Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-19T09:34:39.567Z Has data issue: false hasContentIssue false

Actinobacillus pleuropneumoniae biofilms: Role in pathogenicity and potential impact for vaccination development

Published online by Cambridge University Press:  07 November 2017

Skander Hathroubi
Affiliation:
Department of Microbiology and Environmental Toxicology, University of California, Santa Cruz, CA, USA
Abraham Loera-Muro
Affiliation:
CONACYT-CIBNOR, Centro de Investigaciones Biológicas del Noroeste, SC. Instituto Politécnico Nacional 195, Playa Palo de Santa Rita Sur, La Paz, BCS, México
Alma L. Guerrero-Barrera
Affiliation:
Centro de Ciencias Básicas, Universidad Autónoma de Aguascalientes, Av. Universidad 940, Colonia Ciudad Universitaria, Aguascalientes, AGS, México
Yannick D. N. Tremblay
Affiliation:
Laboratoire Pathogenèse des Bactéries Anaérobies, Département de Microbiologie, Institut Pasteur, 25 rue du Dr Roux, 75015, Paris, France
Mario Jacques*
Affiliation:
Groupe de recherche sur la maladies infectieuses en production animale, Faculté de Médecine Vétérinaire, Université de Montréal, St-Hyacinthe, QC, Canada
*
*Corresponding author. E-mail: mario.jacques@umontreal.ca

Abstract

Actinobacillus pleuropneumoniae is a Gram-negative bacterium that belongs to the family Pasteurellaceae. It is the causative agent of porcine pleuropneumonia, a highly contagious respiratory disease that is responsible for major economic losses in the global pork industry. The disease may present itself as a chronic or an acute infection characterized by severe pathology, including hemorrhage, fibrinous and necrotic lung lesions, and, in the worst cases, rapid death. A. pleuropneumoniae is transmitted via aerosol route, direct contact with infected pigs, and by the farm environment. Many virulence factors associated with this bacterium are well characterized. However, much less is known about the role of biofilm, a sessile mode of growth that may have a critical impact on A. pleuropneumoniae pathogenicity. Here we review the current knowledge on A. pleuropneumoniae biofilm, factors associated with biofilm formation and dispersion, and the impact of biofilm on the pathogenesis A. pleuropneumoniae. We also provide an overview of current vaccination strategies against A. pleuropneumoniae and consider the possible role of biofilms vaccines for controlling the disease.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Both authors contributed equally to this work

References

Archambault, M, Harel, J, Gouré, J, Tremblay, YD and Jacques, M (2012). Antimicrobial susceptibilities and resistance genes of Canadian isolates of Actinobacillus pleuropneumoniae. Microbial Drug Resistance 18: 198206.Google Scholar
Auger, E, Deslandes, V, Ramjeet, M, Contreras, I, Nash, J, Harel, J, Gottschalk, M, Olivier, M and Jacques, M (2009). Host-pathogen interactions of Actinobacillus pleuropneumoniae with porcine lung and tracheal epithelial cells. Infection and Immunity 77: 14261441.Google Scholar
Badmasti, F, Ajdary, S, Bouzari, S, Fooladi, AA, Shahcheraghi, F and Siadat, SD (2015). Immunological evaluation of OMV(PagL)+Bap(1-487aa) and AbOmpA(8-346aa)+Bap(1-487aa) as vaccine candidates against Acinetobacter baumannii sepsis infection. Molecular Immunology 67: 552558. doi: 10.1016/j.molimm.2015.07.031.Google Scholar
Baroch, JA, Gagnon, CA, Lacouture, S and Gottschalk, M (2015). Exposure of feral swine (Sus scrofa) in the United States to selected pathogens. Canadian Journal of Veterinary Research 79: 7478.Google Scholar
Bello-Ortí, B, Deslandes, V, Tremblay, YD, Labrie, J, Howell, KJ, Tucker, AW, Maskell, DJ, Aragon, V and Jacques, M (2014) Biofilm formation by virulent and non-virulent strains of Haemophilus parasuis. Veterinary Research 45: 104.Google Scholar
Bjarnsholt, T., Alhede, M., Eickhardt-Sorensen, S.R., Moser, C., Kühl, M., Jensen, P.O. and Hoiby, N. (2013) The in vivo biofilm. Trends in Microbiology 21: 466474.Google Scholar
Bossé, JT, Sinha, S, Li, MS, O'Dwyer, CA, Nash, JH, Rycroft, AN, Kroll, JS and Langford, PR (2010). Regulation of pga operon expression and biofilm formation in Actinobacillus pleuropneumoniae by σE and H-NS. Journal of Bacteriology 192: 24142423. doi: 10.1128/JB.01513-09.Google Scholar
Bossé, JT, Li, Y, Angen, Ø, Weinert, LA, Chaudhuri, RR, Holden, MT, Williamson, SM, Maskell, DJ, Tucker, AW, Wren, BW, Rycroft, AN and Langford, PR (2014). Multiplex PCR assay for unequivocal differentiation of Actinobacillus pleuropneumoniae serovars 1 to 3, 5 to 8, 10, and 12. Journal of Clinical Microbiology 52: 23802385. doi: 10.1128/JCM.00685-14.Google Scholar
