The opportunistic marine pathogen Vibrio parahaemolyticus becomes virulent by acquiring a plasmid that expresses a deadly toxin

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 34, 2015, Pages 10798-10803

  Lee, Chung Te ^a,b   Chen, I Tung ^a,c   Yang, Yi Ting ^a,c   Ko, Tzu Ping ^d   Huang, Yun Tzu ^a   Huang, Jiun Yan ^a   Huang, Ming Fen ^e   Lin, Shin Jen ^a   Chen, Chien Yu ^c   Lin, Shih Shuen ^c   Lightner, Donald V ^f   Wang, Han Ching ^a   Wang, Andrew H J ^d   Wang, Hao Ching ^e   Hor, Lien I ^b   Lo, Chu Fang ^a,c  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

^e TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^f UNIVERSITY OF ARIZONA   (United States)

Author keywords

AHPND; Pir toxin; Shrimp; Vibrio parahaemolyticus; Virulence plasmid

Indexed keywords

BACTERIAL TOXIN; HETERODIMER; PHOTORHABDUS INSECT RELATED TOXIN A; PHOTORHABDUS INSECT RELATED TOXIN B; UNCLASSIFIED DRUG; VIRULENCE FACTOR; BACTERIAL DNA; BACTERIAL PROTEIN; PORIN;

ARTICLE; BACILLUS; CRYSTAL STRUCTURE; CYTOTOXICITY; GENE INSERTION; GENOME ANALYSIS; HEPATOPANCREATIC NECROSIS DISEASE; HOMOLOGOUS RECOMBINATION; HORIZONTAL GENE TRANSFER; INTESTINE NECROSIS; INTRACELLULAR KILLING; MARINE SPECIES; NONHUMAN; OPPORTUNISTIC INFECTION; PENAEIDAE; PHOTORHABDUS; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; VIBRIO PARAHAEMOLYTICUS; VIBRIO PARAHAEMOLYTICUS INFECTION; VIRUS PATHOGENESIS; VIRUS VIRULENCE; ANIMAL; BACTERIAL GENE; BACTERIUM CONJUGATION; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; OPEN READING FRAME; PATHOGENICITY; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY; VIRULENCE;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL TOXINS; CONJUGATION, GENETIC; DNA, BACTERIAL; GENES, BACTERIAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PENAEIDAE; PLASMIDS; PORINS; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, NUCLEIC ACID; VIBRIO PARAHAEMOLYTICUS; VIRULENCE;

EID: 84940493708     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1503129112     Document Type: Article

References (43)

