Antimicrobial peptides in oyster hemolymph: The bacterial connection

Fish and Shellfish Immunology

Volumn 34, Issue 6, 2013, Pages 1439-1447

  Defer, Diane ^a,b   Desriac, Florie ^a   Henry, Joël ^c   Bourgougnon, Nathalie ^b   Baudy Floc'h, Michèle ^d   Brillet, Benjamin ^a   Le Chevalier, Patrick ^a   Fleury, Yannick ^a  

^a UNIVERSITÉ DE BREST   (France)

^b UNIVERSITÉ DE BRETAGNE SUD   (France)

^c UNIVERSITÉ DE CAEN   (France)

^d UNIVERSITÉ DE RENNES 1   (France)

Author keywords

Antimicrobial peptide; Bacteriocin Like Inhibitory Substance; Bivalve; Hemolymph; Resident bacteria

Indexed keywords

BACTERIA (MICROORGANISMS); BIVALVIA; OSTREIDAE; PSEUDOALTEROMONAS; VIBRIO;

EID: 84877622481     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2013.03.357     Document Type: Article

References (61)

1. Zweifel U.L., Hagstrom A. Total counts of marine bacteria include a large fraction of non-nucleoid-containing bacteria (Ghosts). Appl Environ Microbiol 1995, 61:2180-2185.
2. Suttle C.A. Viruses in the sea. Nature 2005, 437:356-361. 10.1038/nature04160.
3. Otero-González A.J., Magalhães B.S., Garcia-Villarino M., López-Abarrategui C., Sousa D.A., Dias S.C., et al. Antimicrobial peptides from marine invertebrates as a new frontier for microbial infection control. FASEB J 2010, 24:1320-1334. 10.1096/fj.09-143388.
4. Afacan N.J., Yeung A.T.Y., Pena O.M., Hancock R.E.W. Therapeutic potential of host defense peptides in antibiotic-resistant infections. Curr Pharm Des 2012, 18:807-819.
5. Nakatsuji T., Gallo R.L. Antimicrobial peptides: old molecules with new ideas. JInvest Dermatol 2012, 132:887-895. 10.1038/jid.2011.387.
6. Pasupuleti M., Schmidtchen A., Malmsten M. Antimicrobial peptides: key components of the innate immune system. Crit Rev Biotechnol 2012, 32:143-171. 10.3109/07388551.2011.594423.
7. Sperstad S.V., Haug T., Blencke H.-M., Styrvold O.B., Li C., Stensvåg K. Antimicrobial peptides from marine invertebrates: challenges and perspectives in marine antimicrobial peptide discovery. Biotechnol Adv 2011, 29:519-530. 10.1016/j.biotechadv.2011.05.021.
8. Wang G., Li X., Wang Z. APD2: the updated antimicrobial peptide database and its application in peptide design. Nucleic Acids Res 2009, 37:D933-D937. 10.1093/nar/gkn823.
9. Thomas S., Karnik S., Barai R.S., Jayaraman V.K., Idicula-Thomas S.C.A.M.P. a useful resource for research on antimicrobial peptides. Nucleic Acids Res 2010, 38:D774-D780. 10.1093/nar/gkp1021.
10. Seshadri Sundararajan V., Gabere M.N., Pretorius A., Adam S., Christoffels A., Lehväslaiho M., et al. DAMPD: a manually curated antimicrobial peptide database. Nucleic Acids Res 2011, 10.1093/nar/gkr1063.
11. Seebah S., Suresh A., Zhuo S., Choong Y.H., Chua H., Chuon D., et al. Defensins knowledgebase: a manually curated database and information source focused on the defensins family of antimicrobial peptides. Nucleic Acids Res 2007, 35:D265-D268. 10.1093/nar/gkl866.
12. Hammami R., Zouhir A., Le Lay C., Ben Hamida J., Fliss I. BACTIBASE second release: a database and tool platform for bacteriocin characterization. BMC Microbiol 2010, 10:22. 10.1186/1471-2180-10-22.
13. Tincu J.A., Taylor S.W. Antimicrobial peptides from marine invertebrates. Antimicrob Agents Chemother 2004, 48:3645-3654. 10.1128/AAC.48.10.3645-3654.2004.
14. Rajanbabu V., Chen J.-Y. Applications of antimicrobial peptides from fish and perspectives for the future. Peptides 2011, 32:415-420. 10.1016/j.peptides.2010.11.005.
