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ORIGINAL ARTICLE

Comparative transcriptomic analysis of Clostridium perfringens biofilms and planktonic cells

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Pages 593-601 | Received 15 Nov 2015, Accepted 06 Apr 2016, Published online: 19 Sep 2016

References

  • Ahmed, N.A., Petersen, F.C. & Scheie, A.A. (2009). AI-2/LuxS is involved in increased biofilm formation by Streptococcus intermedius in the presence of antibiotics. Antimicrobial Agents and Chemotherapy, 53, 4258–4263. doi: 10.1128/AAC.00546-09
  • Banin, E., Vasil, M.L. & Greenberg, E.P. (2005). Iron and Pseudomonas aeruginosa biofilm formation. Proceedings of the National Academy of Sciences, 102, 11076–11081. doi: 10.1073/pnas.0504266102
  • Bridier, A., Briandet, R., Thomas, V. & Dubois-Brissonnet, F. (2011). Resistance of bacterial biofilms to disinfectants: a review. Biofouling, 27, 1017–1032. doi: 10.1080/08927014.2011.626899
  • Burns, D.A., Heap, J.T. & Minton, N.P. (2010). SleC is essential for germination of Clostridium difficile spores in nutrient-rich medium supplemented with the bile salt taurocholate. Journal of Bacteriology, 192, 657–664. doi: 10.1128/JB.01209-09
  • Caiazza, N.C. & O’Toole, G.A. (2003). Alpha-toxin is required for biofilm formation by Staphylococcus aureus. Journal of Bacteriology, 185, 3214–3217. doi: 10.1128/JB.185.10.3214-3217.2003
  • Carvalhais, V., Franca, A., Cerca, F., Vitorino, R., Pier, G.B., Vilanova, M. & Cerca, N. (2014). Dormancy within Staphylococcus epidermidis biofilms: a transcriptomic analysis by RNA-seq. Applied Microbiology and Biotechnology, 98, 2585–2596. doi: 10.1007/s00253-014-5548-3
  • Charlebois, A., Jacques, M. & Archambault, M. (2014). Biofilm formation of Clostridium perfringens and its exposure to low-dose antimicrobials. Frontiers in Microbiology, 5, 183. doi: 10.3389/fmicb.2014.00183
  • CLSI. (2012). Methods for antimicrobial susceptibility testing of anaerobic bacteria; approved standard (8th edn). CLSI document M11-A6. Wayne, PA: Clinical and Laboratory Standards Institute.
  • Costerton, J.W., Stewart, P.S. & Greenberg, E.P. (1999). Bacterial biofilms: a common cause of persistent infections. Science, 284, 1318–1322. doi: 10.1126/science.284.5418.1318
  • Dawson, L.F., Valiente, E., Faulds-Pain, A., Donahue, E.H. & Wren, B.W. (2012). Characterisation of Clostridium difficile biofilm formation, a role for Spo0A. PLoS One, 7, e50527. doi: 10.1371/journal.pone.0050527
  • Esperanza Troyano, S.-P.L., Rha, C.K. & Sinskey, A.J. (1996). Presence of acetate and succinate in the exopolysaccharide produced by Zoogloea ramigera 115SLR. Carbohydrate Polymers, 31, 35–40. doi: 10.1016/S0144-8617(96)00056-2
  • Ethapa, T., Leuzzi, R., Ng, Y.K., Baban, S.T., Adamo, R., Kuehne, S.A., Scarselli, M., Minton, N.P., Serruto, D. & Unnikrishnan, M. (2013). Multiple factors modulate biofilm formation by the anaerobic pathogen Clostridium difficile. Journal of Bacteriology, 195, 545–555. doi: 10.1128/JB.01980-12
  • Falsetta, M.L., Steichen, C.T., McEwan, A.G., Cho, C., Ketterer, M., Shao, J., Hunt, J., Jennings, M.P. & Apicella, M.A. (2011). The composition and metabolic phenotype of Neisseria gonorrhoeae biofilms. Frontiers in Microbiology, 2, 75. doi: 10.3389/fmicb.2011.00075
  • Flemming, H.C. & Wingender, J. (2010). The biofilm matrix. Nature Reviews Microbiology, 8, 623–633.
