Clinical and genomic analysis of liver abscess-causing Klebsiella pneumoniae identifies new liver abscess-associated virulence genes

Frontiers in Cellular and Infection Microbiology

Volumn 6, Issue NOV, 2016, Pages

  Ye, Meiping ^a   Tu, Jianfei ^b   Jiang, Jianping ^c   Bi, Yingmin ^a   You, Weibo ^b   Zhang, Yanliang ^d   Ren, Jianmin ^b   Zhu, Taohui ^b   Cao, Zhuo ^e   Yu, Zuochun ^b   Shao, Chuxiao ^b   Shen, Zhen ^a   Ding, Baixing ^a   Yuan, Jinyi ^a   Zhao, Xu ^a   Guo, Qinglan ^a   Xu, Xiaogang ^a   Huang, Jinwei ^b   Wang, Minggui ^a  

^a FUDAN UNIVERSITY   (China)

^b LISHUI CENTRAL HOSPITAL   (China)

^c SHANGHAI JIAO TONG UNIVERSITY   (China)

^d NANJING MEDICAL UNIVERSITY   (China)

^e LISHUI PEOPLE S HOSPITAL   (China)

Author keywords

Genome comparative analysis; Hypervirulent Klebsiella pneumoniae; Liver abscess; Plasmid; Virulence

Indexed keywords

AMIKACIN; AZTREONAM; CEFAZOLIN; CEFEPIME; CEFOTETAN; CIPROFLOXACIN; IMIPENEM; LEVOFLOXACIN; PIPERACILLIN PLUS TAZOBACTAM; SULTAMICILLIN; BACTERIAL DNA; VIRULENCE FACTOR;

AMINO ACID SEQUENCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ISOLATION; BLOOD EXAMINATION; COMMUNITY ACQUIRED INFECTION; DIABETES MELLITUS; DIAGNOSTIC PROCEDURE; DNA EXTRACTION; GENOME ANALYSIS; HUMAN; KLEBSIELLA PNEUMONIAE; MINIMUM INHIBITORY CONCENTRATION; MULTILOCUS SEQUENCE TYPING; NUCLEOTIDE SEQUENCE; PHAGOCYTOSIS; PLASMID; POLYMERASE CHAIN REACTION; PULSED FIELD GEL ELECTROPHORESIS; PYOGENIC LIVER ABSCESS; SEQUENCE ANALYSIS; SEROTYPING; STRING TEST; BACTERIAL GENE; BACTERIAL GENOME; BIOLOGY; CHEMISTRY; CHINA; CLASSIFICATION; DNA SEQUENCE; GENETICS; GENOTYPE; ISOLATION AND PURIFICATION; KLEBSIELLA INFECTION; LIVER ABSCESS; MICROBIOLOGY; SEROTYPE;

CHINA; COMPUTATIONAL BIOLOGY; DNA, BACTERIAL; GENES, BACTERIAL; GENOME, BACTERIAL; GENOTYPE; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; LIVER ABSCESS; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SEROGROUP; VIRULENCE FACTORS;

EID: 85006459212     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2016.00165     Document Type: Article

References (56)

