Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 27, 2015, Pages E3574-E3581

  Holt, Kathryn E ^a,b   Wertheim, Heiman ^c,d   Zadoks, Ruth N ^e,f   Baker, Stephen ^c   Whitehouse, Chris A ^g   Dance, David ^d,h   Jenney, Adam ^b,i   Connor, Thomas R ^j,k   Hsu, Li Yang ^l   Severin, Juliëtte ^m   Brisse, Sylvain ⁿ   Cao, Hanwei ^b   Wilksch, Jonathan ^b   Gorrie, Claire ^a,b   Schultz, Mark B ^a   Edwards, David J ^a   Van Nguyen, Kinh ^o   Nguyen, Trung Vu ^o   Dao, Trinh Tuyet ^o   Mensink, Martijn ^e   Le Minh, Vien ^c,p   Nhu, Nguyen Thi Khanh ^c,q   Schultsz, Constance ^c,r   Kuntaman, Kuntaman ^s   Newton, Paul N ^d,h   Moore, Catrin E ^d,h   Strugnell, Richard A ^b   Thomson, Nicholas R ^j,t   more..

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c OXFORD UNIVERSITY CLINICAL RESEARCH UNIT   (Viet Nam)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e Department of Obstetrics Gynecology   (United States)

^f UNIVERSITY OF GLASGOW   (United Kingdom)

^g UNITED STATES ARMY MEDICAL RESEARCH INSTITUTE OF INFECTIOUS DISEASES   (United States)

^h MAHOSOT HOSPITAL   (Laos)

ⁱ ALFRED HOSPITAL   (Australia)

^j WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^k CARDIFF UNIVERSITY   (United Kingdom)

^l NATIONAL UNIVERSITY HEALTH SYSTEM   (Singapore)

^m ERASMUS MEDICAL CENTER   (Netherlands)

ⁿ CNRS   (France)

^o NATIONAL HOSPITAL FOR TROPICAL DISEASES   (Viet Nam)

^p UNIVERSITY OF CALIFORNIA   (United States)

^q UNIVERSITY OF QUEENSLAND   (Australia)

^r UNIVERSITY OF AMSTERDAM   (Netherlands)

^s AIRLANGGA UNIVERSITY   (Indonesia)

^t LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

more..

Author keywords

Antimicrobial resistance; Genomics; Klebsiella pneumoniae; Population structure; Virulence

Indexed keywords

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CONTROLLED STUDY; COW; GENE SEQUENCE; GENOME ANALYSIS; KLEBSIELLA; KLEBSIELLA PNEUMONIAE; KLEBSIELLA QUASIPNEUMONIAE; KLEBSIELLA VARIICOLA; MASTITIS; MICROBIAL DIVERSITY; NONHUMAN; POPULATION STRUCTURE; PRIORITY JOURNAL; PUBLIC HEALTH; ANIMAL; BACTERIAL GENE; BACTERIAL GENOME; CLASSIFICATION; CROSS INFECTION; DNA SEQUENCE; GENETIC VARIABILITY; GENETICS; GENOMICS; HUMAN; KLEBSIELLA INFECTION; MICROBIOLOGY; MULTIDRUG RESISTANCE; PATHOGENICITY; PHYLOGENY; POPULATION DYNAMICS; PROCEDURES; SPECIES DIFFERENCE; STATISTICS AND NUMERICAL DATA; TRENDS; VIRULENCE;

ANIMALIA; KLEBSIELLA PNEUMONIAE;

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN;

ANIMALS; ANTI-INFECTIVE AGENTS; BACTERIAL PROTEINS; CROSS INFECTION; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENES, BACTERIAL; GENETIC VARIATION; GENOME, BACTERIAL; GENOMICS; HUMANS; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; PHYLOGENY; POPULATION DYNAMICS; PUBLIC HEALTH; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; VIRULENCE;

EID: 84936803320     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1501049112     Document Type: Article

References (71)