  • Galperin, M.Y., Mekhedov, S.L., Puigbo, P., Smirnov, S., Wolf, Y.I. & Rigden, D.J. (2012). Genomic determinants of sporulation in Bacilli and Clostridia: towards the minimal set of sporulation-specific genes. Environmental Microbiology, 14, 2870–2890. doi: 10.1111/j.1462-2920.2012.02841.x
  • Gambino, M. & Cappitelli, F. (2016). Mini-review: biofilm responses to oxidative stress. Biofouling, 32, 167–178. doi: 10.1080/08927014.2015.1134515
  • Hamon, M.A. & Lazazzera, B.A. (2001). The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Molecular Microbiology, 42, 1199–1209. doi: 10.1046/j.1365-2958.2001.02709.x
  • Harrison, J.J., Turner, R.J. & Ceri, H. (2005). Persister cells, the biofilm matrix and tolerance to metal cations in biofilm and planktonic Pseudomonas aeruginosa. Environmental Microbiology, 7, 981–994. doi: 10.1111/j.1462-2920.2005.00777.x
  • Hidalgo-Cantabrana, C., Sanchez, B., Milani, C., Ventura, M., Margolles, A. & Ruas-Madiedo, P. (2014). Genomic overview and biological functions of exopolysaccharide biosynthesis in Bifidobacterium spp. Applied and Environmental Microbiology, 80, 9–18. doi: 10.1128/AEM.02977-13
  • Hoiby, N., Bjarnsholt, T., Givskov, M., Molin, S. & Ciofu, O. (2010). Antibiotic resistance of bacterial biofilms. International Journal of Antimicrobial Agents, 35, 322–332. doi: 10.1016/j.ijantimicag.2009.12.011
  • Honma, K., Mishima, E., Inagaki, S. & Sharma, A. (2009). The OxyR homologue in Tannerella forsythia regulates expression of oxidative stress responses and biofilm formation. Microbiology, 155, 1912–1922. doi: 10.1099/mic.0.027920-0
  • Huse, H.K., Kwon, T., Zlosnik, J.E., Speert, D.P., Marcotte, E.M. & Whiteley, M. (2013). Pseudomonas aeruginosa enhances production of a non-alginate exopolysaccharide during long-term colonization of the cystic fibrosis lung. PLoS One, 8, e82621. doi: 10.1371/journal.pone.0082621
  • Ledeboer, N.A. & Jones, B.D. (2005). Exopolysaccharide sugars contribute to biofilm formation by Salmonella enterica serovar Typhimurium on HEp-2 cells and chicken intestinal epithelium. Journal of Bacteriology, 187, 3214–3226. doi: 10.1128/JB.187.9.3214-3226.2005
  • Lepp, D., Gong, J., Songer, J.G., Boerlin, P., Parreira, V.R. & Prescott, J.F. (2013). Identification of accessory genome regions in poultry Clostridium perfringens isolates carrying the netB plasmid. Journal of Bacteriology, 195, 1152–1166. doi: 10.1128/JB.01032-12
  • Lepp, D., Roxas, B., Parreira, V.R., Marri, P.R., Rosey, E.L., Gong, J., Songer, J.G., Vedantam, G. & Prescott, J.F. (2010). Identification of novel pathogenicity loci in Clostridium perfringens strains that cause avian necrotic enteritis. PLoS One, 5, e10795. doi: 10.1371/journal.pone.0010795
  • Lewis, K. (2005). Persister cells and the riddle of biofilm survival. Biochemistry (Moscow), 70, 267–274. doi: 10.1007/s10541-005-0111-6
  • Li, J. & McClane, B.A. (2010). Evaluating the involvement of alternative sigma factors SigF and SigG in Clostridium perfringens sporulation and enterotoxin synthesis. Infection and Immunity, 78, 4286–4293. doi: 10.1128/IAI.00528-10
  • Lin, M.H., Shu, J.C., Huang, H.Y. & Cheng, Y.C. (2012). Involvement of iron in biofilm formation by Staphylococcus aureus. PLoS One, 7, e34388. doi: 10.1371/journal.pone.0034388
  • Lo, A.W., Seers, C.A., Boyce, J.D., Dashper, S.G., Slakeski, N., Lissel, J.P. & Reynolds, E.C. (2009). Comparative transcriptomic analysis of Porphyromonas gingivalis biofilm and planktonic cells. BMC Microbiology, 9, 18. doi: 10.1186/1471-2180-9-18
  • Love, M.I., Huber, W. & Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 31. doi: 10.1186/s13059-014-0550-8
  • Markey, B., Leonard, F., Archambault, M., Cullinane, A. & Maguire, D. (2013). Clinical Veterinary Microbiology (2nd edn., pp. 908). London: Mosby Elsevier.
