Identification of putative adhesins of Actinobacillus suis and their homologues in other members of the family Pasteurellaceae

BMC Research Notes

Janet I. MacInnes¹  Adina R. Bujold¹ 

[1] Department of Pathobiology, Ontario Veterinary College, University of Guelph, Ontario N1G 2W1, Canada

关键词: Bioinformatics;    Adhesins;    Pasteurellaceae;    Actinobacillus suis;   

Others  :  1232650
DOI  :  10.1186/s13104-015-1659-x

 received in 2015-07-17, accepted in 2015-11-02,  发布年份 2015

【 摘 要 】

Background

Actinobacillus suis disease has been reported in a wide range of vertebrate species, but is most commonly found in swine. A. suis is a commensal of the tonsils of the soft palate of swine, but in the presence of unknown stimuli it can invade the bloodstream, causing septicaemia and sequelae such as meningitis, arthritis, and death. It is genotypically and phenotypically similar to A. pleuropneumoniae, the causative agent of pleuropneumonia, and to other members of the family Pasteurellaceae that colonise tonsils. At present, very little is known about the genes involved in attachment, colonisation, and invasion by A. suis (or related members of the tonsil microbiota).

Results

Bioinformatic analyses of the A. suis H91-0380 genome were done using BASys and blastx in GenBank. Forty-seven putative adhesin-associated genes predicted to encode 24 putative adhesins were discovered. Among these are 6 autotransporters, 25 fimbriae-associated genes (encoding 3 adhesins), 12 outer membrane proteins, and 4 additional genes (encoding 3 adhesins). With the exception of 2 autotransporter-encoding genes (aidA and ycgV), both with described roles in virulence in other species, all of the putative adhesin-associated genes had homologues in A. pleuropneumoniae. However, the majority of the closest homologues of the A. suis adhesins are found in A. ureae and A. capsulatus—species not known to infect swine, but both of which can cause systemic infections.

Conclusions

A. suis and A. pleuropneumoniae share many of the same putative adhesins, suggesting that the different diseases, tissue tropism, and host range of these pathogens are due to subtle genetic differences, or perhaps differential expression of virulence factors during infection. However, many of the putative adhesins of A. suis share even greater homology with those of other pathogens within the family Pasteurellaceae. Similar to A. suis, these pathogens (A. capsulatus and A. ureae) cause systemic infections and it is tempting to speculate that they employ similar strategies to invade the host, but more work is needed before that assertion can be made. This work begins to examine adhesin-associated factors that allow some members of the family Pasteurellaceae to invade the bloodstream while others cause a more localised infection.