Bossé, JT, Li, Y, Atherton, TG, Walker, S, Williamson, SM, Rogers, J, Chaudhuri, RR, Weinert, LA, Holden, MT, Maskell, DJ, Tucker, AW, Wren, BW, Rycroft, AN, Langford, PR and BRaDP1T consortium (2015). Characterisation of a mobilisable plasmid conferring florfenicol and chloramphenicol resistance in Actinobacillus pleuropneumoniae. Veterinary Microbiology 178: 279282. doi: 10.1016/j.vetmic.2015.05.020.Google Scholar
Bossé, JT, Li, Y, Sárközi, R, Gottschalk, M, Angen, Ø, Nedbalcova, K, Rycroft, AN, Fodor, L and Langford, PR (2017). A unique capsule locus in the newly designated Actinobacillus pleuropneumoniae serovar 16 and development of a diagnostic PCR. Journal of Clinical Microbiology 55: 902907. doi: 10.1128/JCM.02166-16.Google Scholar
Boukahil, I and Czuprynski, CJ (2015). Characterization of Mannheimia haemolytica biofilm formation in vitro. Veterinary Microbiology 175: 114122.Google Scholar
Briandet, R, Fechner, L, Naïtali, M and Dreanno, C (2012). Biofilms, quand les microbes s'organisent. Editions Quae, France.Google Scholar
Buettner, FF, Maas, A and Gerlach, GF (2008). An Actinobacillus pleuropneumoniae arcA deletion mutant is attenuated and deficient in biofilm formation. Veterinary Microbioliology 127: 106115.Google Scholar
Buettner, F, Konze, S, Maas, A and Gerlach, G (2011). Proteomic and immunoproteomic characterization of a DIVA subunit vaccine against Actinobacillus pleuropneumoniae. Proteome Science 9: 123.Google Scholar
Chen, Z, Chien, MS, Chang, NY, Chen, TH, Wu, CM, Huang, C, Lee, WC and Hsuan, SL (2011). Mechanisms underlying Actinobacillus pleuropneumoniae exotoxin ApxI induced expression of IL-1b, IL-8 and TNF-a in porcine alveolar macrophages. Veterinary Research 42: 210.Google Scholar
Chiers, K, De Waele, T, Pasmans, F, Ducatelle, R and Haesebrouck, F (2010). Virulence factors of Actinobacillus pleuropneumoniae involved in colonization, persistence and induction of lesions in its porcine host. Veterinary Research 41: 65.Google Scholar
Clifford, JC, Rapicavoli, JN and Roper, MC (2013). A rhamnose-rich O-antigen mediates adhesion, virulence and host colonization for the xylem-limited phytopathogen, Xylella fastidiosa. Molecular Plant-Microbe Interactions 26: 676685. doi: 10.1094/MPMI-12-12-0283-R.Google Scholar
Coenye, T and Nelis, HJ (2010). In vitro and in vivo model systems to study microbial biofilm formation. Journal of Microbiology Methods 83: 89105.Google Scholar
Coffey, BM and Anderson, GG (2014). Biofilm formation in the 96-well microtiter plate. Methods Molecular Biology 1149: 631641.Google Scholar
Dalai, B, Zhou, R, Wan, Y, Kang, M, Li, L, Li, T, Zhang, S and Chen, H (2009). Histone-like protein H-NS regulates biofilm formation and virulence of Actinobacillus pleuropneumoniae. Microbial Pathogenesis 46: 128134.Google Scholar
Dayao, D, Gibson, JS, Blackall, PJ and Turni, C (2016). Antimicrobial resistance genes in Actinobacillus pleuropneumoniae, Haemophilus parasuis and Pasteurella multocida isolated from Australian pigs. Australian Veterinary Journal 94: 227231. doi: 10.1111/avj.12458.Google Scholar
Dayao, DA, Gibson, JS, Blackall, PJ and Turni, C (2014). Antimicrobial resistance in bacteria associated with porcine respiratory disease in Australia. Veterinary Microbiology 171: 232235. doi: 10.1016/j.vetmic.2014.03.014.Google Scholar
De Brucker, K, Tan, Y, Vints, K, De Cremer, K, Braem, A, Verstraeten, N, Michiels, J, Vleugels, J, Cammue, BP and Thevissen, K (2015). Fungal beta-1,3-glucan increases ofloxacin tolerance of Escherichia coli in a polymicrobial E. coli/Candida albicans biofilm. Antimicrobial Agents and Chemotherapy 59: 30523058.Google Scholar
de Gouw, D, Serra, DO, de Jonge, MI, Hermans, PW, Wessels, HJ, Zomer, A, Yantorno, OM, Diavatopoulos, DA and Mooi, FR (2014). The vaccine potential of Bordetella pertussis biofilm-derived membrane proteins. Emerging Microbes & Infections 3: e58. doi:10.1038/emi.2014.58.Google Scholar
Del Pozo-Sacristán, R, Michiels, A, Martens, M, Haesebrouck, F and Maes, D (2014). Efficacy of vaccination against Actinobacillus pleuropneumoniae in two Belgian farrow-to-finish pig herds with a history of chronic pleurisy. Veterinary Record 174: 302.Google Scholar