1. Jones RN (2010) Microbial etiologies of hospital-acquired bacterial pneumonia and ventilator-associated bacterial pneumonia. Clin Infect Dis 51(Suppl 1):S81-S87.
2. Falade AG, Ayede AI (2011) Epidemiology, aetiology and management of childhood acute community-acquired pneumonia in developing countries-a review. Afr J Med Med Sci 40(4):293-308.
3. Jarvis WR, Munn VP, Highsmith AK, Culver DH, Hughes JM (1985) The epidemiology of nosocomial infections caused by Klebsiella pneumoniae. Infect Control 6(2):68-74.
4. Podschun R, Ullmann U (1998) Klebsiella spp. as nosocomial pathogens: Epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin Microbiol Rev 11(4): 589-603.
5. Brisse S, Grimont F, Grimont P (2006) The genus Klebsiella. The Prokaryotes A Handbook on the Biology of Bacteria, 3rd edition, eds Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (Springer, New York), 3rd Ed. Vol 6: Proteobacteria: Gamma Subclass.
6. Shon AS, Bajwa RP, Russo TA (2013) Hypervirulent (hypermucoviscous) Klebsiella pneumoniae: A new and dangerous breed. Virulence 4(2):107-118.
7. Broberg CA, Palacios M, Miller VL (2014) Klebsiella: A long way to go towards understanding this enigmatic jet-setter. F1000Prime Rep 6:64-76.
8. Jang S, et al. (2010) Pleuritis and suppurative pneumonia associated with a hypermucoviscosity phenotype of Klebsiella pneumoniae in California sea lions (Zalophus californianus). Vet Microbiol 141(1-2):174-177.
9. Twenhafel NA, et al. (2008) Multisystemic abscesses in African green monkeys (Chlorocebus aethiops) with invasive Klebsiella pneumoniae-identification of the hypermucoviscosity phenotype. Vet Pathol 45(2):226-231.
10. Schukken Y, et al. (2012) The "other" gram-negative bacteria in mastitis: Klebsiella, serratia, and more. Vet Clin North Am Food Anim Pract 28(2):239-256.
11. Bagley ST (1985) Habitat association of Klebsiella species. Infect Control 6(2):52-58.
12. Bialek-Davenet S, et al. (2014) Genomic definition of hypervirulent and multidrugresistant Klebsiella pneumoniae clonal groups. Emerg Infect Dis 20(11):1812-1820.
13. Brisse S, et al. (2009) Virulent clones of Klebsiella pneumoniae: Identification and evolutionary scenario based on genomic and phenotypic characterization. PLoS ONE 4(3):e4982.
14. Struve C, Krogfelt KA (2004) Pathogenic potential of environmental Klebsiella pneumoniae isolates. Environ Microbiol 6(6):584-590.
15. Brisse S, Verhoef J (2001) Phylogenetic diversity of Klebsiella pneumoniae and Klebsiella oxytoca clinical isolates revealed by randomly amplified polymorphic DNA, gyrA and parC genes sequencing and automated ribotyping. Int J Syst Evol Microbiol 51(Pt 3):915-924.
16. Fevre C, Passet V, Weill FX, Grimont PA, Brisse S (2005) Variants of the Klebsiella pneumoniae OKP chromosomal beta-lactamase are divided into two main groups, OKP-A and OKP-B. Antimicrob Agents Chemother 49(12):5149-5152.
17. Brisse S, Passet V, Grimont PA (2014) Description of Klebsiella quasipneumoniae sp. nov., isolated from human infections, with two subspecies, Klebsiella quasipneumoniae subsp. quasipneumoniae subsp. nov. and Klebsiella quasipneumoniae subsp. similipneumoniae subsp. nov., and demonstration that Klebsiella singaporensis is a junior heterotypic synonym of Klebsiella variicola. Int J Syst Evol Microbiol 64(Pt 9):3146-3152.
18. Rosenblueth M, Martínez L, Silva J, Martínez-Romero E (2004) Klebsiella variicola, a novel species with clinical and plant-associated isolates. Syst Appl Microbiol 27(1):27-35.
19. Maatallah M, et al. (2014) Klebsiella variicola is a frequent cause of bloodstream infection in the stockholm area, and associated with higher mortality compared to K. pneumoniae. PLoS ONE 9(11):e113539.
20. Centers for Disease Control and Prevention (2013) Antibiotic Resistance Threats in the United States, 2013 (Centers Dis Control, Atlanta).
21. Department of Health and Department for Environment Food & Rural Affairs (2013) UK Five Year Antimicrobial Resistance Strategy 2013 to 2018. (Department of Health, London).
22. Chaves J, et al. (2001) SHV-1 beta-lactamase is mainly a chromosomally encoded species-specific enzyme in Klebsiella pneumoniae. Antimicrob Agents Chemother 45(10):2856-2861.
23. Sirot J, et al. (1988) Klebsiella pneumoniae and other Enterobacteriaceae producing novel plasmid-mediated beta-lactamases markedly active against third-generation cephalosporins: Epidemiologic studies. Rev Infect Dis 10(4):850-859.
