Virulence and draft genome sequence overview of multiple strains of the swine pathogen Haemophilus parasuis

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Brockmeier, Susan L ^a   Register, Karen B ^a   Kuehn, Joanna S ^b   Nicholson, Tracy L ^a   Loving, Crystal L ^a   Bayles, Darrell O ^a   Shore, Sarah M ^a   Phillips, Gregory J ^b  

^a NATIONAL ANIMAL DISEASE CENTER   (United States)

^b IOWA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; GENOMIC DNA; PILIN; BACTERIAL ANTIGEN; FIMBRIA PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENOME; BACTERIAL METABOLISM; BACTERIAL OUTER MEMBRANE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CESAREAN SECTION; COLOSTRUM; CONTROLLED STUDY; DRUG TARGETING; GENOME ANALYSIS; GENOTYPE PHENOTYPE CORRELATION; GLASSER DISEASE; HAEMOPHILUS INFECTION; HAEMOPHILUS PARASUIS; MORBIDITY; MORTALITY; NONHUMAN; NUCLEOTIDE SEQUENCE; SEQUENCE ANALYSIS; SEROTYPE; SWINE; ANIMAL; CHROMOSOME MAP; GENETICS; HIGH THROUGHPUT SEQUENCING; IMMUNOLOGY; MICROBIOLOGY; NEWBORN; PATHOGENICITY; PATHOLOGY; PIG; SEROTYPING; SEVERITY OF ILLNESS INDEX; SURVIVAL; SWINE DISEASE; VETERINARY; VIRULENCE;

ADHESINS, BACTERIAL; ANIMALS; ANIMALS, NEWBORN; ANTIGENS, BACTERIAL; CESAREAN SECTION; CHROMOSOME MAPPING; FIMBRIAE PROTEINS; GENOME, BACTERIAL; HAEMOPHILUS INFECTIONS; HAEMOPHILUS PARASUIS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; SEROTYPING; SEVERITY OF ILLNESS INDEX; SURVIVAL ANALYSIS; SWINE; SWINE DISEASES; VIRULENCE;

EID: 84940277372     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0103787     Document Type: Article

References (54)