1. Alcántar-Curiel, M. D., and Girón, J. A. (2015). Klebsiella pneumoniae and the pyogenic liver abscess: implications and association of the presence of rpmA genes and expression of hypermucoviscosity. Virulence 6, 407-409. doi: 10.1080/21505594.2015.1030101
2. Alikhan, N. F., Petty, N. K., Ben Zakour, N. L., and Beatson, S. A. (2011). BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 12:402. doi: 10.1186/1471-2164-12-402
3. Bankevich, A., Nurk, S., Antipov, D., Gurevich, A. A., Dvorkin, M., Kulikov, A. S., et al. (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455-477. doi: 10.1089/cmb.2012.0021
4. Barton, B. M., Harding, G. P., and Zuccarelli, A. J. (1995). A general method for detecting and sizing large plasmids. Anal. Biochem. 226, 235-240. doi: 10.1006/abio.1995.1220
5. Bialek-Davenet, S., Criscuolo, A., Ailloud, F., Passet, V., Jones, L., Delannoy-Vieillard, A. S., et al. (2014). Genomic definition of hypervirulent and multidrug-resistant Klebsiella pneumoniae clonal groups. Emerging Infect. Dis. 20, 1812-1820. doi: 10.3201/eid2011.140206
6. Brisse, S., Fevre, C., Passet, V., Issenhuth-Jeanjean, S., Tournebize, R., Diancourt, L., et al. (2009). Virulent Clones of Klebsiella pneumoniae: identification and evolutionary scenario based on genomic and phenotypic characterization. PLoS ONE 4:e4982. doi: 10.1371/journal.pone.0004982
7. Chen, Y. T., Chang, H. Y., Lai, Y. C., Pan, C. C., Tsai, S. F., and Peng, H. L. (2004). Sequencing and analysis of the large virulence plasmid pLVPK of Klebsiella pneumoniae CG43. Gene 337, 189-198. doi: 10.1016/j.gene.2004.05.008
8. Cheng, D. L., and Lin, C. L. (1986). Klebsiella pneumoniae liver abscess associated with septic endophthalmitis. Arch. Intern. Med. 146, 1913-1916.
9. Chou, H. C., Lee, C. Z., Ma, L. C., Fang, C. T., Chang, S. C., and Wang, J. T. (2004). Isolation of a chromosomal region of Klebsiella pneumoniae associated with allantoin metabolism and liver infection. Infect. Immun. 72, 3783-3792. doi: 10.1128/IAI.72.7.3783-3792.2004
10. Chung, D. R., Lee, H. R., Lee, S. S., Kim, S. W., Chang, H. H., Jung, S. I., et al. (2008). Evidence for clonal dissemination of the serotype K1 Klebsiella pneumoniae strain causing invasive liver abscesses in Korea. J. Clin. Microbiol. 46, 4061-4063. doi: 10.1128/jcm.01577-08
11. Etienne, K. A., Gillece, J., Hilsabeck, R., Schupp, J. M., Colman, R., Lockhart, S. R., et al. (2012). Whole genome sequence typing to investigate the Apophysomyces outbreak following a tornado in Joplin, Missouri, 2011. PLoS ONE 7:e49989. doi: 10.1371/journal.pone.0049989
12. Galperin, M. Y., Makarova, K. S., Wolf, Y. I., and Koonin, E. V. (2015). Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucleic Acids Res 43, D261-D269. doi: 10.1093/nar/gku1223
13. Gu, D., Guo, M., Yang, M., Zhang, Y., Zhou, X., and Wang, Q. (2016). A sigmaE-mediated temperature gauge controls a switch from LuxR-mediated virulence gene expression to thermal stress adaptation in Vibrio alginolyticus. PLoS Pathog. 12:e1005645. doi: 10.1371/journal.ppat.1005645
14. Gunn, J. S., Belden, W. J., and Miller, S. I. (1998). Identification of PhoP-PhoQ activated genes within a duplicated region of the Salmonella typhimurium chromosome. Microb. Pathog. 25, 77-90. doi: 10.1006/mpat.1998.0217