【 授权许可】

   
2015 Bujold and Maclnnes.

【 参考文献 】

• [1]Kernaghan S, Bujold AR, MacInnes JI: The microbiome of the soft palate of swine. Anim Health Res Rev 2012, 13:110-120.
• [2]MacInnes JI, Desrosiers R: Agents of the “suis-ide diseases” of swine: actinobacillus suis, Haemophilus parasuis, and Streptococcus suis. Can J Vet Res 1999, 63:83-89.
• [3]Bosse JT, Janson H, Sheehan BJ, Beddek AJ, Rycroft AN, Kroll JS, Langford PR: Actinobacillus pleuropneumoniae: pathobiology and pathogenesis of infection. Microb Infect 2002, 4:225-235.
• [4]MacInnes JI: Actinobacillus. In Pathogenesis of bacterial infections in animals. 4th edition. Edited by Gyles CL, Prescott JF, Songer G, Thoen CO. Wiley-Blackwell, Ames; 2010:363-386.
• [5]Jeannotte ME, Slavic D, Frey J, Kuhnert P, MacInnes JI: Analysis of non-porcine isolates of Actinobacillus suis. Vet Microbiol 2002, 85:83-93.
• [6]MacInnes JI, Mackinnon J, Bujold AR, Ziebell K, Kropinski AM, Nash JH: Complete genome sequence of Actinobacillus suis H91-0380, a virulent serotype O2 strain. J Bacteriol 2012, 194:6686-6687.
• [7]Ofek I, Doyle RJ: Bacterial adhesion to cells and tissues. Chapman & Hall, New York; 1994.
• [8]Soto GE, Hultgren SJ: Bacterial adhesins: common themes and variations in architecture and assembly. J Bacteriol 1999, 181:1059-1071.
• [9]Klemm P, Schembri MA: Bacterial adhesins: function and structure. Int J Med Microbiol 2000, 290:27-35.
• [10]Linke D, Goldman A: Bacterial adhesion: chemistry, biology and physics. Springer, Dordrecht; 2011.
• [11]Cotter SE, Surana NK, St Geme JW 3rd: Trimeric autotransporters: a distinct subfamily of autotransporter proteins. Trends Microbiol 2005, 13:199-205.
• [12]Surana NK, Cutter D, Barenkamp SJ, St Geme JW 3rd: The Haemophilus influenzae Hia autotransporter contains an unusually short trimeric translocator domain. J Biol Chem 2004, 279:14679-14685.
• [13]Hoiczyk E, Roggenkamp A, Reichenbecher M, Lupas A, Heesemann J: Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. EMBO J 2000, 19:5989-5999.
• [14]Roggenkamp A, Ackermann N, Jacobi CA, Truelzsch K, Hoffmann H, Heesemann J: Molecular analysis of transport and oligomerization of the Yersinia enterocolitica adhesin YadA. J Bacteriol 2003, 185:3735-3744.
• [15]Watson AA, Alm RA, Mattick JS: Identification of a gene, pilF, required for type 4 fimbrial biogenesis and twitching motility in Pseudomonas aeruginosa. Gene 1996, 180:49-56.
• [16]Carbonnelle E, Helaine S, Prouvensier L, Nassif X, Pelicic V: Type IV pilus biogenesis in Neisseria meningitidis: PilW is involved in a step occurring after pilus assembly, essential for fibre stability and function. Mol Microbiol 2005, 55:54-64.
• [17]Cerveny L, Straskova A, Dankova V, Hartlova A, Ceckova M, Staud F, Stulik J: Tetratricopeptide repeat motifs in the world of bacterial pathogens: role in virulence mechanisms. Infect Immun 2013, 81:629-635.
• [18]Planet PJ, Kachlany SC, Fine DH, DeSalle R, Figurski DH: The widespread colonization island of Actinobacillus actinomycetemcomitans. Nat Genet 2003, 34:193-198.
• [19]Spinola SM, Fortney KR, Katz BP, Latimer JL, Mock JR, Vakevainen M, Hansen EJ: Haemophilus ducreyi requires an intact flp gene cluster for virulence in humans. Infect Immun 2003, 71:7178-7182.
• [20]Fuller TE, Kennedy MJ, Lowery DE: Identification of Pasteurella multocida virulence genes in a septicemic mouse model using signature-tagged mutagenesis. Microb Pathog 2000, 29:25-38.
• [21]Tomich M, Fine DH, Figurski DH: The TadV protein of Actinobacillus actinomycetemcomitans is a novel aspartic acid prepilin peptidase required for maturation of the Flp1 pilin and TadE and TadF pseudopilins. J Bacteriol 2006, 188:6899-6914.
• [22]Tomich M, Planet PJ, Figurski DH: The tad locus: postcards from the widespread colonization island. Nat Rev Microbiol 2007, 5:363-375.
• [23]Li T, Xu Z, Zhang T, Li L, Chen H, Zhou R: The genetic analysis of the flp locus of Actinobacillus pleuropneumoniae. Arch Microbiol 2012, 194:167-176.