  • Miyata, S., Moriyama, R., Miyahara, N. & Makino, S. (1995). A gene (sleC) encoding a spore-cortex-lytic enzyme from Clostridium perfringens S40 spores; cloning, sequence analysis and molecular characterization. Microbiology, 141, 2643–2650. doi: 10.1099/13500872-141-10-2643
  • Myers, G.S., Rasko, D.A., Cheung, J.K., Ravel, J., Seshadri, R., DeBoy, R.T., Ren, Q., Varga, J., Awad, M.M., Brinkac, L.M., Daugherty, S.C., Haft, D.H., Dodson, R.J., Madupu, R., Nelson, W.C., Rosovitz, M.J., Sullivan, S.A., Khouri, H., Dimitrov, G.I., Watkins, K.L., Mulligan, S., Benton, J., Radune, D., Fisher, D.J., Atkins, H.S., Hiscox, T., Jost, B.H., Billington, S.J., Songer, J.G., McClane, B.A., Titball, R.W., Rood, J.I., Melville, S.B. & Paulsen, I.T. (2006). Skewed genomic variability in strains of the toxigenic bacterial pathogen, Clostridium perfringens. Genome Research, 16, 1031–1040. doi: 10.1101/gr.5238106
  • Obana, N., Nakamura, K. & Nomura, N. (2014). A sporulation factor is involved in the morphological change of Clostridium perfringens biofilms in response to temperature. Journal of Bacteriology, 196, 1540–1550. doi: 10.1128/JB.01444-13
  • Ohtani, K., Hayashi, H. & Shimizu, T. (2002). The luxS gene is involved in cell-cell signalling for toxin production in Clostridium perfringens. Molecular Microbiology, 44, 171–179. doi: 10.1046/j.1365-2958.2002.02863.x
  • Pantaléon, V., Bouttier, S., Soavelomandroso, A.P., Janoir, C. & Candela, T. (2014). Biofilms of Clostridium species. Anaerobe, 30, 193–198. doi: 10.1016/j.anaerobe.2014.09.010
  • Petit, L., Gibert, M. & Popoff, M.R. (1999). Clostridium perfringens: toxinotype and genotype. Trends in Microbiology, 7, 104–110. doi: 10.1016/S0966-842X(98)01430-9
  • Prigent-Combaret, C., Prensier, G., Le Thi, T.T., Vidal, O., Lejeune, P. & Dorel, C. (2000). Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of flagella, curli and colanic acid. Environmental Microbiology, 2, 450–464. doi: 10.1046/j.1462-2920.2000.00128.x
  • Resch, A., Rosenstein, R., Nerz, C. & Gotz, F. (2005). Differential gene expression profiling of Staphylococcus aureus cultivated under biofilm and planktonic conditions. Applied and Environmental Microbiology, 71, 2663–2676. doi: 10.1128/AEM.71.5.2663-2676.2005
  • Rumbo-Feal, S., Gomez, M.J., Gayoso, C., Alvarez-Fraga, L., Cabral, M.P., Aransay, A.M., Rodríguez-Ezpeleta, N., Fullaondo, A., Valle, J., Tomás, M., Bou, G. & Poza, M. (2013). Whole transcriptome analysis of Acinetobacter baumannii assessed by RNA-sequencing reveals different mRNA expression profiles in biofilm compared to planktonic cells. PLoS One, 8, e72968. doi: 10.1371/journal.pone.0072968
  • Sabev, H.A., Robson, G.D. & Handley, P.S. (2006). Influence of starvation, surface attachment and biofilm growth on the biocide susceptibility of the biodeteriogenic yeast Aureobasidium pullulans. Journal of Applied Microbiology, 101, 319–330. doi: 10.1111/j.1365-2672.2006.03014.x