15. Healy, C., Golby, P., MacHugh, D. E., and Gordon, S. V. (2016). The MarR family transcription factor Rv1404 coordinates adaptation of Mycobacterium tuberculosis to acid stress via controlled expression of Rv1405c, a virulence-associated methyltransferase. Tuberculosis (Edinb.) 97, 154-162. doi: 10.1016/j.tube.2015.10.003
16. Holt, K. E., Wertheim, H., Zadoks, R. N., Baker, S., Whitehouse, C. A., Dance, D., et al. (2015). Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. Proc. Natl. Acad. Sci. U.S.A. 112, E3574-E3581. doi: 10.1073/pnas.1501049112
17. Hsieh, P. F., Lin, T. L., Lee, C. Z., Tsai, S. F., and Wang, J. T. (2008). Serum-induced iron-acquisition systems and TonB contribute to virulence in Klebsiella pneumoniae causing primary pyogenic liver abscess. J. Infect. Dis. 197, 1717-1727. doi: 10.1086/588383
18. Hsu, C. R., Lin, T. L., Chen, Y. C., Chou, H. C., and Wang, J. T. (2011). The role of Klebsiella pneumoniae rmpA in capsular polysaccharide synthesis and virulence revisited. Microbiology 157(Pt 12), 3446-3457. doi: 10.1099/mic.0.050336-0
19. Hu, B. S., Lau, Y. J., Shi, Z. Y., and Lin, Y. H. (1999). Necrotizing fasciitis associated with Klebsiella pneumoniae liver abscess. Clin. Infect. Dis. 29, 1360-1361. doi: 10.1086/313471
20. Hyun, J. I., Kim, Y. J., Jeon, Y. H., Kim, S. I., Park, Y. J., Kang, M. W., et al. (2014). A case of ventriculitis associated with renal abscess caused by Serotype K1 Klebsiella pneumoniae. Infect Chemother 46, 120-124. doi: 10.3947/ic.2014.46.2.120
21. Inouye, M., Dashnow, H., Raven, L. A., Schultz, M. B., Pope, B. J., Tomita, T., et al. (2014). SRST2: rapid genomic surveillance for public health and hospital microbiology labs. Genome Med. 6:90. doi: 10.1186/s13073-014-0090-6
22. Kim, J. H., Yang, W. J., and Kim, T. H. (2014). Klebsiella pneumonia-induced prostate abscess: how to work it up? Can. Urol. Assoc. J. 8, E841-E844. doi: 10.5489/cuaj.2155
23. Lemaitre, C., Bidet, P., Bingen, E., and Bonacorsi, S. (2012). Transcriptional analysis of the Escherichia coli ColV-Ia plasmid pS88 during growth in human serum and urine. BMC Microbiol. 12:115. doi: 10.1186/1471-2180-12-115
24. Li, L. S., and He, N. S. (2001). Interventional Radiology-Non Vascular. Beijing: People's Medical Publishing House.
25. Li, L., Stoeckert, C. J. Jr., and Roos, D. S. (2003). OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178-2189. doi: 10.1101/gr.1224503
26. Lin, J. C., Chang, F. Y., Fung, C. P., Xu, J. Z., Cheng, H. P., Wang, J. J., et al. (2004). High prevalence of phagocytic-resistant capsular serotypes of Klebsiella pneumoniae in liver abscess. Microbes Infect. 6, 1191-1198. doi: 10.1016/j.micinf.2004.06.003
27. Lin, J. C., Koh, T. H., Lee, N., Fung, C. P., Chang, F. Y., Tsai, Y. K., et al. (2014). Genotypes and virulence in serotype K2 Klebsiella pneumoniae from liver abscess and non-infectious carriers in Hong Kong, Singapore and Taiwan. Gut Pathog. 6:21. doi: 10.1186/1757-4749-6-21
28. Liu, Y. M., Li, B. B., Zhang, Y. Y., Zhang, W., Shen, H., Li, H., et al. (2014). Clinical and molecular characteristics of emerging hypervirulent Klebsiella pneumoniae bloodstream infections in mainland China. Antimicrob. Agents Chemother. 58, 5379-5385. doi: 10.1128/aac.02523-14