15. Hubert F., Noël T., Roch P. Amember of the arthropod defensin family from edible mediterranean mussels (Mytilus galloprovincialis). Eur J Biochem 1996, 240:302-306. 10.1111/j.1432-1033.1996.0302h.x.
16. Charlet M., Chernysh S., Philippe H., Hetru C., Hoffmann J.A., Bulet P. Innate immunity. JBiol Chem 1996, 271:21808-21813. 10.1074/jbc.271.36.21808.
17. Mitta G., Hubert F., Dyrynda E.A., Boudry P., Roch P. Mytilin B and MGD2, two antimicrobial peptides of marine mussels: gene structure and expression analysis. Dev Comp Immunol 2000, 24:381-393.
18. Mitta G., Vandenbulcke F., Noël T., Romestand B., Beauvillain J.C., Salzet M., et al. Differential distribution and defence involvement of antimicrobial peptides in mussel. JCell Sci 2000, 113(Pt 15):2759-2769.
19. Gerdol M., De Moro G., Manfrin C., Venier P., Pallavicini A. Big defensins and mytimacins, new AMP families of the mediterranean mussel Mytilus galloprovincialis. Dev Comp Immunol 2012, 36:390-399. 10.1016/j.dci.2011.08.003.
20. Mitta G., Vandenbulcke F., Hubert F., Roch P. Mussel defensins are synthesised and processed in granulocytes then released into the plasma after bacterial challenge. JCell Sci 1999, 112(Pt 23):4233-4242.
21. Seo J.-K., Crawford J.M., Stone K.L., Noga E.J. Purification of a novel arthropod defensin from the American oyster, Crassostrea virginica. Biochem Biophysical Res Commun 2005, 338:1998-2004. 10.1016/j.bbrc.2005.11.013.
22. Gueguen Y., Herpin A., Aumelas A., Garnier J., Fievet J., Escoubas J.-M., et al. Characterization of a defensin from the oyster Crassostrea gigas. Recombinant production, folding, solution structure, antimicrobial activities, and gene expression. JBiol Chem 2006, 281:313-323. 10.1074/jbc.M510850200.
23. Gonzalez M., Gueguen Y., Desserre G., De Lorgeril J., Romestand B., Bachère E. Molecular characterization of two isoforms of defensin from hemocytes of the oyster Crassostrea gigas. Dev Comp Immunol 2007, 31:332-339. 10.1016/j.dci.2006.07.006.
24. Rosa R.D., Santini A., Fievet J., Bulet P., Destoumieux-Garzón D., Bachère E. Big defensins, a diverse family of antimicrobial peptides that follows different patterns of expression in hemocytes of the oyster Crassostrea gigas. PLoS One 2011, 6. 10.1371/journal.pone.0025594.
25. Schmitt P., Wilmes M., Pugnière M., Aumelas A., Bachère E., Sahl H.-G., et al. Insight into invertebrate defensin mechanism of action. JBiol Chem 2010, 285:29208-29216. 10.1074/jbc.M110.143388.
26. Hubert F., Van der Knaap W., Noël T., Roch P. Cytotoxic and antibacterial properties of Mytilus galloprovincialis, Ostrea edulis and Crassostrea gigas (bivalve molluscs) hemolymph. Aquatic Living Resour 1996, 9:115-124. 10.1051/alr:1996015.
27. Anderson R.S., Beaven A.E. Antibacterial activities of oyster ( Crassostrea virginica) and mussel ( Mytilus edulis and Geukensia demissa) plasma. Aquatic Living Resour 2001, 14:343-349. 10.1016/S0990-7440(01)01143-3.
28. Defer D., Bourgougnon N., Fleury Y. Screening for antibacterial and antiviral activities in three bivalve and two gastropod marine molluscs. Aquaculture 2009, 293:1-7. 10.1016/j.aquaculture.2009.03.047.
29. Schmitt P., Rosa R.D., Duperthuy M., De Lorgeril J., Bachère E., Destoumieux-Garzón D. The antimicrobial defense of the Pacific oyster, Crassostrea gigas. How diversity may compensate for scarcity in the regulation of resident/pathogenic microflora. Front Microbiol 2012, 3:160. 10.3389/fmicb.2012.00160.
30. Wiegand I., Hilpert K., Hancock R.E.W. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat Protoc 2008, 3:163-175. 10.1038/nprot.2007.521.
