Abstract
A collection of 70 Burkholderia cepacia complex isolates, recovered from clinical, water, and agricultural resources in China in our previous studies, were tested to assess their potential pathogenicity and association of biofilm formation with pathogenicity. The pathogenicity was tested in the alternative infection models alfalfa, detached lettuce midrib, Galleria mellonella (wax moth), rat agar bead, and lettuce intact leaves. Severe to moderate pathogenicity were observed for isolates of clinical and water origin compared to agricultural isolates, with the exception of a few clinical isolates exhibiting reduced pathogenicity. Virulent isolates persisted in rat lungs until 21 days post infection causing histopathological changes like inflammation, while in lettuce midrib tissues invasion, localization, and replication of bacteria were observed. Biofilm formation ability was also documented in high frequency among water and clinical virulent isolates compared to agricultural isolates. Although variations in pathogenicity were observed for a few isolates, results obtained from different model systems including lettuce were consistent. Our studies indicate that water and clinical isolates showed severe virulence and strong biofilm formation ability compared to agricultural isolates. The results also show lettuce as a promising infection model not only to study the pathogenicity factors used by Bcc bacteria but also for characterization the in vivo transcriptional profile for different niches adaptation of this opportunistic pathogen.
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Bernier SP, Silo-Suh L, Woods DE, Ohman DE, Sokol PA (2003) Comparative analysis of plant and animal models for characterization of Burkholdetia cepacia virulence. Infect Immun 71(9):5306–5313. doi:10.1128/iai.71.9.5306-5313.2003
Bielecki P, Puchałka J, Wos-Oxley ML, Loessner H, Glik J et al (2011) In vivo expression profiling of Pseudomonas aeruginosa infections reveals niche-specific and strain-independent transcriptional programs. PLoS ONE 6(9):e24235. doi:10.1371/journal.pone.0024235
Cash HA, Woods DE, McCullough B, Johanson WG Jr, Bass JA (1979) A rat model of chronic respiratory infection with Pseudomonas aeruginosa. Am Rev Respir Dis 119:453–459
Castonguay-Vanier J, Vial L, Tremblay J, Deziel E (2010) Drosophila melanogaster as a model host for the Burkholderia cepacia complex. PLoS One 5(7). doi:10.1371/journal.pone.0011467
Coenye T, Vandamme P (2003) Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol 5:719–729. doi:10.1046/j.1462-2920.2003.00471.x
Conway B-D, Venu V, Speert DP (2002) Biofilm formation and acyl homoserine lactone production in the Burkholderia cepacia complex. J Bacteriol 184:5678–5685
Corbett CR, Burtnick MN, Kooi C, Woods DE, Sokol PA (2003) An extracellular zinc metalloprotease gene of Burkholderia cepacia. Microbiology 149:2263–2271. doi:10.1099/mic.0.26243-0
Cunha MV, Sousa SA, Leitão JH, Moreira LM, Videira PA, Sá-Correia I (2004) Studies on the involvement of the exopolysaccharide produced by cystic fibrosis-associated isolates of the Burkholderia cepacia complex in biofilm formation and in persistence of respiratory infections. J Clin Microbiol 42:3052–3058
Fang Y, Lou MM, Li B, Xie GL, Wang F, Zhang LX, Luo YC (2010) Characterization of Burkholderia cepacia complex from cystic fibrosis patients in China and their chitosan susceptibility. World J Microbiol Biotechnol 26:443–450. doi:10.1007/s11274-009-0187-z
Fang Y, Xie GL, Lou MM, Li B, Ibrahim M (2011) Diversity analysis of Burkholderia cepacia complex in the water bodies of West Lake, Hangzhou, China. J Microbiol 49:309–314. doi:10.1007/s12275-011-0267-2
Govan JRW, Hughes JE, Vandamme P (1996) Burkholderia cepacia: medical, taxonomic and ecological issues. J Med Microbiol 45:395–407
Ibrahim M, He L, Lou MM, Bo Z, Li B, Xie GL, Zhang G (2011) Prevalence of potential pathogenicity and molecular characterizations of Burkhoderia cepacia complex (BCC) among isolates from bamboo rhizosphere in China. Res J Chem Environ 15:998–1005
Johnston RB Jr (2001) Clinical aspects of chronic granulomatous disease. Curr Opin Hematol 8:17–22
Li B, Fang Y, Zhang GQ, Yu RR, Lou MM, Xie GL, Wang YL, Sun GC (2010) Molecular characterization of Burkholderia cepacia complex isolates causing bacterial fruit rot of apricot. Plant Pathol J 26:223–230