Ethapa, T, Leuzzi, R, Ng, YK, Baban, ST, Adamo, R, Kuehne, SA, Scarselli, M, Minton, NP, Serruto, D and Unnikrishnan, M (2013). Multiple factors modulate biofilm formation by the anaerobic pathogen Clostridium difficile. Journal of Bacteriology 195: 545555.Google Scholar
Fattahian, Y, Rasooli, I, Gargari, SLM, Rahbar, MR, Astaneh, SDA and Amani, J (2011). Protection against Acinetobacter baumannii infection via its functional deprivation of biofilm associated protein (Bap). Microbial Pathogenesis 51: 402406.Google Scholar
Flores-Mireles, AL, Pinkner, JS, Caparon, MG and Hultgren, SJ (2014). Ebpa vaccine antibodies block binding of Enterococcus faecalis to fibrinogen to prevent catheter-associated bladder infection in mice. Science Translational Medicine 6: 254ra127. doi: 10.1126/scitranslmed.3009384.Google Scholar
Flores-Valdez, MA (2016). Vaccines directed against microorganisms or their products present during biofilm lifestyle: can we make a translation as a broad biological model to tuberculosis? Frontiers in Microbiology 7: 14.Google Scholar
Frey, J (1995). Virulence in Actinobacillus pleuropneumoniae and RTX toxins. Trends in Microbiology 3: 257261.Google Scholar
Gil, C, Solano, C, Burgui, S, Latasa, C, García, B, Toledo-Arana, A, Lasa, I and Valle, J (2014). Biofilm matrix exoproteins induce a protective immune response against Staphylococcus aureus biofilm infection. Infection and Immunity 82: 10171029.Google Scholar
Goeres, D, Hamilton, M, Beck, N, Buckingham-Meyer, K, Hilyard, J, Loetterle, L, Lorenz, L, Walker, D and Stewart, P (2009). A method for growing a biofilm under low shear at the air-liquid interface using the drip flow biofilm reactor. Nature Protocols 4: 783788.Google Scholar
Gogoi-Tiwari, J, Williams, V, Waryah, CB, Eto, KY, Tau, M, Costantino, P, Tiwari, HK and Mukkur, T (2015). Comparative studies of the immunogenicity and protective potential of biofilm vs planktonic Staphylococcus aureus vaccine against bovine mastitis using non-invasive mouse mastitis as a model system. Biofouling 31: 543554. doi: 10.1080/08927014.2015.1074681.Google Scholar
Gogoi-Tiwari, J, Williams, V, Waryah, CB, Mathavan, S, Tiwari, HK, Costantino, P and Mukkur, T (2016). Intramammary immunization of pregnant mice with staphylococcal protein a reduces the post-challenge mammary gland bacterial load but not pathology. PLoS ONE 11: e0148383. doi: 10.1371/journal.pone.0148383.Google Scholar
Gómez-Laguna, J, Islas, A, Muñoz, D, Ruiz, A, Villamil, A, Carrasco, L and Quezada, M (2014). Infection dynamics and acute phase response of an Actinobacillus pleuropneumoniae field isolate of moderate virulence in pigs. Veterinary Microbiology 173: 332339. doi: 10.1016/j.vetmic.2014.08.015.Google Scholar
Gottschalk, M (2015). The challenge of detecting herds sub-clinically infected with Actinobacillus pleuropneumoniae. The Veterinary Journal 206: 3038. doi: 10.1016/j.tvjl.2015.06.016.Google Scholar
Gottschalk, M and Lacouture, S (2015). Canada: distribution of Streptococcus suis (from 2012 to 2014) and Actinobacillus pleuropneumoniae (from 2011 to 2014) serotypes isolated from diseased pigs. The Canadian Veterinary Journal 56: 10931094.Google Scholar
Grasteau, A, Tremblay, YD, Labrie, J and Jacques, M (2011). Novel genes associated with biofilm formation of Actinobacillus pleuropneumoniae. Veterinary Microbiology 153: 134143. doi: 10.1016/j.vetmic.2011.03.029.Google Scholar
Harriott, MM and Noverr, MC (2009). Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrobial Agents and Chemotherapy 53: 39143922.Google Scholar
Harro, JM, Peters, BM, O'May, GA, Archer, N, Kerns, P, Prabhakara, R and Shirtliff, ME (2010). Vaccine development in Staphylococcus aureus: taking the biofilm phenotype into consideration. FEMS Immunology and Medical Microbiology 59: 306323. doi: 10.1111/j.1574-695X.2010.00708.x.Google Scholar
Hathroubi, S, Fontaine-Gosselin, , Tremblay, YD, Labrie, J and Jacques, M (2015). Sub-inhibitory concentrations of penicillin G induce biofilm formation by field isolates of Actinobacillus pleuropneumoniae. Veterinary Microbiology 179: 277286.Google Scholar
Hathroubi, S, Hancock, MA, Bossé, JT, Langford, PR, Tremblay, YD, Labrie, J and Jacques, M (2016a). Surface polysaccharide mutants reveal that absence of O antigen reduces biofilm formation of Actinobacillus pleuropneumoniae. Infection and Immunity 84: 127137.Google Scholar
Hathroubi, S, Beaudry, F, Provost, C, Martelet, L, Segura, M, Gagnon, CA and Jacques, M (2016b). Impact of Actinobacillus pleuropneumoniae biofilm mode of growth on the lipid a structures and stimulation of immune cells. Innate Immunity 22: 353362.Google Scholar
