðardóttir HM, Male R, Nilsen F, Eichner C, Dondrup M, Dalvin S. Chitin synthesis and degradation in Lepeophtheirus salmonis: Molecular characterization and gene expression profile during synthesis of a new exoskeleton. Comp Biochem Physiol Part A. 2019;227: 123–133. doi: 10.1016/j.cbpa.2018.10.008 30326269

21. Eichner C, Harasimczuk E, Nilsen F, Grotmol S, Dalvin S. Molecular characterisation and functional analysis of LsChi2, a chitinase found in the salmon louse (Lepeophtheirus salmonis salmonis, Krøyer 1838). Exp Parasitol. 2015;151–152: 39–48. doi: 10.1016/j.exppara.2015.01.011 25643862

22. Hamre LA, Glover KA, Nilsen F. Establishment and characterisation of salmon louse (Lepeophtheirus salmonis (Krøyer 1837)) laboratory strains. Parasitol Int. 2009;58(4): 451–460. doi: 10.1016/j.parint.2009.08.009 19732850

23. Aaen SM, Horsberg TE. A screening of multiple classes of pharmaceutical compounds for effect on preadult salmon lice Lepeophtheirus salmonis. J Fish Dis. 2016;39(19): 1213–1223. doi: 10.1111/jfd.12463 27037538

24. Eichner C, Nilsen F, Grotmol S, Dalvin S. A method for stable gene knock-down by RNA interference in larvae of the salmon louse (Lepeophtheirus salmonis). Exp Parasitol. 2014;140: 44–51. doi: 10.1016/j.exppara.2014.03.014 24632188

25. Frost P, Nilsen F. Validation of reference genes for transcription profiling in the salmon louse, Lepeophtheirus salmonis, by quantitative real-time PCR. Vet Parasitol. 2003;118(1–2): 169–174. doi: 10.1016/j.vetpar.2003.09.020 14651887

26. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and. Methods. 2001;25(2): 402–408. doi: 10.1006/meth.2001.1262 11846609

27. Post LC, de Jong BJ, Vincent WR. 1-(2,6-disubstituted benzoyl)-3-phenylurea insecticides: Inhibitors of chitin synthesis. Pestic Biochem Physiol. 1974;4(4): 473–483. doi: 10.1016/0048-3575(74)90072-8

28. van Eck WH. Mode of action of two benzoylphenyl ureas as inhibitors of chitin synthesis in insects. Insect Biochem. 1979;9(3): 295–300. doi: 10.1016/0020-1790(79)90009-X

29. Branson EJ, Ronsberg SS, Ritchie G. Efficacy of teflubenzuron (Calicide) for the treatment of sea lice, Lepeophtheirus salmonis (Kroyer 1838), infestations of farmed Atlantic salmon (Salmo salar L.). Aquac Res. 2000;31(11): 861–867.

30. Ritchie G, Rønsberg SS, Hoff KA, Branson EJ. Clinical efficacy of teflubenzuron (Calicide®) for the treatment of Lepeophtheirus salmonis infestations of farmed Atlantic salmon Salmo salar at low water temperatures. Dis Aquat Organ. 2002;51(2): 101–106. doi: 10.3354/dao051101 12363081

31. Christiansen ME, Costlow JD, Monroe RJ. Effects of the insect growth regulator Dimilin (TH 6040) on larval development of two estuarine crabs. Mar Biol. 1978;50(1): 29–36. doi: 10.1007/BF00390539

32. Karimazadeh R, Hejazi MJ, Rahimzadeh Khoei F, Moghaddam M. Laboratory evalution of five chitin synthesis inihibtors against the Colorado potato beetle, Leptinotarsa decemlineate. J Insect Sci. 2007;7(50): 1–6.

33. Savitz JD, Wright DA, Smucker RA. Toxic Effects of the Insecticide Diflubenzuron (Dimilin ®) on Survival and Development of Nauplii of the Estuarine Copepod, Eurytemora affinis. Mar Eviron Reasearch. 1994;37(3): 297–312.

34. Christiansen ME, Costlow JD. Ultrastructural Study of the Exoskeleton of the Estuarine Crab Rhithropanopeus harrisii: Effect of the Insect Growth Regulator Dimilin (Diflubenzuron) on the Formation of the Larval Cuticle. Mar Biol. 1982;66(3): 217–226.

35. Binnington KC. Ultrastructural changes in the cuticle of the sheep blowfly, Lucilia, induced by certain insecticides and biological inhibitors. Tissue Cell. 1985;17(1): 131–140. doi: 10.1016/0040-8166(85)90021-7 3923653

36. Gijswijt MJ, Deul DH, de Jong BJ. Inhibition of chitin synthesis by benzoyl-phenylurea insecticides, III. Similarity in action in Pieris brassicae (L.) with Polyoxin D. Pestic Biochem Physiol. 1979;12(1): 87–94. doi: 10.1016/0048-3575(79)90098-1

37. Al-Mokhlef AA, Mariy FM, Emam AK, Ali GM. Effect of teflubenzuron on ultrastructure and components of the integument in Schistocerca gregaria (Forskal) 5th instar nymphs. Ann Agric Sci. 2012;57(1): 1–6. doi: 10.1016/j.aoas.2012.03.010

38. Cunningham PA. A Review of Toxicity Testing and Degradation Studies Used to Predict the Effects of Diflubenzuron (Dimilin ®) on Estuarine Crustaceans. 1986;40(1): 63–86.