31. Fleury Y., Dayem M.A., Montagne J.J., Chaboisseau E., Le Caer J.P., Nicolas P., et al. Covalent structure, synthesis, and structure-function studies of mesentericin Y 105(37), a defensive peptide from gram-positive bacteria Leuconostoc mesenteroides. JBiol Chem 1996, 271:14421-14429.
32. Schägger H., Von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100kDa. Anal. Biochem 1987, 166:368-379.
33. Bhunia A.K., Johnson M.G. Amodified method to directly detect in SDS-PAGE the bacteriocin of Pediococcus acidilactici. Lett Appl Microbiol 1992, 15:5-7. 10.1111/j.1472-765X.1992.tb00709.x.
34. Stackebrandt E, Ebers J. Taxonomic parameters revisited: tarnished gold standards. 2006;6:152-6.
35. Desriac F., Defer D., Bourgougnon N., Brillet B., Le Chevalier P., Fleury Y. Bacteriocin as weapons in the marine animal-associated bacteria warfare: inventory and potential applications as an aquaculture probiotic. Mar Drugs 2010, 8:1153-1177. 10.3390/md8041153.
36. Yeaman M.R., Yount N.Y. Mechanisms of antimicrobial peptide action and resistance. Pharmacol Rev 2003, 55:27-55. 10.1124/pr.55.1.2.
37. Gueguen Y., Romestand B., Fievet J., Schmitt P., Destoumieux-Garzón D., Vandenbulcke F., et al. Oyster hemocytes express a proline-rich peptide displaying synergistic antimicrobial activity with a defensin. Mol Immunol 2009, 46:516-522. 10.1016/j.molimm.2008.07.021.
38. Gonzalez M., Gueguen Y., Destoumieux-Garzón D., Romestand B., Fievet J., Pugnière M., et al. Evidence of a bactericidal permeability increasing protein in an invertebrate, the Crassostrea gigas Cg-BPI. Proc Natl Acad Sci 2007, 104:17759-17764. 10.1073/pnas.0702281104.
39. Schmitt P., Lorgeril J de, Gueguen Y., Destoumieux-Garzón D., Bachère E. Expression, tissue localization and synergy of antimicrobial peptides and proteins in the immune response of the oyster Crassostrea gigas. Dev Comp Immunol 2012, 37:363-370. 10.1016/j.dci.2012.01.004.
40. Field D., Hill C., Cotter P.D., Ross R.P. The dawning of a "golden era" in lantibiotic bioengineering. Mol Microbiol 2010, 78:1077-1087. 10.1111/j.1365-2958.2010.07406.x.
41. Zhang G., Fang X., Guo X., Li L., Luo R., Xu F., et al. The oyster genome reveals stress adaptation and complexity of shell formation. Nature 2012, 490:49-54. 10.1038/nature11413.
42. Gueguen Y., Cadoret J.P., Flament D., Barreau-Roumiguière C., Girardot A.L., Garnier J., et al. Immune gene discovery by expressed sequence tags generated from hemocytes of the bacteria-challenged oyster, Crassostrea gigas. Gene 2003, 303:139-145.
43. Fontana R., Mendes M.A., Souza BM de, Konno K., César L.M.M., Malaspina O., et al. Jelleines: a family of antimicrobial peptides from the royal Jelly of honeybees (Apis mellifera). Peptides 2004, 25:919-928. 10.1016/j.peptides.2004.03.016.
44. Caboche S., Pupin M., Leclère V., Fontaine A., Jacques P., Kucherov G. NORINE: a database of nonribosomal peptides. Nucleic Acids Res 2008, 36:D326-D331. 10.1093/nar/gkm792.
45. Olafsen J.A., Mikkelsen H.V., Giæver H.M., Høvik Hansen G. Indigenous bacteria in hemolymph and tissues of marine bivalves at low temperatures. Appl Environ Microbiol 1993, 59:1848-1854.
46. Garnier M., Labreuche Y., Garcia C., Robert M., Nicolas J.-L. Evidence for the involvement of pathogenic bacteria in summer mortalities of the Pacific oyster Crassostrea gigas. Microb Ecol 2007, 53:187-196. 10.1007/s00248-006-9061-9.