Hathroubi, S, Mekni, MA, Domenico, P, Nguyen, D and Jacques, M (2017). Biofilms: microbial shelters against antibiotics. Microbial Drug Resistance 23: 147156. doi: 10.1089/mdr.2016.0087.Google Scholar
Hu, J, Xu, T, Zhu, T, Lou, Q, Wang, X, Wu, Y, Huang, R, Liu, J, Liu, H, Yu, F, Ding, B, Huang, Y, Tong, W and Qu, D (2011). Monoclonal antibodies against accumulation-associated protein affect EPS biosynthesis and enhance bacterial accumulation of Staphylococcus epidermidis. PLoS ONE 6: e20918. doi: 10.1371/journal.pone.0020918.Google Scholar
Huang, L, Xu, Q, Liu, C, Fan, M and Li, Y (2013). Anti-caries DNA vaccine-induced secretory immunoglobulin A antibodies inhibit formation of Streptococcus mutans biofilms in vitro. Acta Pharmacologica Sinica 34: 239246.Google Scholar
Huang, TP, Somers, EB and Wong, AC (2006). Differential biofilm formation and motility associated with lipopolysaccharide/exopolysaccharide-coupled biosynthetic genes in Stenotrophomonas maltophilia. Journal of Bacteriology 188: 31163120. doi: 10.1128/JB.188.8.3116-3120.2006.Google Scholar
Hur, J and Lee, JH (2014). Optimization of immune strategy for a construct of Salmonella-delivered ApxIA, ApxIIA, ApxIIIA and OmpA antigens of Actinobacillus pleuropneumoniae for prevention of porcine pleuropneumonia using a murine model. Veterinary Research Communications 38: 8791.Google Scholar
Hur, J, Eo, SK, Park, SY, Choi, Y and Lee, JH (2016). Immunological study of an attenuated Salmonella Typhimurium expressing ApxIA, ApxIIA, ApxIIIA and OmpA of Actinobacillus pleuropneumoniae in a mouse model. The Journal of Veterinary Medical Science 77: 16931696.Google Scholar
Ito, H (2015). The genetic organization of the capsular polysaccharide biosynthesis region of Actinobacillus pleuropneumoniae serotype 14. The Journal of Veterinary Medical Science 77: 583586. doi: 10.1292/jvms.14-0174.Google Scholar
Izano, EA, Sadovskaya, I, Vinogradov, E, Mulks, MH, Velliyagounder, K, Ragunath, C, Kher, WB, Ramasubbu, N, Jabbouri, S, Perry, MB and Kaplan, JB (2007). Poly-N-acetylglucosamine mediates biofilm formation and antibiotic resistance in Actinobacillus pleuropneumoniae. Microbial Pathogenesis g 43: 19.Google Scholar
Jacques, M, Aragon, V and Tremblay, YDN (2010). Biofilm formation in bacterial pathogens of veterinary importance. Animal Health Research Review 11: 97121.Google Scholar
Jacques, M, Grenier, D, Labrie, J, Provost, C and Gagnon, C (2015). Persistence of porcine reproductive and respiratory syndrome virus and porcine circovirus type 2 in bacterial biofilms. Journal of Swine Health & Production 23: 132136.Google Scholar
Jefferson, KK (2004). What drives bacteria to produce a biofilm? FEMS Microbiology Letters 236: 163173.Google Scholar
Jin, H, Zhou, R, Kang, M, Luo, R, Cai, X and Chen, H (2006). Biofilm formation by field isolates and reference strains of Haemophilus parasuis. Veterinary Microbiology 118(1–2): 117123.Google Scholar
Kaplan, JB and Mulks, MH (2005). Biofilm formation is prevalent among field isolates of Actinobacillus pleuropneumoniae. Veterinary Microbiology 108(1–2): 8994.Google Scholar
Kaplan, JB, Velliyagounder, K, Ragunath, C, Rohde, H, Mack, D, Knobloch, JK and Ramasubbu, N (2004). Genes involved in the synthesis and degradation of matrix polysaccharide in Actinobacillus actinomycetemcomitans and Actinobacillus pleuropneumoniae biofilms. Journal of Bacteriology 186: 82138220. doi: 10.1128/JB.186.24.8213-8220.2004.Google Scholar
Kim, MY, Kim, TG and Yang, MS (2016). Production and immunogenicity of Actinobacillus pleuropneumoniae ApxIIA protein in transgenic rice callus. Protein Expression and Purification S1046-5928: 30088-2.Google Scholar
Kragh, KN, Hutchison, JB, Melaugh, G, Rodesney, C, Roberts, AE, Irie, Y, Jensen, , Diggle, SP, Allen, RJ, Gordon, V and Bjarnsholt, T (2016). Role of multicellular aggregates in biofilm formation. mBio 7: e00237-16.Google Scholar
Labrie, J, Pelletier-Jacques, G, Deslandes, V, Ramjeet, M, Auger, E, Nash, JH and Jacques, M (2010). Effects of growth conditions on biofilm formation by Actinobacillus pleuropneumoniae. Veterinary Research 41: 03.Google Scholar
Lam, H, Kesselly, A, Stegalkina, S, Kleanthous, H and Yethon, JA (2014). Antibodies to PhnD inhibit staphylococcal biofilms. Infection and Immunity 82: 37643774. doi:10.1128/IAI.02168-14.Google Scholar