  • Sanchez, C.J., Kumar, N., Lizcano, A., Shivshankar, P., Dunning Hotopp, J.C., Jorgensen, J.H., Tettelin, H. & Orihuela, C.J. (2011). Streptococcus pneumoniae in biofilms are unable to cause invasive disease due to altered virulence determinant production. PLoS One, 6, e28738. doi: 10.1371/journal.pone.0028738
  • Sarker, M.R., Carman, R.J. & McClane, B.A. (1999). Inactivation of the gene (cpe) encoding Clostridium perfringens enterotoxin eliminates the ability of two cpe-positive C. perfringens type A human gastrointestinal disease isolates to affect rabbit ileal loops. Molecular Microbiology, 33, 946–958. doi: 10.1046/j.1365-2958.1999.01534.x
  • Sauer, K. (2003). The genomics and proteomics of biofilm formation. Genome Biology, 4, 219. doi: 10.1186/gb-2003-4-6-219
  • Sauer, K. & Camper, A.K. (2001). Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. Journal of Bacteriology, 183, 6579–6589. doi: 10.1128/JB.183.22.6579-6589.2001
  • Sauer, K., Camper, A.K., Ehrlich, G.D., Costerton, J.W. & Davies, D.G. (2002). Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. Journal of Bacteriology, 184, 1140–1154. doi: 10.1128/jb.184.4.1140-1154.2002
  • Scallan, E., Hoekstra, R.M., Angulo, F.J., Tauxe, R.V., Widdowson, M.A., Roy, S.L., Jones, J.L. & Griffin, P.M. (2011). Foodborne illness acquired in the United States—major pathogens. Emerging Infectious Diseases, 17, 7–15. doi: 10.3201/eid1701.P11101
  • Scallan, E., Hoekstra, R.M., Mahon, B.E., Jones, T.F. & Griffin, P.M. (2015). An assessment of the human health impact of seven leading foodborne pathogens in the United States using disability adjusted life years. Epidemiology and Infection, 143, 2795–2804. doi: 10.1017/S0950268814003185
  • Schembri, M.A., Kjaergaard, K. & Klemm, P. (2003). Global gene expression in Escherichia coli biofilms. Molecular Microbiology, 48, 253–267. doi: 10.1046/j.1365-2958.2003.03432.x
  • Songer, J.G. (2010). Clostridia as agents of zoonotic disease. Veterinary Microbiology, 140, 399–404. doi: 10.1016/j.vetmic.2009.07.003
  • Stanley, D., Wu, S.B., Rodgers, N., Swick, R.A. & Moore, R.J. (2014). Differential responses of cecal microbiota to fishmeal, Eimeria and Clostridium perfringens in a necrotic enteritis challenge model in chickens. PLoS One, 9, e104739. doi: 10.1371/journal.pone.0104739
  • Stewart, P.S. & Franklin, M.J. (2008). Physiological heterogeneity in biofilms. Nature Reviews Microbiology, 6, 199–210. doi: 10.1038/nrmicro1838
  • Taylor, R.H., Falkinham, J.O.3rd, Norton, C.D. & LeChevallier, M.W. (2000). Chlorine, chloramine, chlorine dioxide, and ozone susceptibility of Mycobacterium avium. Applied and Environmental Microbiology, 66, 1702–1705. doi: 10.1128/AEM.66.4.1702-1705.2000
  • Thomas, M.K., Murray, R., Flockhart, L., Pintar, K., Pollari, F., Fazil, A., Nesbitt, A. & Marshall, B. (2013). Estimates of the burden of foodborne illness in Canada for 30 specified pathogens and unspecified agents, Circa 2006. Foodborne Pathogens and Disease, 10, 639–648.
