Characterization and function of the first antibiotic isolated from a vent organism: The extremophile metazoan Alvinella pompejana

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Tasiemski, Aurélie ^a   Jung, Sascha ^b   Boidin Wichlacz, Céline ^a   Jollivet, Didier ^c   Cuvillier Hot, Virginie ^a   Pradillon, Florence ^d   Vetriani, Costantino ^e   Hecht, Oliver ^b   Sönnichsen, Frank D ^b   Gelhaus, Christoph ^b   Hung, Chien Wen ^b   Tholey, Andreas ^b   Leippe, Matthias ^b   Grötzinger, Joachim ^b   Gaill, Françoise ^f  

^a UNIV LILLE   (France)

^b UNIVERSITY OF KIEL   (Germany)

^c SORBONNE UNIVERSITÉ   (France)

^d IFREMER   (France)

^e RUTGERS UNIVERSITY   (United States)

^f MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALVINELLACIN; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG; ANTIMICROBIAL CATIONIC PEPTIDE;

ALVINELLA POMPEJANA; ARTICLE; BIOASSAY; CONTROLLED STUDY; EPIBIONT; GENE EXPRESSION; GENE INDUCTION; GENE STRUCTURE; HYDROTHERMAL VENT; MICROBIAL COMMUNITY; MICROFLORA; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYCHAETA; PROTEIN PURIFICATION; PROTEIN TERTIARY STRUCTURE; SEQUENCE ANALYSIS; SHIPBOARD BIOLOGICAL ASSAY; SPECIES INVASION; WORM; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; ECOSYSTEM; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PROTEIN SECONDARY STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; ECOSYSTEM; EVOLUTION, MOLECULAR; HYDROTHERMAL VENTS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POLYCHAETA; PROTEIN STRUCTURE, SECONDARY;

EID: 84899719879     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095737     Document Type: Article

References (41)