Lee, SH, Lee, S, Chae, C and Ryu, DY (2014). A recombinant chimera comprising the R1 and R2 repeat regions of M. hyopneumoniae P97 and the N-terminal region of A. pleuropneumoniae ApxIII elicits immune responses. BMC Veterinary Research 10: 43.Google Scholar
Li, G, Xie, F, Zhang, Y, Bossé, JT, Langford, PR and Wang, C (2015). Role of (p)ppGpp in viability and biofilm formation of Actinobacillus pleuropneumoniae S8. PLoS ONE 10: e0141501.Google Scholar
Li, HS, Shin, MK, Singh, B, Maharjan, S, Park, TE, Kang, SK, Yoo, HS, Hong, ZS, Cho, CS and Choi, YJ (2016c). Nasal immunization with mannan-decorated mucoadhesive HPMCP microspheres containing ApxIIA toxin induces protective immunity against challenge infection with Actinobacillus pleuropneumoniae in mice. Journal of Controlled Release 233: 114125.Google Scholar
Li, J and Wang, N (2011). The wxacO gene of Xanthomonas citri ssp. citri encodes a protein with a role in lipopolysaccharide biosynthesis, biofilm formation, stress tolerance and virulence. Molecular Plant Pathology 12: 381396.Google Scholar
Li, L, Zhou, R, Li, T, Kang, M, Wan, Y, Xu, Z and Chen, H (2008). Enhanced biofilm formation and reduced virulence of Actinobacillus pleuropneumoniae luxS mutant. Microbial Pathogenesis 45(3): 192200.Google Scholar
Li, L, Xu, Z, Zhou, Y, Li, T, Sun, L, Chen, H and Zhou, R (2011). Analysis on Actinobacillus pleuropneumoniae LuxS regulated genes reveals pleiotropic roles of LuxS/AI-2 on biofilm formation, adhesion ability and iron metabolism. Microbial Pathogenesis 50: 293302.Google Scholar
Li, L, Xu, Z, Zhou, Y, Sun, L, Liu, Z, Chen, H and Zhou, R (2012). Global effects of catecholamines on Actinobacillus pleuropneumoniae gene expression. PLoS ONE 7: e31121.Google Scholar
Li, L, Sun, C, Yang, F, Yang, S, Feng, X, Gu, J, Han, W, Langford, PR and Lei, L (2013). Identification of proteins of Propionibacterium acnes for use as vaccine candidates to prevent infection by the pig pathogen Actinobacillus pleuropneumoniae. Vaccine 31: 52695275.Google Scholar
Li, L, Zhu, J, Yang, K, Xu, Z, Liu, Z and Zhou, R (2014). Changes in gene expression of Actinobacillus pleuropneumoniae in response to anaerobic stress reveal induction of central metabolism and biofilm formation. Journal of Microbiology 52: 473481.Google Scholar
Li, Y, Cao, S, Zhang, L, Yuan, J, Lau, GW, Wen, Y, Wu, R, Zhao, Q, Huang, X, Yan, Q, Huang, Y and Wen, X (2016a). Absence of TolC impairs biofilm formation in Actinobacillus pleuropneumoniae by reducing initial attachment. PLoS ONE 11: e0163364.Google Scholar
Li, Y, Cao, S, Zhang, L, Lau, GW, Wen, Y, Wu, R, Zhao, Q, Huang, X, Yan, Q, Huang, Y and Wen, X (2016b). A TolC-like protein of Actinobacillus pleuropneumoniae is involved in antibiotic resistance and biofilm formation. Frontiers in Microbiology 7: 1618.Google Scholar
Little, DJ, Poloczek, J, Whitney, JC, Robinson, H, Nitz, M and Howell, PL (2012). The structure- and metal-dependent activity of Escherichia coli PgaB provides insight into the partial de-N-acetylation of poly-beta-1,6-N-acetyl-D-glucosamine. Journal of Biological Chemistry 287: 3112631137.Google Scholar
Loera-Muro, A, Jacques, M, Avelar-González, FJ, Labrie, J, Tremblay, YD, Oropeza-Navarro, R and Guerrero-Barrera, A (2016). Auxotrophic Actinobacillus pleuropneumoniae grows in multispecies biofilms without the need for nicotinamide-adenine dinucleotide (NAD) supplementation. BMC Microbiology 16: 128. doi: 10.1186/s12866-016-0742-3.Google Scholar
Loera-Muro, V, Jacques, M, Tremblay, Y, Avelar-González, F, Loera-Muro, A, Ramírez, E, Medina, A, González, H and Guerrero-Barrera, AL (2013). Detection of Actinobacillus pleuropneumoniae in drinking water from pig farms. Microbiology 159: 536544. doi: 10.1099/mic.0.057992-0.Google Scholar
Lone, AG, Deslandes, V, Nash, JH, Jacques, M and Macinnes, JI (2009). Modulation of gene expression in Actinobacillus pleuropneumoniae exposed to bronchoalveolar fluid. PLoS ONE 4: e6139.Google Scholar
Lopez-Bermudez, J, Quintanar-Guerrero, D, Lara-Puente, H, Tórtora-Perez, J, Suárez, F, Ciprián-Carrasco, A and Mendoza, S (2014). Oral immunization against porcine pleuropneumonia using the cubic phase of monoolein and purified toxins of Actinobacillus pleuropneumoniae. Vaccine 32: 68056811.Google Scholar
Lu, YC, Li, MC, Chen, YM, Chu, CY, Lin, SF and Yang, WJ (2011). DNA vaccine encoding type IV pilin of Actinobacillus pleuropneumoniae induces strong immune response but confers limited protective efficacy against serotype 2 challenge. Vaccine 29: 77407746.Google Scholar