29. Luo, Y., Wang, Y., Ye, L., and Yang, J. (2014). Molecular epidemiology and virulence factors of pyogenic liver abscess causing Klebsiella pneumoniae in China. Clin. Microbiol. Infect. 20, O818-O824. doi: 10.1111/1469-0691.12664
30. Ma, L. C., Fang, C. T., Lee, C. Z., Shun, C. T., and Wang, J. T. (2005). Genomic heterogeneity in Klebsiella pneumoniae strains is associated with primary pyogenic liver abscess and metastatic infection. J. Infect. Dis. 192, 117-128. doi: 10.1086/430619
31. Merlet, A., Cazanave, C., Dutronc, H., de Barbeyrac, B., Brisse, S., and Dupon, M. (2012). Primary liver abscess due to CC23-K1 virulent clone of Klebsiella pneumoniae in France. Clin. Microbiol. Infect. 18, E338-E339. doi: 10.1111/j.1469-0691.2012.03953.x
32. Mizuta, K., Ohta, M., Mori, M., Hasegawa, T., Nakashima, I., and Kato, N. (1983). Virulence for mice of Klebsiella strains belonging to the O1 group: relationship to their capsular (K) types. Infect. Immun. 40, 56-61.
33. Nassif, X., and Sansonetti, P. J. (1986). Correlation of the virulence of Klebsiella pneumoniae K1 and K2 with the presence of a plasmid encoding aerobactin. Infect. Immun. 54, 603-608.
34. Nassif, X., Fournier, J. M., Arondel, J., and Sansonetti, P. J. (1989). Mucoid phenotype of Klebsiella pneumoniae is a plasmid-encoded virulence factor. Infect. Immun. 57, 546-552.
35. Podschun, R., and Ullmann, U. (1998). Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin. Microbiol. Rev. 11, 589-603.
36. Pomakova, D. K., Hsiao, C. B., Beanan, J. M., Olson, R., MacDonald, U., Keynan, Y., et al. (2012). Clinical and phenotypic differences between classic and hypervirulent Klebsiella pneumonia: an emerging and under-recognized pathogenic variant. Eur. J. Clin. Microbiol. Infect. Dis. 31, 981-989. doi: 10.1007/s10096-011-1396-6
37. Qu, T. T., Zhou, J. C., Jiang, Y., Shi, K. R., Li, B., Shen, P., et al. (2015). Clinical and microbiological characteristics of Klebsiella pneumoniae liver abscess in East China. BMC Infect. Dis. 15:161. doi: 10.1186/s12879-015-0899-7
38. Saccente, M. (1999). Klebsiella pneumoniae liver abscess, endophthalmitis, and meningitis in a man with newly recognized diabetes mellitus. Clin. Infect. Dis. 29, 1570-1571. doi: 10.1086/313539
39. Shang, H., Wang, Y. S., and Shen, Z. Y. (2015). National Guide to Clinical Laboratory Procedures. Beijing: People's Medical Publishing House.
40. Shon, A. S., Bajwa, R. P., and Russo, T. A. (2013). Hypervirulent (hypermucoviscous) Klebsiella pneumoniae: a new and dangerous breed. Virulence 4, 107-118. doi: 10.4161/viru.22718
41. Siu, L. K., Fung, C. P., Chang, F. Y., Lee, N., Yeh, K. M., Koh, T. H., et al. (2011). Molecular typing and virulence analysis of serotype K1 Klebsiella pneumoniae strains isolated from liver abscess patients and stool samples from noninfectious subjects in Hong Kong, Singapore, and Taiwan. J. Clin. Microbiol. 49, 3761-3765. doi: 10.1128/JCM.00977-11
42. Siu, L. K., Yeh, K. M., Lin, J. C., Fung, C. P., and Chang, F. Y. (2012). Klebsiella pneumoniae liver abscess: a new invasive syndrome. Lancet Infect. Dis. 12, 881-887. doi: 10.1016/S1473-3099(12)70205-0
43. Struve, C., Roe, C. C., Stegger, M., Stahlhut, S. G., Hansen, D. S., Engelthaler, D. M., et al. (2015). Mapping the Evolution of Hypervirulent Klebsiella pneumoniae. MBio 6:e00630. doi: 10.1128/mBio.00630-15