• [24]Carruthers MD, Tracy EN, Dickson AC, Ganser KB, Munson RS Jr, Bakaletz LO: Biological roles of nontypeable Haemophilus influenzae type IV pilus proteins encoded by the pil and com operons. J Bacteriol 2012, 194:1927-1933.
• [25]Bakaletz LO, Baker BD, Jurcisek JA, Harrison A, Novotny LA, Bookwalter JE, Mungur R, Munson RS Jr: Demonstration of Type IV pilus expression and a twitching phenotype by Haemophilus influenzae. Infect Immun 2005, 73:1635-1643.
• [26]Jurcisek JA, Bakaletz LO: Biofilms formed by nontypeable Haemophilus influenzae in vivo contain both double-stranded DNA and type IV pilin protein. J Bacteriol 2007, 189:3868-3875.
• [27]Jurcisek JA, Bookwalter JE, Baker BD, Fernandez S, Novotny LA, Munson RS Jr, Bakaletz LO: The PilA protein of non-typeable Haemophilus influenzae plays a role in biofilm formation, adherence to epithelial cells and colonization of the mammalian upper respiratory tract. Mol Microbiol 2007, 65:1288-1299.
• [28]Hunt ML, Adler B, Townsend KM: The molecular biology of Pasteurella multocida. Vet Microbiol 2000, 72:3-25.
• [29]Boekema BK, Stockhofe-Zurwieden N, Smith HE, Kamp EM, van Putten JP, Verheijden JH: Adherence of Actinobacillus pleuropneumoniae to primary cultures of porcine lung epithelial cells. Vet Microbiol 2003, 93:133-144.
• [30]Boekema BK, Van Putten JP, Stockhofe-Zurwieden N, Smith HE: Host cell contact-induced transcription of the type IV fimbria gene cluster of Actinobacillus pleuropneumoniae. Infect Immun 2004, 72:691-700.
• [31]Zhou Y, Li L, Chen Z, Yuan H, Chen H, Zhou R: Adhesion protein ApfA of Actinobacillus pleuropneumoniae is required for pathogenesis and is a potential target for vaccine development. Clin Vaccine Immunol 2013, 20:287-294.
• [32]Wall D, Kaiser D: Type IV pili and cell motility. Mol Microbiol 1999, 32:1-10.
• [33]Craig L, Pique ME, Tainer JA: Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2004, 2:363-378.
• [34]Hansen JK, Forest KT: Type IV pilin structures: insights on shared architecture, fiber assembly, receptor binding and type II secretion. J Mol Microbiol Biotechnol 2006, 11:192-207.
• [35]Galdiero S, Falanga A, Cantisani M, Tarallo R, Della Pepa ME, D’Oriano V, Galdiero M: Microbe-host interactions: Structure and role of Gram-negative bacterial porins. Curr Protein Peptide Sci 2012, 13:843-854.
• [36]Ojha S, Lacouture S, Gottschalk M, MacInnes JI: Characterization of colonization-deficient mutants of Actinobacillus suis. Vet Microbiol 2010, 140:122-130.
• [37]Ojha S, Sirois M, Macinnes JI: Identification of Actinobacillus suis genes essential for the colonization of the upper respiratory tract of swine. Infect Immun 2005, 73:7032-7039.
• [38]Novotny LA, Jurcisek JA, Pichichero ME, Bakaletz LO: Epitope mapping of the outer membrane protein P5-homologous fimbrin adhesin of nontypeable Haemophilus influenzae. Infect Immun 2000, 68:2119-2128.
• [39]Hill DJ, Toleman MA, Evans DJ, Villullas S, Van Alphen L, Virji M: The variable P5 proteins of typeable and non-typeable Haemophilus influenzae target human CEACAM1. Mol Microbiol 2001, 39:850-862.
• [40]Regelink AG, Dahan D, Moller LV, Coulton JW, Eijk P, Van Ulsen P, Dankert J, Van Alphen L: Variation in the composition and pore function of major outer membrane pore protein P2 of Haemophilus influenzae from cystic fibrosis patients. Antimicrob Agents Chemother 1999, 43:226-232.
• [41]Andersen C, Maier E, Kemmer G, Blass J, Hilpert AK, Benz R, Reidl J: Porin OmpP2 of Haemophilus influenzae shows specificity for nicotinamide-derived nucleotide substrates. J Biol Chem 2003, 278:24269-24276.
• [42]Reddy MS, Bernstein JM, Murphy TF, Faden HS: Binding between outer membrane proteins of nontypeable Haemophilus influenzae and human nasopharyngeal mucin. Infect Immun 1996, 64:1477-1479.
• [43]Locht C, Antoine R, Jacob-Dubuisson F: Bordetella pertussis, molecular pathogenesis under multiple aspects. Curr Opin Microbiol 2001, 4:82-89.