Li B, Liu BP, Yu RR, Lou MM, Wang YL, Xie GL, Li HY, Sun GC (2011) Phenotypic and molecular characterization of rhizobacterium Burkholderia sp. strain R456 antagonistic to Rhizoctonia solani, sheath blight of rice. World J Microbiol Biotechnol 27:2305–2313
Lin L, Duo SS, Bao WY, Lin SE (2007) Analysis of outbreak of nosocomial bloodstream infection with Burkholderia cepacia by recA-RFLP. Chin J Infect Control 6:219–223
Lou M, Fang Y, Zhang G, Xie GL, Zhu B, Ibrahim M (2010) Diversity of Burkholderia cepacia complex from the moso bamboo (Phyllostachys edulis) rhizosphere soil. Curr Microbiol 62:650–658
Lou MM, Zhang LX, Su T, Xie GL (2007) Genomovars of Burkholderia cepacia complex from rice rhizosphere and clinic in China. Rice Sci 14:229–234
Loutet SA, Valvano MA (2010) A decade of Burkholderia cenocepacia virulence determinant research. Infect Immun 78(10):4088–4100. doi:10.1128/iai.00212-10
Mahenthiralingam E, Urban TA, Goldberg JB (2005) The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3:144–156. doi:10.1038/nrmicro1085
Miche L, Faure D, Blot M, Cabanne-Giuli E, Balandreau J (2001) Detection and activity of insertion sequences in environmental strains of Burkholderia. Environ Microbiol 3:766–773
Neely MN, Caparon M (2002) Streptococcus-zebrafish model of bacterial pathogenesis. Infect Immun 70:3904–3914
O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79
Petrova OE, Sauer K (2010) The novel two-component regulatory system BfiSR regulates biofilm development by controlling the small RNA rsmZ through CafA. J Bacteriol 192:5275–5288. doi:10.1128/jb.00387-10
Pirone L, Chiarini L, Dalmastri C, Bevivino A, Tabacchioni S (2005) Detection of cultured and uncultured Burkholderia cepacia complex bacteria naturally occurring in the maize rhizosphere. Environ Microbiol 7:1734–1742. doi:10.1111/j.1462-2920.2005.00897.x
Rahme LG, Ausubel FM, Cao H, Drenkard E, Goumnerov BC, Lau GW, Mahajan-Miklos S, Plotnikova J, Tan MW, Tsongalis J, Walendziewicz CL, Tompkins RG (2000) Plants and animals share functionally common bacterial virulence factors. Proc Natl Acad Sci 97:8815–8821
Seed KD, Dennis JJ (2008) Development of Galleria mellonella as an alternative infection model for the Burkholderia cepacia complex. Infect Immun 76:1267–1275. doi:10.1128/iai.01249-07
Sharan R, Chhibber S (2009) Alfalfa infection model: is it a potential alternative for mouse pneumonia model to study pathogenesis of Stenotrophomonas maltophilia? World J Microbiol Biotechnol 25:1609–1614. doi:10.1007/s11274-009-0052-0
Sousa SA, Ramos CG, Leitão JH (2011) Burkholderia cepacia complex: emerging multihost pathogens equipped with a wide range of virulence factors and determinants. Int J Microbiol 2011. Article ID 607575
Starkey M, Rahme LG (2009) Modeling Pseudomonas aeruginosa pathogenesis in plant hosts. Nat Protoc 4:117–124. doi:10.1038/nprot.2008.224
Vial L, Groleau MC, Lamarche MG, Filion G, Castonguay-Vanier J, Dekimpe V, Daigle F, Charette SJ, Deziel E (2010) Phase variation has a role in Burkholderia ambifaria niche adaptation. ISME J 4:49–60. doi:10.1038/ismej.2009.95
Yoder-Himes DR, Chain PSG, Zhu Y, Wurtzel O, Rubin EM, Tiedje JM, Sorek R (2009) Mapping the Burkholderia cenocepacia niche response via high-throughput sequencing. Proc Natl Acad Sci USA 106:3976–3981. doi:10.1073/pnas.0813403106
Acknowledgments
This project was supported by the Special Fund for Agro-scientific Research in the Public Interest (201003029, 201003066) and National Natural Science Foundation of China (30871655). We are thankful to Dr. Cui (Hangzhou Red Cross Hospital) for his technical assistance for animal study and rat lungs analysis and Dr. Jianshun Chen, Institute of Preventive Veterinary Medicine, Zhejiang University, China for providing technical assistance for animal experiments.
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Ibrahim, M., Tang, Q., Shi, Y. et al. Diversity of potential pathogenicity and biofilm formation among Burkholderia cepacia complex water, clinical, and agricultural isolates in China. World J Microbiol Biotechnol 28, 2113–2123 (2012). https://doi.org/10.1007/s11274-012-1016-3
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DOI: https://doi.org/10.1007/s11274-012-1016-3