1. Vahle JL, Haynes JS, Andrews JJ (1995) Experimental reproduction of Haemophilus parasuis infection in swine: clinical, bacteriological, and morphologic findings. J Vet Diagn Invest 7: 476-80.
2. Vahle JL, Haynes JS, Andrews JJ (1997) Interaction of Haemophilus parasuis with nasal and tracheal mucosa following intranasal inoculation of cesarean derived colostrum deprived (CDCD) swine. Can J Vet Res 61: 200-206.
3. Riley MG, Russell EG, Callinan RB (1977) Haemophilus parasuis infection in swine. J Am Vet Med Assoc 171: 649-651.
4. Little TW (1970) Haemophilus infection in pigs. Vet Rec 87: 399-402.
5. Brockmeier SL (2004) Prior infection with Bordetella bronchiseptica increases nasal colonization by Haemophilus parasuis in swine. Vet Microbiol 99: 75-78.
6. Holtkamp D, Rotto H, Garcia R (2007) Swine News Newsletter. 30: 4.
7. Solano-Aguilar GI, Pijoan C, Rapp-Gabrielson V, Collins J, Carvalho LF, et al. (1999) Protective role of maternal antibodies against Haemophilus parasuis infection. Am J Vet Res 60: 81-87.
8. Oliveira S, Batista L, Torremorell M, Pijoan C (2001) Experimental colonization of piglets and gilts with systemic strains of Haemophilus parasuis and Streptococcus suis to prevent disease. Can J Vet Res 65: 161-167.
9. Oliveira S, Galina L, Blanco I, Canals A, Pijoan C (2003) Naturally-farrowed, artificially reared pigs as an alternative model for experimental infection by Haemophilus parasuis. Can J Vet Res 67: 146-150.
10. Blanco I, Galina-Pantoja L, Oliveira S, Pijoan C, Sanchez C, et al. (2004) Comparison between Haemophilus parasuis infection in colostrum-deprived and sow-reared piglets. Vet Microbiol 103: 21-27.
11. Kielstein P, Rapp-Gabrielson VJ (1992) Designation of 15 serovars of Haemophilus parasuis on the basis of immunodiffusion using heat-stable antigen extracts. J Clin Microbiol 30: 862-865.
12. Rapp-Gabrielson VJ, Gabrielson DA (1992) Prevalence of Haemophilus parasuis serovars among isolates from swine. Am J Vet Res 53: 659-664.
13. Olvera A, Cerda-Cuellar M, Nofrarias M, Revilla E, Segales J, et al. (2007) Dynamics of Haemophilus parasuis genotypes in a farm recovered from an outbreak of Glässer's disease. Vet Microbiol 123: 230-237.
14. Miniats OP, Smart NL, Ewert E (1991) Vaccination of gnotobiotic primary specific pathogen-free pigs against Haemophilus parasuis. Can J Vet Res 55: 33-36.
15. Miniats OP, Smart NL, Rosendal S (1991) Cross protection among Haemophilus parasuis strains in immunized gnotobiotic pigs. Can J Vet Res 55: 37-41.
16. Brockmeier SL, Loving CL, Mullins MA, Register KB, Nicholson TL, et al. (2013) Virulence, transmission, and heterologous protection among four isolates of Haemophilus parasuis. Clin Vaccine Immunol 20: 1466-1472.
17. Fu S, Ou J, Zhang M, Xu J, Liu H, et al. (2013) The live attenuated Actinobacillus pleuropneumoniae triple-deletion mutant ΔapxIC ΔapxIIC ΔapxIV-ORF1 strain, SLW05, immunizes pigs against lethal challenge with Haemophilus parasuis. Clin Vaccine Immunol 20: 134-139.
18. Cerda-Cuellar M, Aragon V (2008) Serum-resistance in Haemophilus parasuis is associated with systemic disease in swine. Vet J 175: 384-389.
19. Olvera A, Ballester M, Nofrarias M, Sibila M, Aragon V (2009) Differences in phagocytosis susceptibility in Haemophilus parasuis strains. Vet Res 40: 24-35.
20. Pina S, Olvera A, Barcelo A, Bensaid A (2009) Trimeric autotransporters of Haemophilus parasuis: generation of an extensive passenger domain repertoire specific for pathogenic strains. J Bacteriol 191: 576-587.
21. Costa-Hurtado M, Ballester M, Galofre-Mila N, Darji A, Aragon V (2012) VtaA8 and VtaA9 from Haemophilus parasuis delay phagocytosis by alveolar macrophages. Vet Res 43: 57-66.
22. Zhang B, Feng S, Xu C, Zhou S, He Y, et al. (2012) Serum resistance in Haemophilus parasuis SC096 strain requires outer membrane protein P2 expression. FEMS Microbiol Lett 326: 109-115.
23. Zhang B, He Y, Xu C, Xu L, Feng S, et al. (2012) Cytolethal distending toxin (CDT) of the Haemophilus parasuis SC096 strain contributes to serum resistance and adherence to and invasion of PK-15 and PUVEC cells. Vet Microbiol 157: 237-242.
24. Yue M, Yang F, Yang J, Bei W, Cai X, et al. (2009) Complete genome sequence of Haemophilus parasuis SH0165. J Bacteriol 191: 1359-1360.
25. Blackall PJ, Turni C (2013) Understanding the virulence of Haemophilus parasuis. Vet J 198:549-550.
26. Amano H, Shibata M, Kajio N, Morozumi T (1994) Pathologic observations of pigs intranasally inoculated with serovar 1, 4 and 5 of Haemophilus parasuis using immunoperoxidase method. J Vet Med Sci 56: 639-644.
27. Amano H, Shibata M, Kajio N, Morozumi T (1996) Pathogenicity of Haemophilus parasuis serovars 4 and 5 in contact-exposed pigs. J Vet Med Sci 58: 559-561.