• [44]Nicholson TL, Brockmeier SL, Loving CL: Contribution of Bordetella bronchiseptica filamentous hemagglutinin and pertactin to respiratory disease in swine. Infect Immun 2009, 77:2136-2146.
• [45]Sandal I, Shao JQ, Annadata S, Apicella MA, Boye M, Jensen TK, Saunders GK, Inzana TJ: Histophilus somni biofilm formation in cardiopulmonary tissue of the bovine host following respiratory challenge. Microbes Infect 2009, 11:254-263.
• [46]Darvish Alipour Astaneh S, Rasooli I, Mousavi Gargari SL: The role of filamentous hemagglutinin adhesin in adherence and biofilm formation in Acinetobacter baumannii ATCC19606. Microb Pathog 2014, 74C:42-49.
• [47]Verma S, Sharma M, Katoch S, Verma L, Kumar S, Dogra V, Chahota R, Dhar P, Singh G: Profiling of virulence associated genes of Pasteurella multocida isolated from cattle. Vet Res Commun 2013, 37:83-89.
• [48]Brentjens RJ, Ketterer M, Apicella MA, Spinola SM: Fine tangled pili expressed by Haemophilus ducreyi are a novel class of pili. J Bacteriol 1996, 178:808-816.
• [49]Haikarainen T, Papageorgiou AC: Dps-like proteins: structural and functional insights into a versatile protein family. Cell Mol Life Sci 2010, 67:341-351.
• [50]Huergo LF, Rahman H, Ibrahimovic A, Day CJ, Korolik V: Campylobacter jejuni Dps protein binds DNA in the presence of iron or hydrogen peroxide. J Bacteriol 2013, 195:1970-1978.
• [51]Theoret JR, Cooper KK, Glock RD, Joens LA: A Campylobacter jejuni Dps homolog has a role in intracellular survival and in the development of campylobacterosis in neonate piglets. Foodborne Pathog Dis 2011, 8:1263-1268.
• [52]Theoret JR, Cooper KK, Zekarias B, Roland KL, Law BF, Curtiss R 3rd, Joens LA: The Campylobacter jejuni Dps homologue is important for in vitro biofilm formation and cecal colonization of poultry and may serve as a protective antigen for vaccination. Clin Vaccine Immunol 2012, 19:1426-1431.
• [53]Pang B, Hong W, Kock ND, Swords WE: Dps promotes survival of nontypeable Haemophilus influenzae in biofilm communities in vitro and resistance to clearance in vivo. Front Cell Infect Microbiol 2012, 2:58.
• [54]Mullen LM, Nair SP, Ward JM, Rycroft AN, Williams RJ, Henderson B: Comparative functional genomic analysis of Pasteurellaceae adhesins using phage display. Vet Microbiol 2007, 122:123-134.
• [55]Mullen LM, Bosse JT, Nair SP, Ward JM, Rycroft AN, Robertson G, Langford PR, Henderson B: Pasteurellaceae ComE1 proteins combine the properties of fibronectin adhesins and DNA binding competence proteins. PLoS One 2008, 3:e3991.
• [56]Mullen LM, Nair SP, Ward JM, Rycroft AN, Williams RJ, Robertson G, Mordan NJ, Henderson B: Novel adhesin from Pasteurella multocida that binds to the integrin-binding fibronectin FnIII9-10 repeats. Infect Immun 2008, 76:1093-1104.
• [57]Calcutt MJ, Foecking MF, Mhlanga-Mutangadura T, Reilly TJ. Genome sequence of Actinobacillus suis type strain ATCC 33415T. Genome Announc 2014; 2.
• [58]Van Domselaar GH, Stothard P, Shrivastava S, Cruz JA, Guo A, Dong X, Lu P, Szafron D, Greiner R, Wishart DS: BASys: a web server for automated bacterial genome annotation. Nucleic Acids Res 2005, 33:W455-W459.
• [59]Thornton B, Basu C: Real-time PCR (qPCR) primer design using free online software. Biochem Mol Biol Educ 2011, 39:145-154.
• [60]Darling AE, Mau B, Perna NT: progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010, 5:e11147.
• [61]Van Ostaaijen J, Frey J, Rosendal S, MacInnes JI: Actinobacillus suis strains isolated from healthy and diseased swine are clonal and carry apxICABDvar. suis and apxIICAvar. suis toxin genes. J Clin Microbiol 1997, 35:1131-1137.
• [62]Slavic D, DeLay J, Hayes MA, MacInnes JI: Comparative pathogenicity of different Actinobacillus suis O/K serotypes. Can J Vet Res 2000, 64:81-87.
• [63]Foote SJ, Bosse JT, Bouevitch AB, Langford PR, Young NM, Nash JH: The complete genome sequence of Actinobacillus pleuropneumoniae L20 (serotype 5b). J Bacteriol 2008, 190:1495-1496.