MacInnes, JI, Gottschalk, M, Lone, AG, Metcalf, DS, Ojha, S, Rosendal, T, Watson, SB and Friendship, RM (2008). Prevalence of Actinobacillus pleuropneumoniae, Actinobacillus suis, Haemophilus parasuis, Pasteurella multocida, and Streptococcus suis in representative Ontario swine herds. Canadian Journal of Veterinary Research 72: 242248.Google Scholar
Merritt, J, Qi, F, Goodman, SD, Anderson, MH and Shi, W (2003). Mutation of luxS affects biofilm formation in Streptococcus mutans. Infection and Immunity 71: 19721979.Google Scholar
Morioka, A, Shimazaki, Y, Uchiyama, M and Suzuki, S (2016). Serotyping reanalysis of unserotypable Actinobacillus pleuropneumoniae isolates by agar gel diffusion test. Journal of Veterinary Medical Science 78: 723725. doi: 10.1292/jvms.15-0538.Google Scholar
Musken, M, Di Fiore, S, Dotsch, A, Fischer, R and Haussler, S (2010). Genetic determinants of Pseudomonas aeruginosa biofilm establishment. Microbiology 156: 431441.Google Scholar
Nadell, CD, Drescher, K, Wingreen, NS and Bassler, BL (2015). Extracellular matrix structure governs invasion resistance in bacterial biofilms. ISME Journal 9: 17001709.Google Scholar
Nair, N, Vinod, V, Suresh, MK, Vijayrajratnam, S, Biswas, L, Peethambaran, R, Vasudevan, AK and Biswas, R (2015). Amidase, a cell wall hydrolase, elicits protective immunity against Staphylococcus aureus and S. epidermidis. International Journal of Biological Macromolecules 77: 314321. doi: 10.1016/j.ijbiomac.2015.03.047.Google Scholar
Nicolet, J (1988). Taxonomy and serological identification of Actinobacillus pleuropneumoniae. Canadian Veterinary Journal 29: 578580.Google Scholar
Olsen, I (2015). Biofilm-specific antibiotic tolerance and resistance. European Journal of Clinical Microbiology & Infectious Diseases 34: 877886.Google Scholar
Olson, ME, Ceri, H, Morck, DW, Buret, AG and Read, RR (2002). Biofilm bacteria: formation and comparative susceptibility to antibiotics. Canadian Journal of Veterinary Research 66: 8692.Google Scholar
O'May, GA, Jacobsen, SM, Longwell, M, Stoodley, P, Mobley, HL and Shirtliff, ME (2009). The high-affinity phosphate transporter Pst in Proteus mirabilis HI4320 and its importance in biofilm formation. Microbiology 155: 15231535.Google Scholar
Opriessnig, T, Giménez-Lirola, LG and Halbur, PG (2011). Polymicrobial respiratory disease in pigs. Animal Health Research Review 12: 133148.Google Scholar
O'Reilly, T and Niven, DF (1986). Defining the metabolic and growth responses of porcine haemophili to exogenous pyridine nucleotides and precursors. Journal of General Microbiology 132: 807818.Google Scholar
Otto, K and Silhavy, TJ (2002). Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proceedings of the National Academy of Sciences USA 99: 22872292.Google Scholar
Peddayelachagiri, BV, Paul, S, Makam, SS, Urs, RM, Kingston, JJ, Tuteja, U, Sripathy, MH and Batra, HV (2014). Functional characterization and evaluation of in vitro protective efficacy of murine monoclonal antibodies BURK24 and BURK37 against Burkholderia pseudomallei. PLoS ONE 9: e90930. doi:10.1371/journal.pone.0090930.Google Scholar
Perry, MB, Angen, O, Maclean, LL, Lacouture, S, Kokotovic, B and Gottschalk, M (2012). An atypical biotype I Actinobacillus pleuropneumoniae serovar 13 is present in North America. Veterinary Microbiology 156: 403410.Google Scholar
Peters, BM, Jabra-Rizk, MA, O'May, GA, Costerton, JW and Shirtliff, ME (2012). Polymicrobial interactions: impact on pathogenesis and human disease. Clinical Microbiology Reviews 25: 193213.Google Scholar
Pohl, S, Bertschinger, HU, Frederiksen, W and Mannheim, W (1983). Transfer of Haemophilus pleuropneumoniae and the Pasteurella haernolytica-like organism causing porcine necrotic pleuropneumonia to the genus Actinobacillus (Actinobacillus pleuropneumoniae comb. nov.) on the basis of phenotypic and deoxyribonucleic acid relatedness. International Journal of Systematic Bacteriology 33: 510514.Google Scholar
Prouty, AM, Schwesinger, WH and Gunn, JS (2002). Biofilm formation and interaction with the surfaces of gallstones by Salmonella spp. Infection and Immunity 70: 26402649.Google Scholar
Ramjeet, M, Cox, AD, Hancock, MA, Mourez, M, Labrie, J, Gottschalk, M and Jacques, M (2008). Mutation in the LPS outer core biosynthesis gene, galU, affects LPS interaction with the RTX toxins ApxI and ApxII and cytolytic activity of Actinobacillus pleuropneumoniae serotype 1. Molecular Microbiology 70: 221235.Google Scholar