44. Tan, T. Y., Cheng, Y., Ong, M., and Ng, L. S. (2014). Performance characteristics and clinical predictive value of the string test for detection of hepato-virulent Klebsiella pneumoniae isolated from blood cultures. Diagn. Microbiol. Infect. Dis. 78, 127-128. doi: 10.1016/j.diagmicrobio.2013.10.014
45. Tang, H. L., Chiang, M. K., Liou, W. J., Chen, Y. T., Peng, H. L., Chiou, C. S., et al. (2010). Correlation between Klebsiella pneumoniae carrying pLVPK-derived loci and abscess formation. Eur. J. Clin. Microbiol. Infect. Dis. 29, 689-698. doi: 10.1007/s10096-010-0915-1
46. Tu, Y. C., Lu, M. C., Chiang, M. K., Huang, S. P., Peng, H. L., Chang, H. Y., et al. (2009). Genetic requirements for Klebsiella pneumoniae-induced liver abscess in an oral infection model. Infect. Immun. 77, 2657-2671. doi: 10.1128/IAI.01523-08
47. Turton, J. F., Perry, C., Elgohari, S., and Hampton, C. V. (2010). PCR characterization and typing of Klebsiella pneumoniae using capsular type-specific, variable number tandem repeat and virulence gene targets. J. Med. Microbiol. 59(Pt 5), 541-547. doi: 10.1099/jmm.0.015198-0
48. Wattam, A. R., Abraham, D., Dalay, O., Disz, T. L., Driscoll, T., Gabbard, J. L., et al. (2014). PATRIC, the bacterial bioinformatics database and analysis resource. Nucleic Acids Res. 42, D581-D591. doi: 10.1093/nar/gkt1099
49. Wu, C. C., Huang, Y. J., Fung, C. P., and Peng, H. L. (2010). Regulation of the Klebsiella pneumoniae Kpc fimbriae by the site-specific recombinase KpcI. Microbiology 156(Pt 7), 1983-1992. doi: 10.1099/mic.0.038158-0
50. Wu, K. M., Li, L. H., Yan, J. J., Tsao, N., Liao, T. L., Tsai, H. C., et al. (2009). Genome sequencing and comparative analysis of Klebsiella pneumoniae NTUH-K2044, a strain causing liver abscess and meningitis. J. Bacteriol. 191, 4492-4501. doi: 10.1128/JB.00315-09
51. Xu, H., Zhao, Y., Qian, G., and Liu, F. (2015). XocR, a LuxR solo required for virulence in Xanthomonas oryzae pv. oryzicola. Front. Cell. Infect. Microbiol. 5:37. doi: 10.3389/fcimb.2015.00037
52. Ye, J., McGinnis, S., and Madden, T. L. (2006). BLAST: improvements for better sequence analysis. Nucleic Acids Res. 34, W6-W9. doi: 10.1093/nar/gkl164
53. Yeh, K. M., Lin, J. C., Yin, F. Y., Fung, C. P., Hung, H. C., Siu, L. K., et al. (2010). Revisiting the importance of virulence determinant magA and its surrounding genes in Klebsiella pneumoniae causing pyogenic liver abscesses: exact role in serotype K1 capsule formation. J. Infect. Dis. 201, 1259-1267. doi: 10.1086/606010
54. Yu, W. L., Ko, W. C., Cheng, K. C., Lee, C. C., Lai, C. C., and Chuang, Y. C. (2008). Comparison of prevalence of virulence factors for Klebsiella pneumoniae liver abscesses between isolates with capsular K1/K2 and non-K1/K2 serotypes. Diagn. Microbiol. Infect. Dis. 62, 1-6. doi: 10.1016/j.diagmicrobio.2008.04.007
55. Zankari, E., Hasman, H., Cosentino, S., Vestergaard, M., Rasmussen, S., Lund, O., et al. (2012). Identification of acquired antimicrobial resistance genes. J. Antimicrob. Chemother. 67, 2640-2644. doi: 10.1093/jac/dks261
56. Zhang, Y., Zhao, C., Wang, Q., Wang, X., Chen, H., Li, H., et al. (2016). High prevalence of hypervirulent Klebsiella pneumoniae infection in China: geographic distribution, clinical characteristics and antimicrobial resistance. Antimicrob. Agents Chemother. 60, 6115-6120. doi: 10.1128/AAC.01127-16