  • Thompson, D.R., Parreira, V.R., Kulkarni, R.R. & Prescott, J.F. (2006). Live attenuated vaccine-based control of necrotic enteritis of broiler chickens. Veterinary Microbiology, 113, 25–34. doi: 10.1016/j.vetmic.2005.10.015
  • Tsikrikonis, G., Maniatis, A.N., Labrou, M., Ntokou, E., Michail, G., Daponte, A., Stathopoulos, C., Tsakris, A. & Pournaras S. (2012). Differences in biofilm formation and virulence factors between clinical and fecal enterococcal isolates of human and animal origin. Microbial Pathogenesis, 52, 336–343. doi: 10.1016/j.micpath.2012.03.003
  • Varga, J.J., Therit, B. & Melville, S.B. (2008). Type IV pili and the CcpA protein are needed for maximal biofilm formation by the Gram-positive anaerobic pathogen Clostridium perfringens. Infection and Immunity, 76, 4944–4951. doi: 10.1128/IAI.00692-08
  • Vidal, J.E., Ludewick, H.P., Kunkel, R.M., Zahner, D. & Klugman, K.P. (2011). The LuxS-dependent quorum-sensing system regulates early biofilm formation by Streptococcus pneumoniae strain D39. Infection and Immunity, 79, 4050–4060. doi: 10.1128/IAI.05186-11
  • Wade, B. & Keyburn, A.L. (2015). The true cost of necrotic enteritis. World Poultry.
  • Wang, Y., Yi, L., Wu, Z., Shao, J., Liu, G., Fan, H., Zhang, W. & Lu, C. (2012). Comparative proteomic analysis of Streptococcus suis biofilms and planktonic cells that identified biofilm infection-related immunogenic proteins. PLoS One, 7, e33371. doi: 10.1371/journal.pone.0033371
  • Wijman, J.G., de Leeuw, P.P., Moezelaar, R., Zwietering, M.H. & Abee, T. (2007). Air-liquid interface biofilms of Bacillus cereus: formation, sporulation, and dispersion. Applied and Environmental Microbiology, 73, 1481–1488. doi: 10.1128/AEM.01781-06
  • Xu, L., Li, H., Vuong, C., Vadyvaloo, V., Wang, J., Yao, Y., Otto, M. & Gao, Q.. (2006). Role of the luxS quorum-sensing system in biofilm formation and virulence of Staphylococcus epidermidis. Infection and Immunity, 74, 488–496. doi: 10.1128/IAI.74.1.488-496.2006
  • Yao, Y., Sturdevant, D.E. & Otto, M. (2005). Genomewide analysis of gene expression in Staphylococcus epidermidis biofilms: insights into the pathophysiology of S. epidermidis biofilms and the role of phenol-soluble modulins in formation of biofilms. The Journal of Infectious Diseases, 191, 289–298. doi: 10.1086/426945
  • Zhang, W., Culley, D.E., Nie, L. & Scholten, J.C. (2007). Comparative transcriptome analysis of Desulfovibrio vulgaris grown in planktonic culture and mature biofilm on a steel surface. Applied Microbiology and Biotechnology, 76, 447–457. doi: 10.1007/s00253-007-1014-9

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