Rioux, S, Galarneau, C, Harel, J, Kobisch, M, Frey, J, Gottschalk, M and Jacques, M (2000). Isolation and characterization of a capsule-deficient mutant of Actinobacillus pleuropneumoniae serotype 1. Microbial Pathogenesis 28: 279289.Google Scholar
Sadilkova, L, Nepereny, J, Vrzal, V, Sebo, P and Osicka, R (2012). Type IV fimbrial subunit protein ApfA contributes to protection against porcine pleuropneumonia. Veterinary Research 43: 2.Google Scholar
Sandal, I, Hong, W, Swords, WE and Inzana, TJ (2007). Characterization and comparison of biofilm development by pathogenic and commensal isolates of Histophilus somni. Journal of Bacteriology 189: 81798185.Google Scholar
Sárközi, R, Makrai, L and Fodor, L (2015). Identification of a proposed new serovar of Actinobacillus pleuropneumoniae: serovar 16. Acta Veterinaria Hungarica 63: 444450. doi: 10.1556/004.2015.041.Google Scholar
Schmidt, C, Cibulski, SP, Andrade, CP, Teixeira, TF, Valera, APM, Scheffer, CM, Franco, AC, Almeida, LL and Roehe, PM (2016). Swine influenza virus and association with the porcine respiratory disease complex in pig farms in southern Brazil. Zoonoses and Public Health 63: 234240.Google Scholar
Schwartz, K, Stephenson, R, Hernandez, M, Jambang, N and Boles, BR (2010). The use of drip flow and rotating disk reactors for Staphylococcus aureus biofilm analysis. Journal of Visualized Experiments 46: e2470.Google Scholar
Serrano, L, Tenorio-Gutiérrez, V, Suárez, F, Reyes-Cortés, R, Rodríguez-Mendiola, M, Arias-Castro, C, Godínez-Vargas, D and de la Garza, M (2008). Identification of Actinobacillus pleuropneumoniae biovars 1 and 2 in pigs using a PCR assay. Molecular and Cellular Probes 22: 305312.Google Scholar
Shahrooei, M, Hira, V, Khodaparast, L, Khodaparast, L, Stijlemans, B, Kucharíková, S, Burghout, P, Hermans, PWM and Elderea, JV (2012). Vaccination with SesC decreases Staphylococcus epidermidis biofilm formation. Infection and Immunity 80: 36603668.Google Scholar
Shao, M, Wang, Y, Wang, C, Guo, Y, Peng, Y, Liu, J, Li, G, Liu, H and Liu, S (2010). Evaluation of multicomponent recombinant vaccines against Actinobacillus pleuropneumoniae in mice. Acta Veterinaria Scandinavica 52: 52.Google Scholar
Shin, MK, Jung, MH, Lee, WJ, Choi, PS, Jang, YS and Yoo, HS (2011). Generation of transgenic corn-derived Actinobacillus pleuropneumoniae ApxIIA fused with the cholera toxin B subunit as a vaccine candidate. Journal of Veterinary Science 12: 401403.Google Scholar
Shope, RE (1964). Porcine contagious pleuropneumonia. I. Experimental transmission, etiology, and pathology. Journal of Experimental Medicine 119: 357368.Google Scholar
Shope, RE, White, DC and Leidy, G (1964). Porcine contagious pleuropneumonia. II. Studies of the pathogenicity of the etiological agent, Hemophilus pleuropneumoniae. Journal of Experimental Medicine 119: 369375.Google Scholar
Sjölund, M and Wallgren, P (2010). Field experience with two different vaccination strategies aiming to control infections with Actinobacillus pleuropneumoniae in a fattening pig herd. Acta Veterinaria Scandinavica 52: 23.Google Scholar
Speziale, P, Pietrocola, G, Foster, T and Geoghegan, J (2014). Protein-based biofilm matrices in staphylococci. Frontiers in Cellular and Infection Microbiology 4: 171.Google Scholar
Stewart, PS and Franklin, MJ (2008). Physiological heterogeneity in biofilms. Nature Review Microbiology 6: 199210.Google Scholar
Subashchandrabosea, S, Leveque, RM, Kirkwoodc, RN, Kiupela, M and Mulksa, MH (2013). The RNA chaperone Hfq promotes fitness of Actinobacillus pleuropneumoniae during porcine pleuropneumonia. Infection and Immunity 81: 29522961.Google Scholar
Tegetmeyer, H, Fricke, K and Baltes, N (2009). An isogenic Actinobacillus pleuropneumoniae AasP mutant exhibits altered biofilm formation but retains virulence. Veterinary Microbiology 137: 392396.Google Scholar
Theoret, JR, Cooper, KK, Zekarias, B, Roland, KL, Law, BF, Curtiss, R and Joensa, LA (2012). 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. Clinical and Vaccine Immunology 19: 14261431.Google Scholar
To, H, Nagai, S, Iwata, A, Koyama, T, Oshima, A and Tsutsumi, N (2016). Genetic and antigenic characteristics of ApxIIA and ApxIIIA from Actinobacillus pleuropneumoniae serovars 2, 3, 4, 6, 8 and 15. Microbiology and Immunology 60: 447458.Google Scholar
Tremblay, YDN, Deslandes, V and Jacques, M (2013a). Actinobacillus pleuropneumoniae genes expression in biofilms cultured under static conditions and in a drip-flow apparatus. BMC Genomics 14: 364.Google Scholar