28. Frandoloso R, Martínez S, Rodríguez-Ferri EF, García-Iglesias MJ, Pérez-Martínez C, et al. (2011) Development and characterization of protective Haemophilus parasuis subunit vaccines based on native proteins with affinity to porcine transferrin and comparison with other subunit and commercial vaccines. Clin Vaccine Immunol 18: 50-58.
29. Olvera A, Pina S, Pérez-Simó M, Aragón V, Segalés J, et al. (2011) Immunogenicity and protection against Haemophilus parasuis infection after vaccination with recombinant virulence associated trimeric autotransporters (VtaA). Vaccine 29: 2797-2802.
30. Rapp-Gabrielson VJ, Gabrielson DA, Schamber GJ (1992) Comparative virulence of Haemophilus parasuis serovars 1 to 7 in guinea pigs. Am J Vet Res 53: 987-994.
31. Xu Z, Yue M, Zhou R, Jin Q, Fan Y, et al. (2011) Genomic characterization of Haemophilus parasuis SH0165, a highly virulent strain of serovar 5 prevalent in China. PLoS One 6: e19631.
32. Mullins MA, Register KB, Bayles DO, Dyer DW, Kuehn JS, et al. (2011) Genome sequence of Haemophilus parasuis strain 29755. Stand Genomics 5: 61-68.
33. Kielstein P, Rosner H, Muller W (1991) Typing of heat-stable soluble Haemophilus parasuis antigen by means of agar gel precipitation and the dotblot procedure. J Vet Med B 38: 315-320.
34. Mullins MA, Register KB, Brunelle BW, Aragon V, Galofre-Mila N, et al. (2013) A curated public database for multilocus sequence typing (MLST) and analysis of Haemophilus parasuis based on an optimized typing scheme. Vet Microbiol 162: 899-906.
35. Quail MA, Kozarewa I, Smith F, Scally A, Stephens PJ, et al. (2008) A large genome center's improvements to the Illumina sequencing system. Nat Methods 5: 1005-1010.
36. Kuehn JS, Register KB, Phillips GJ (2013) Draft Genome Sequences for 10 Isolates of the Swine Pathogen Haemophilus parasuis. Genome Announc1: e00739-13. doi: 10.1128/genomeA.00739-13.
37. Shao Y, He X, Harrison EM, Tai C, Ou HY, et al. (2010) mGenomeSubtractor: a web-based tool for parallel in silico subtractive hybridization analysis of multiple bacterial genomes. Nucleic Acids Res 38: W194-200.
38. Chevreux B, Wetter T, Suhai S (1999) Genome sequence assembly using trace signals and additional sequence information. Computer Science and Biology: Proceedings of the German Conference on Bioinformatics (GCB) 99, pp. 45-56.
39. Darling AC, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14: 1394-1403.
40. Darling AE, Mau B, Perna NT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5: e11147.
41. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
42. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
43. McWilliam H, Valentin F, Goujon M, Li W, Narayanasamy M, et al. (2009) Web services at the European Bioinformatics Institute-2009. Nucleic Acids Res 37: W6-10.
44. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, et al. (2008) The RAST Server: Rapid Annotations using Subsystems Technology. BMC Genomics 9.
45. Stothard P, Wishart DS (2005) Circular genome visualization and exploration using CGView. Bioinformatics 21: 537-539.
46. Eddy SR (2011) Accelerated Profile HMM Searches. PLoS Comput Biol 7: e1002195.
47. Yoon SH, Park YK, Lee S, Choi D, Oh TK, et al (2007) Towards pathogenomics: a web-based resource for pathogenicity islands. Nucleic Acids Research 35: D395-D400.
48. Apicella MA (2008) Bacterial Pathogenesis: Methods in Molecular Biology, volume 431, pp 3-13. Isolation and Characterization of Lipopolysaccharides. Available: http://link.springer.com/protocol/10.1007/978-1-60327-032-8-1
49. Costa-Hurtado M, Olvera A, Martinez-Moliner V, Galorfre-Mila N, Martinez P, et al. (2013) Changes in macrophage phenotype after infection of pigs with Haemophilus parasuis strains with different levels of virulence. Infect Immun 81: 2327-2333.
50. Howell KJ, Weinert LS, Luan SL, Peters SE, Chaudhuri RR, et al. (2013) Gene content and diversity of the loci encoding biosynthesis of capsular polysaccharides of the 15 serovar reference strains of Haemophilus parasuis. J Bacteriol 195: 4264-4273.
51. Li Y, Kwok AH, Jiang J, Zou Y, Zheng F, et al. (2013) Complete genome analysis of a Haemophilus parasuis serovar 12 strain from China. PLoS One 8: e68350.
52. Yuan F, Fu S, Hu J, Li J, Chang H, et al. (2012) Evaluation of recombinant proteins of Haemophilus parasuis strain SH0165 as vaccine candidates in a mouse model. Res Vet Sci 93: 51-56.
53. Zhou M, Guo Y, Zhao J, Hu Q, Hu Y, et al. (2009) Identification and characterization of novel immunogenic outer membrane proteins of Haemophilus parasuis serovar 5. Vaccine 27: 5271-5277.
54. Daines DA, Jarisch J, Smith AL (2004) Identification and characterization of a nontypeable Haemophilus influenzae putative toxin-antitoxin locus. BMC Microbiology 4: 30.