1. NACA-FAO (2011) Quarterly Aquatic Animal Disease Report (Asia and Pacific Region), 2011/2, April-June 2011 (NACA, Bangkok).
2. Lightner DV, Redman RM, Pantoja CR, Noble BL, Tran L (2012) Early mortality syndrome affects shrimp in Asia. Global Aquaculture Advocate 15:40.
3. Gomez-Gil B, Soto-Rodríguez S, Lozano R, Betancourt-Lozano M (2014) Draft genome sequence of Vibrio parahaemolyticus Strain M0605, which causes severe mortalities of shrimps in Mexico. Genome Announc 2(2):e00055-14.
4. Nunan L, Lightner D, Pantoja C, Gomez-Jimenez S (2014) Detection of acute hepatopancreatic necrosis disease (AHPND) in Mexico. Dis Aquat Organ 111(1):81-86.
5. FAO Fisheries and Aquaculture (2013) Report of the FAO/MARD Technical Workshop on Early Mortality Syndrome (EMS) or Acute Hepatopancreatic Necrosis Syndrome (AHPNS) of Cultured Shrimp (under TCP/VIE/3304). rep. no. 1053, Hanoi, Viet Nam, 25-27 June
6. Tran L, et al. (2013) Determination of the infectious nature of the agent of acute hepatopancreatic necrosis syndrome affecting penaeid shrimp. Dis Aquat Organ 105(1):45-55.
7. Joshi J, et al. (2014) Variation in Vibrio parahaemolyticus isolates from a single Thai shrimp farm experiencing an outbreak of acute hepatopancreatic necrosis disease (AHPND). Aquaculture 428-429:297-302.
8. De Schryver P, Defoirdt T, Sorgeloos P (2014) Early mortality syndrome outbreaks: A microbial management issue in shrimp farming? PLoS Pathog 10(4):e1003919.
9. Yang YT, et al. (2014) Draft genome sequences of four strains of Vibrio parahaemolyticus, three of which cause early mortality syndrome/acute hepatopancreatic necrosis disease in shrimp in China and Thailand. Genome Announc 2(5):e00816-14.
10. Kondo H, et al. (2014) Draft genome sequences of six strains of Vibrio parahaemolyticus isolated from early mortality syndrome/acute hepatopancreatic necrosis disease shrimp in Thailand. Genome Announc 2(2):e00221-e14.
11. Gomez-Jimenez S, et al. (2014) High-quality draft genomes of two Vibrio parahaemolyticus strains aid in understanding acute hepatopancreatic necrosis disease of cultured shrimps in Mexico. Genome Announc 2(4):e00800-e00814.
12. Han JE, Tang KFJ, Tran LH, Lightner DV (2015) Photorhabdus insect-related (Pir) toxin-like genes in a plasmid of Vibrio parahaemolyticus, the causative agent of acute hepatopancreatic necrosis disease (AHPND) of shrimp. Dis Aquat Organ 113(1):33-40.
13. Zerbino DR, Birney E (2008) Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18(5):821-829.
14. Angiuoli SV, Salzberg SL (2011) Mugsy: Fast multiple alignment of closely related whole genomes. Bioinformatics 27(3):334-342.
15. Aziz RK, et al. (2008) The RAST Server: Rapid Annotations using Subsystems Technology. BMC Genomics 9:75.
16. Nielsen AK, Thorsted P, Thisted T, Wagner EGH, Gerdes K (1991) The rifampicin-inducible genes srnB from F and pnd from R483 are regulated by antisense RNAs and mediate plasmid maintenance by killing of plasmid-free segregants. Mol Microbiol 5(8):1961-1973.
17. Waterfield N, Kamita SG, Hammock BD, ffrench-Constant R (2005) The Photorhabdus Pir toxins are similar to a developmentally regulated insect protein but show no juvenile hormone esterase activity. FEMS Microbiol Lett 245(1):47-52.
18. Soto-Rodriguez SA, Gomez-Gil B, Lozano-Olvera R, Betancourt-Lozano M, Morales-Covarrubias MS (2015) Field and experimental evidence of Vibrio parahaemolyticus as the causative agent of acute hepatopancreatic necrosis disease of cultured shrimp (Litopenaeus vannamei) in Northwestern Mexico. Appl Environ Microbiol 81(5):1689-1699.
19. Soberón M, et al. (2010) Pore formation by Cry toxins. Adv Exp Med Biol 677:127-142.
20. Xu C, Wang BC, Yu Z, Sun M (2014) Structural insights into Bacillus thuringiensis Cry, Cyt and parasporin toxins. Toxins (Basel) 6(9):2732-2770.
21. Jenkins JL, Lee MK, Valaitis AP, Curtiss A, Dean DH (2000) Bivalent sequential binding model of a Bacillus thuringiensis toxin to gypsy moth aminopeptidase N receptor. J Biol Chem 275(19):14423-14431.
22. Crosa JH (1980) A plasmid associated with virulence in the marine fish pathogen Vibrio anguillarum specifies an iron-sequestering system. Nature 284(5756):566-568.
23. Lee CT, et al. (2008) A common virulence plasmid in biotype 2 Vibrio vulnificus and its dissemination aided by a conjugal plasmid. J Bacteriol 190(5):1638-1648.
24. Le Roux F, et al. (2011) Virulence of an emerging pathogenic lineage of Vibrio nigripulchritudo is dependent on two plasmids. Environ Microbiol 13(2):296-306.
25. Vadivelu J, et al. (1996) Hemolysins and plasmid profiles of Vibrio parahaemolyticus. Southeast Asian J Trop Med Public Health 27(1):126-131.
26. Kongrueng J, et al. (2014) Characterization of Vibrio parahaemolyticus causing acute hepatopancreatic necrosis disease in southern Thailand. J Fish Dis, 10.1111/jfd.12308.
27. Soberón M, Gill SS, Bravo A (2009) Signaling versus punching hole: How do Bacillus thuringiensis toxins kill insect midgut cells? Cell Mol Life Sci 66(8):1337-1349.
28. Pigott CR, Ellar DJ (2007) Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol Mol Biol Rev 71(2):255-281.
29. Coplin DL, Rowan RG, Chisholm DA, Whitmoyer RE (1981) Characterization of plasmids in Erwiniastewartii. Appl Environ Microbiol 42(4):599-604.
30. Grochulski P, et al. (1995) Bacillus thuringiensis CryIA(a) insecticidal toxin: crystal structure and channel formation. J Mol Biol 254(3):447-464.
31. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Lab Press, Cold Spring Harbor, NY), 2nd Ed.
32. Shao CP, Hor LI (2000) Metalloprotease is not essential for Vibrio vulnificus virulence in mice. Infect Immun 68(6):3569-3573.
33. Philippe N, Alcaraz JP, Coursange E, Geiselmann J, Schneider D (2004) Improvement of pCVD442, a suicide plasmid for gene allele exchange in bacteria. Plasmid 51(3):246-255.
34. Lightner DV (1996) A Handbook of Shrimp Pathology and Diagnostic Procedures for Diseases of Cultured Penaeid Shrimp (World Aquaculture Society, Baton Rouge, LA).
35. Aranguren FL, Tang KFJ, Lightner DV (2010) Quantification of the bacterial agent of necrotizing hepatopancreatitis (NHP-B) by real-time PCR and comparison of survival and NHP load of two shrimp populations. Aquaculture 307(3-4):187-192.
36. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307-326.
37. Terwilliger TC, Berendzen J (1999) Automated MAD and MIR structure solution. Acta Crystallogr D Biol Crystallogr 55(Pt 4):849-861.
38. Cowtan K (2006) The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr 62(Pt 9):1002-1011.
39. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66(Pt 4):486-501.
40. Vagin AA, et al. (2004) REFMAC5 dictionary: Organisation of prior chemical knowledge and guidelines for its use. Acta Crystallogr D Biol Crystallogr 60(Pt 12 Pt 1): 2284-2295.
41. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: Programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50(Pt 5):760-763.
42. Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J (2009) DNAPlotter: Circular and linear interactive genome visualization. Bioinformatics 25(1):119-120.
43. Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95-98.