Tremblay, YDN, Lévesque, C, Segers, RP and Jacques, M (2013b). Method to grow Actinobacillus pleuropneumoniae biofilm on a biotic surface. BMC Veterinary Research 9: 213.Google Scholar
Tremblay, YDN, Labrie, J, Chénier, S and Jacques, M (2017). Actinobacillus pleuropneumoniae grows as aggregates in the lung of pigs: is it time to refine our in vitro biofilm assays? Microbial Biotechnology 10: 756760. doi: 10.1111/1751-7915.12432.Google Scholar
Turni, C, Singh, R, Schembri, MA and Blackall, PJ (2014). Evaluation of a multiplex PCR to identify and serotype Actinobacillus pleuropneumoniae serovars 1, 5, 7, 12 and 15. Letters in Applied Microbiology 59: 362369. doi: 10.1111/lam.12287.Google Scholar
Vogt, MC, Schraner, EM, Aguilar, C and Eichwald, C (2016). Heterologous expression of antigenic peptides in Bacillus subtilis biofilms. Microbial Cell Factories 15: 137. doi: 10.1186/s12934-016-0532-5.Google Scholar
Vogt, SL and Raivio, TL (2012). Just scratching the surface: an expanding view of the Cpx envelope stress response. FEMS Microbiology Letters 326: 211. doi: 10.1111/j.1574-6968.2011.02406.x.Google Scholar
Wang, L, Vinogradov, EV and Bogdanove, AJ (2013). Requirement of the lipopolysaccharide O-chain biosynthesis gene wxocB for type III secretion and virulence of Xanthomonas oryzae pv. oryzicola. Journal of Bacteriology 195: 19591969. doi: 10.1128/JB.02299-12.Google Scholar
Wang, L, Qin, W, Yang, S, Zhai, R, Zhou, L, Sun, C, Pan, F, Ji, Q, Wang, Y, Gu, J, Feng, X, Du, C, Han, W, Langford, PR and Lei, L (2015). The Adh adhesin domain is required for trimeric autotransporter Apa1-mediated Actinobacillus pleuropneumoniae adhesion, autoaggregation, biofilm formation and pathogenicity. Veterinary Microbiology 177: 175183.Google Scholar
Wang, L, Qin, W, Zhang, J, Bao, C, Zhang, H, Che, Y, Sun, C, Gu, J, Feng, X, Du, C, Han, W, Richard, PL and Lei, L (2016). Adh enhances Actinobacillus pleuropneumoniae pathogenicity by binding to OR5M11 and activating p38 which induces apoptosis of PAMs and IL-8 release. Scientific Reports 6: 24058. doi: 10.1038/srep24058.Google Scholar
Willems, HM, Xu, Z and Peters, BM (2016). Polymicrobial biofilm studies: from basic science to biofilm control. Current Oral Health Reports 3: 3644.Google Scholar
Wu, C, Labrie, J, Tremblay, YD, Haine, D, Mourez, M and Jacques, M (2013). Zinc as an agent for the prevention of biofilm formation by pathogenic bacteria. Journal of Applied Microbiology 115: 3040.Google Scholar
Xiao, L, Zhou, L, Sun, C, Feng, X, Du, C, Gao, Y, Ji, Q, Yang, S, Wang, Y, Han, W, Langford, PR and Lei, L (2012). Apa is a trimeric autotransporter adhesin of Actinobacillus pleuropneumoniae responsible for autoagglutination and host cell adherence. Journal of Basic Microbiology 52: 598607.Google Scholar
Xie, F, Zhang, Y, Li, G, Liu, S and Wang, C (2013). The ClpP protease is required for the stress tolerance and biofilm formation in Actinobacillus pleuropneumoniae. PLoS ONE 8: e53600.Google Scholar
Xie, F, Li, G, Zhang, W, Zhang, Y, Zhou, L, Liu, S, Liu, S and Wang, C (2016a). Outer membrane lipoprotein VacJ is required for the membrane integrity, serum resistance and biofilm formation of Actinobacillus pleuropneumoniae. Veterinary Microbiology 183: 18.Google Scholar
Xie, F, Li, G, Zhang, Y, Zhou, L, Liu, S, Liu, S and Wang, C (2016b). The Lon protease homologue LonA, not LonC, contributes to the stress tolerance and biofilm formation of Actinobacillus pleuropneumoniae. Microbial Pathogenesis 93: 3843. doi: 10.1016/j.micpath.2016.01.009.Google Scholar
Yan, L, Zhang, L, Ma, H, Chiu, D and Bryers, JD (2014). A single B-repeat of Staphylococcus epidermidis accumulation-associated protein induces protective immune responses in an experimental biomaterial-associated infection mouse model. Clinical and Vaccine Immunology 21: 12061214. doi: 10.1128/CVI.00306-14.Google Scholar
Yang, F, Ma, Q, Lei, L, Huang, J, Ji, Q, Zhai, R, Wang, L, Wang, Y, Li, L, Sun, C, Feng, X and Han, W (2014). Specific humoral immune response induced by Propionibacterium acnes can prevent Actinobacillus pleuropneumoniae infection in mice. Clinical and Vaccine Immunology 21: 407416.Google Scholar
Yi, L, Wang, Y, Ma, Z, Lin, HX, Xu, B, Grenier, D, Fan, HJ and Lu, CP (2016). Identification and characterization of a Streptococcus equi ssp. Zooepidemicus immunogenic GroEL protein involved in biofilm formation. Veterinary Research 47: 50. doi: 10.1186/s13567-016-0334-0.Google Scholar