39. Saidy EL. Detoxification Mechanisms of Diflubenzuron and Teflubenzuron the Larvae of Spodoptera littoraiis (Boisd.). Pestic Biochem Physiol. 1989;222: 211–222.

40. Khajepour S, Izadi H, Asari MJ. Evaluation of Two Formulated Chitin Synthesis Inhibitors, Hexaflumuron and Lufenuron Against the Raisin Moth, Ephestia figulilella. J Insect Sci. 2012;12(102): 1–7. doi: 10.1673/031.012.10201 23425138

41. Coppen GDA, Jepsont PC. Comparative Laboratory Evaluation of the Acute and Chronic Toxicology of Diflubenzuron, Hexaflumuron and Teflubenzuron against I1 Instar Desert Locust, (Schistocerca gregaria) (Orthoptera: Acrididae). Pestic Sci. 1996;46: 183–190.

42. Macken A, Lillicrap A, Langfold K. Benzoylurea pesticides used as veterinary medicines in aquaculture: risk and developmental effects on nontarget crustaceans. Enviro Toxic and Chem. 2015;34(7): 1533–1542. doi: 10.1002/etc.2920 25663472

43. Nimmo DR, Hamaker TL, Moore JC, Sommers CA. Effect of Diflubenzuron on an Estuarine Crustacean. Bull Environ Toxicol. 1979;22(6): 767–770.

44. Julin AM, Sanders HO. Toxicity of the IGR, diflubenzuron, to freshwater invertebrates and fishes. Mosquito News. 1978. pp. 256–259.

45. Weis JS, Cohen R, Kwiatkowsi JK. Effects of diflubenzuron on limb regeneration and molting in the fiddler crab, Uca pugilator. Aquat Toxicol. 1987;10: 279–290.

46. Langford KH, Oxnevad S, Schoyen M, Thomas KV. Environmental screening of veterinary medicines used in aquaculture—diflubenzuron and teflubenzuron. 2011.

47. Tom M, Manfrin C, Chung SJ, Sagi A, Gerdol M, De Moro G, et al. Expression of cytoskeletal and molt-related genes is temporally scheduled in the hypodermis of the crayfish Procambarus clarkii during premolt. J Exp Biol. 2014;217: 4193–4202. doi: 10.1242/jeb.109009 25278476

48. Tan S, Degnan B, Lehnert S. The Penaeus monodon Chitinase 1 Gene Is Differentially Expressed in the Hepatopancreas During the Molt Cycle. Mar Biotechnol (NY). 2000;2: 126–135. doi: 10.1007/s101269900016 10811951

49. Li X, Xu Z, Zhou G, Lin H, Zhou J, Zeng Q, et al. Molecular characterization and expression analysis of five chitinases associated with molting in the Chinese mitten crab, Eriocheir sinensis. Comp Biochem Physiol Part—B Biochem Mol Biol. 2015;187: 110–120. doi: 10.1016/j.cbpb.2015.05.007 26005205

50. Niu S, Yang L, Zuo H, Zheng J, Weng S, He J, et al. A chitinase from pacific white shrimp Litopenaeus vannamei involved in immune regulation. Dev Comp Immunol. 2018;85: 161–169. doi: 10.1016/j.dci.2018.04.013 29678533

51. Abehsera S, Glazer L, Tynyakov J, Plaschkes I, Chalifa-Caspi V, Khalaila I, et al. Binary gene expression patterning of the molt cycle: The case of chitin metabolism. PLoS One. 2015;10(4): 1–20. doi: 10.1371/journal.pone.0122602 25919476

52. Merzendorfer H, Zimoch L. Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases. J Exp Biol. 2003;206: 4393–4412. doi: 10.1242/jeb.00709 14610026

53. Sandlund L, Nilsen F, Male R, Dalvin S. The ecdysone receptor (EcR) is a major regulator of tissue development and growth in the marine salmonid ectoparasite, Lepeophtheirus salmonis (Copepoda, Caligidae). Mol Biochem Parasitol. 2016;208(2): 65–73. doi: 10.1016/j.molbiopara.2016.06.007 27345580

54. Merzendorfer H, Kim HS, Chaudhari SS, Kumari M, Specht CA, Butcher S, et al. Genomic and proteomic studies on the effects of the insect growth regulator diflubenzuron in the model beetle species Tribolium castaneum. Insect Biochem Mol Biol. 2012;42(4): 264–276. doi: 10.1016/j.ibmb.2011.12.008 22212827

55. Zhang J, Zhu KY. Characterization of a chitin synthase cDNA and its increased mRNA level associated with decreased chitin synthesis in Anopheles quadrimaculatus exposed to diflubenzuron. Insect Biochem Mol Biol. 2006;36(9): 712–725. doi: 10.1016/j.ibmb.2006.06.002 16935220

56. Xia W-K, Ding T-B, Niu J-Z, Liao C-Y, Zhong R, Yang W-J, et al. Exposure to Diflubenzuron Results in an Up-Regulation of a Chitin Synthase 1 Gene in Citrus Red Mite, Panonychus citri (Acari: Tetranychidae). Int J Mol Sci. 2014;15(3): 3711–3728. doi: 10.3390/ijms15033711 24590130


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