47. Bowman J.P. Bioactive compound synthetic capacity and ecological significance of marine bacterial genus pseudoalteromonas. Mar Drugs 2007, 5:220-241.
48. Flemer B., Kennedy J., Margassery L.M., Morrissey J.P., O'Gara F., Dobson A.D.W. Diversity and antimicrobial activities of microbes from two Irish marine sponges, Suberites carnosus and Leucosolenia sp. JAppl Microbiol 2012, 112:289-301. 10.1111/j.1365-2672.2011.05211.x.
49. Gram L., Melchiorsen J., Bruhn J.B. Antibacterial activity of marine culturable bacteria collected from a global sampling of ocean surface waters and surface swabs of marine organisms. Mar Biotechnol 2010, 12:439-451. 10.1007/s10126-009-9233-y.
50. Romanenko L.A., Uchino M., Kalinovskaya N.I., Mikhailov V.V. Isolation, phylogenetic analysis and screening of marine mollusc-associated bacteria for antimicrobial, hemolytic and surface activities. Microbiol Res 2008, 163:633-644.
51. Pinkerton D.M., Banwell M.G., Garson M.J., Kumar N., De Moraes M.O., Cavalcanti B.C., et al. Antimicrobial and cytotoxic activities of synthetically derived tambjamines C and E - J, BE-18591, and a related alkaloid from the marine bacterium Pseudoalteromonas tunicata. Chem Biodivers 2010, 7:1311-1324. 10.1002/cbdv.201000030.
52. Murphy A.C., Fukuda D., Song Z., Hothersall J., Cox R.J., Willis C.L., et al. Engineered thiomarinol antibiotics active against MRSA are generated by mutagenesis and mutasynthesis of Pseudoalteromonas SANK73390. Angew Chem Int Ed Engl 2011, 50:3271-3274. 10.1002/anie.201007029.
53. Hayashida-Soiza G., Uchida A., Mori N., Kuwahara Y., Ishida Y. Purification and characterization of antibacterial substances produced by a marine bacterium Pseudoalteromonas haloplanktis strain. JAppl Microbiol 2008, 105:1672-1677. 10.1111/j.1365-2672.2008.03878.x.
54. Kalinovskaya N.I., Ivanova E.P., Alexeeva Y.V., Gorshkova N.M., Kuznetsova T.A., Dmitrenok A.S., et al. Low-molecular-weight, biologically active compounds from marine Pseudoalteromonas species. Curr Microbiol 2004, 48:441-446. 10.1007/s00284-003-4240-0.
55. Longeon A., Peduzzi J., Barthélemy M., Corre S., Nicolas J.-L., Guyot M. Purification and partial identification of novel antimicrobial protein from marine bacterium Pseudoalteromonas species strain X153. Mar Biotechnol 2004, 6:633-641. 10.1007/s10126-004-3009-1.
56. Gómez D., Espinosa E., Bertazzo M., Lucas-Elío P., Solano F., Sanchez-Amat A. The macromolecule with antimicrobial activity synthesized by Pseudoalteromonas luteoviolacea strains is an L-amino acid oxidase. Appl Microbiol Biotechnol 2008, 79:925-930. 10.1007/s00253-008-1499-x.
57. Yu M., Wang J., Tang K., Shi X., Wang S., Zhu W.-M., et al. Purification and characterization of antibacterial compounds of Pseudoalteromonas flavipulchra JG1. Microbiology 2011, 158:835-842. 10.1099/mic.0.055970-0.
58. Duquesne S., Destoumieux-Garzón D., Peduzzi J., Rebuffat S. Microcins, gene-encoded antibacterial peptides from enterobacteria. Nat Prod Rep 2007, 24:708-734. 10.1039/b516237h.
59. De Vuyst L., Leroy F. Bacteriocins from lactic acid bacteria: production, purification, and food applications. JMol Microbiol Biotechnol 2007, 13:194-199. 10.1159/000104752.
60. Shnit-Orland M., Kushmaro A. Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol Ecol 2009, 67:371-380. 10.1111/j.1574-6941.2008.00644.x.
61. Kvennefors E.C.E., Sampayo E., Kerr C., Vieira G., Roff G., Barnes A.C. Regulation of bacterial communities through antimicrobial activity by the coral holobiont. Microb Ecol 2012, 63:605-618. 10.1007/s00248-011-9946-0.