1. Le Bris N, Gaill F (2007) How does the annelid Alvinella pompejana deal with an extreme hydrothermal environment? Rev Environ Sci Biotechnol 6: 197-221. (Pubitemid 46130088)
2. Girguis PR and Lee RW (2006) Thermal preference and tolerance of alvinellids. Science 312: 231.
3. Cary SC, Cottrell MT, Stein JL, Camacho F, Desbruyeres D (1997) Molecular Identification and Localization of Filamentous Symbiotic Bacteria Associated with the Hydrothermal Vent Annelid Alvinella pompejana. Appl Environ Microbiol 63: 1124-1130. (Pubitemid 27098505)
4. Cary SC, Shank T and Stein J (1998) Worms basks in extreme temperatures. Nature 391: 545-546.
5. Chevaldonné P, Desbruyères D, Childress JJ (1992) Some like it hot. and some even hotter. Nature 359: 593-594.
6. Ravaux J, Hamel G, Zbinden M, Tasiemski A, Boutet I, et al. (2013) Thermal limit for metazoan life in question: in vivo heat tolerance of the Pompeii worm. PLoSONE 8.
7. Grzymski JJ, Murray AE, Campbell BJ, Kaplarevic M, Gao GR, et al. (2008) Metagenome analysis of an extreme microbial symbiosis reveals eurythermal adaptation and metabolic flexibility. Proc Natl Acad Sci U S A 105: 17516-17521.
8. Dale C, Moran NA (2006) Molecular interactions between bacterial symbionts and their hosts. Cell 126: 453-465. (Pubitemid 44163611)
9. Tennessen JA (2005) Molecular evolution of animal antimicrobial peptides: widespread moderate positive selection. J Evol Biol 18: 1387-1394.
10. Login FH, Balmand S, Vallier A, Vincent-Monegat C, Vigneron A, et al. (2011) Antimicrobial peptides keep insect endosymbionts under control. Science 334: 362-365.
11. Sperstad SV, Haug T, Blencke HM, Styrvold OB, Li C, et al. (2011) Antimicrobial peptides from marine invertebrates: challenges and perspectives in marine antimicrobial peptide discovery. Biotechnol Adv 29: 519-530.
12. Austin B (1988) Marine Microbiology. Cambridge University Press.
13. Stetter KO, Konig H, Stackebrandt E (1983) Pyrodictium gen.nov., a New Genus of Submarine Disc-Shaped Sulphur Reducing Archaebacteria Growing Optimally at 105 degrees C. Syst Appl Microbiol 4: 535-551.
14. Vetriani C, Speck MD, Ellor SV, Lutz RA, Starovoytov V (2004) Thermovibrio ammonificans sp. nov., a thermophilic, chemolithotrophic, nitrate-ammonifying bacterium from deep-sea hydrothermal vents. Int J Syst Evol Microbiol 54: 175-181. (Pubitemid 38181287)
15. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, et al. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6: 277-293.
16. Johnson BA (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol Biol 278: 313-352.
17. Güntert P (2004) Automated NMR structure calculation with CYANA. Methods Mol Biol 278: 353-378.
18. Fedders H, Leippe M (2008) A reverse search for antimicrobial peptides in Ciona intestinalis: identification of a gene family expressed in hemocytes and evaluation of activity. Dev Comp Immunol 32: 286-298. (Pubitemid 350180077)
19. Herbst R, Ott C, Jacobs T, Marti T, Marciano-Cabral F, et al. (2002) Poreforming polypeptides of the pathogenic protozoon Naegleria fowleri. J Biol Chem 277: 22353-22360. (Pubitemid 34967203)
20. Leippe M, Ebel S, Schoenberger OL, Horstmann RD, Muller-Eberhard HJ (1991) Pore-forming peptide of pathogenic Entamoeba histolytica. Proc Natl Acad Sci U S A 88: 7659-7663. (Pubitemid 21915213)
21. Gagniere N, Jollivet D, Boutet I, Brelivet Y, Busso D, et al. (2010) Insights into metazoan evolution from Alvinella pompejana cDNAs. BMC Genomics 11: 634.
22. Baert JL, Britel M, Slomianny MC, Delbart C, Fournet B, et al. (1991) Yolk protein in leech. Identification, purification and characterization of vitellin and vitellogenin. Eur J Biochem 201: 191-198.
23. Salzet M, Bulet P, Wattez C, Malecha J (1994) FMRFamide-related peptides in the sex segmental ganglia of the Pharyngobdellid leech Erpobdella octoculata. Identification and involvement in the control of hydric balance. Eur J Biochem 221: 269-275. (Pubitemid 24120571)
24. Boidin-Wichlacz C, Vergote D, Slomianny C, Jouy N, Salzet M, et al. (2012) Morphological and functional characterization of leech circulating blood cells: role in immunity and neural repair. Cell Mol Life Sci 69: 1717-1731.
25. Tasiemski A (2008) Antimicrobial peptides in annelids. Invertebrate Survival Journal 166.
26. Salzet M, Tasiemski A, Cooper E (2006) Innate immunity in lophotrochozoans: the annelids. Curr Pharm Des 12: 3043-3050. (Pubitemid 44227568)
27. Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415: 389-395.
28. Willander H, Hermansson E, Johansson J, Presto J (2011) BRICHOS domain associated with lung fibrosis, dementia and cancer-a chaperone that prevents amyloid fibril formation? FEBS J 278: 3893-3904.
29. Andra J, Jakovkin I, Grotzinger J, Hecht O, Krasnosdembskaya AD, et al. (2008) Structure and mode of action of the antimicrobial peptide arenicin. Biochem J 410: 113-122. (Pubitemid 351300330)
30. Maroti G, Kereszt A, Kondorosi E, Mergaert P (2011) Natural roles of antimicrobial peptides in microbes, plants and animals. Res Microbiol 162: 363-374.
31. Sanchez-Pulido L, Devos D, Valencia A (2002) BRICHOS: a conserved domain in proteins associated with dementia, respiratory distress and cancer. Trends Biochem Sci 27: 329-332. (Pubitemid 34756511)
32. Zhu S, Gao B (2012) Evolutionary origin of beta-defensins. Dev Comp Immunol.
33. Struck TH, Paul C, Hill N, Hartmann S, Hosel C, et al. (2011) Phylogenomic analyses unravel annelid evolution. Nature 471: 95-98.
34. Sicot FX, Mesnage M, Masselot M, Exposito JY, Garrone R, et al. (2000) Molecular adaptation to an extreme environment: origin of the thermal stability of the pompeii worm collagen. J Mol Biol 302: 811-820.
35. Hourdez S, Lallier FH, De Cian MC, Green BN, Weber RE, et al. (2000) Gas transfer system in Alvinella pompejana (Annelida polychaeta, Terebellida): functional properties of intracellular and extracellular hemoglobins. Physiol Biochem Zool 73: 365-373.
36. Nakagawa S, Takaki Y, Shimamura S, Reysenbach AL, Takai K, et al. (2007) Deep-sea vent epsilon-proteobacterial genomes provide insights into emergence of pathogens. Proc Natl Acad Sci U S A 104: 12146-12150. (Pubitemid 47185644)
37. Cottin D, Ravaux J, Leger N, Halary S, Toullec JY, et al. (2008) Thermal biology of the deep-sea vent annelid Paralvinella grasslei : in vivo studies. J Exp Biol 211: 2196-2204.
38. Bonch-Osmolovskaya EA, Perevalova AA, Kolganova TV, Rusanov, II, Jeanthon C, et al. (2011) Activity and distribution of thermophilic prokaryotes in hydrothermal fluid, sulfidic structures, and sheaths of alvinellids (East Pacific Rise, 13 degrees N). Appl Environ Microbiol 77: 2803-2806.
39. Moussard H, Moreira D, Cambon-Bonavita MA, Lopez-Garcia P, Jeanthon C (2006) Uncultured Archaea in a hydrothermal microbial assemblage: phylogenetic diversity and characterization of a genome fragment from a euryarchaeote. FEMS Microbiol Ecol 57: 452-469. (Pubitemid 44200469)
40. Herwald H, Egesten A (2011) The discovery of pathogen recognition receptors (PRR). J Innate Immun 3: 435-436.
41. Salzman NH, Hung K, Haribhai D, Chu H, Karlsson-Sjoberg J, et al. (2009) Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 11: 76-83.