24. Nordmann P, Cuzon G, Naas T (2009) The real threat of Klebsiella pneumoniae carbapenemase- producing bacteria. Lancet Infect Dis 9(4):228-236.
25. Nordmann P, Poirel L, Walsh TR, Livermore DM (2011) The emerging NDM carbapenemases. Trends Microbiol 19(12):588-595.
26. Chen L, et al. (2014) Carbapenemase-producing Klebsiella pneumoniae: Molecular and genetic decoding. Trends Microbiol 22(12):686-696.
27. Snitkin ES, et al. (2012) Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci Transl Med 4(148):148ra116.
28. Wright MS, et al. (2014) Population structure of KPC-producing Klebsiella pneumoniae isolates frommidwestern U.S. hospitals. Antimicrob Agents Chemother 58(8):4961-4965.
29. Chen L, Mathema B, Pitout JD, DeLeo FR, Kreiswirth BN (2014) Epidemic Klebsiella pneumoniae ST258 is a hybrid strain. MBio 5(3):e01355-14.
30. Deleo FR, et al. (2014) Molecular dissection of the evolution of carbapenem-resistant multilocus sequence type 258 Klebsiella pneumoniae. Proc Natl Acad Sci USA 111(13): 4988-4993.
31. Mathers AJ, et al. (2015) Klebsiella pneumoniae carbapenemase (KPC)-producing K. pneumoniae at a single institution: Insights into endemicity from whole-genome sequencing. Antimicrob Agents Chemother 59(3):1656-1663.
32. Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106(45):19126-19131.
33. Sheppard SK, McCarthy ND, Falush D, Maiden MC (2008) Convergence of Campylobacter species: Implications for bacterial evolution. Science 320(5873):237-239.
34. de Melo ME, Cabral AB, Maciel MA, da Silveira VM, de Souza Lopes AC (2011) Phylogenetic groups among Klebsiella pneumoniae isolates from Brazil: Relationship with antimicrobial resistance and origin. Curr Microbiol 62(5):1596-1601.
35. Brisse S, van Himbergen T, Kusters K, Verhoef J (2004) Development of a rapid identification method for Klebsiella pneumoniae phylogenetic groups and analysis of 420 clinical isolates. Clin Microbiol Infect 10(10):942-945.
36. Fouts DE, et al. (2008) Complete genome sequence of the N2-fixing broad host range endophyte Klebsiella pneumoniae 342 and virulence predictions verified in mice. PLoS Genet 4(7):e1000141.
37. Pinto-Tomás AA, et al. (2009) Symbiotic nitrogen fixation in the fungus gardens of leaf-cutter ants. Science 326(5956):1120-1123.
38. Pommier T, Canbäck B, Lundberg P, Hagström A, Tunlid A (2009) RAMI: A tool for identification and characterization of phylogenetic clusters in microbial communities. Bioinformatics 25(6):736-742.
39. Lawson DJ, Hellenthal G, Myers S, Falush D (2012) Inference of population structure using dense haplotype data. PLoS Genet 8(1):e1002453.
40. Carniel E (2001) The Yersinia high-pathogenicity island: An iron-uptake island. Microbes Infect 3(7):561-569.
41. Nassif X, Sansonetti PJ (1986) Correlation of the virulence of Klebsiella pneumoniae K1 and K2 with the presence of a plasmid encoding aerobactin. Infect Immun 54(3):603-608.
42. Putze J, et al. (2009) Genetic structure and distribution of the colibactin genomic island among members of the family Enterobacteriaceae. Infect Immun 77(11):4696-4703.
43. Chen YT, et al. (2004) Sequencing and analysis of the large virulence plasmid pLVPK of Klebsiella pneumoniae CG43. Gene 337:189-198.
44. Lagos R, et al. (2001) Structure, organization and characterization of the gene cluster involved in the production of microcin E492, a channel-forming bacteriocin. Mol Microbiol 42(1):229-243.
45. Cheng HY, et al. (2010) RmpA regulation of capsular polysaccharide biosynthesis in Klebsiella pneumoniae CG43. J Bacteriol 192(12):3144-3158.
46. Lai YC, Peng HL, Chang HY (2003) RmpA2, an activator of capsule biosynthesis in Klebsiella pneumoniae CG43, regulates K2 cps gene expression at the transcriptional level. J Bacteriol 185(3):788-800.
47. Chou HC, et al. (2004) Isolation of a chromosomal region of Klebsiella pneumoniae associated with allantoin metabolism and liver infection. Infect Immun 72(7): 3783-3792.
48. Ma LC, Fang CT, Lee CZ, Shun CT, Wang JT (2005) Genomic heterogeneity in Klebsiella pneumoniae strains is associated with primary pyogenic liver abscess and metastatic infection. J Infect Dis 192(1):117-128.
49. Lai YC, Lin GT, Yang SL, Chang HY, Peng HL (2003) Identification and characterization of KvgAS, a two-component system in Klebsiella pneumoniae CG43. FEMS Microbiol Lett 218(1):121-126.
50. Wu KM, et al. (2009) Genome sequencing and comparative analysis of Klebsiella pneumoniae NTUH-K2044, a strain causing liver abscess and meningitis. J Bacteriol 191(14):4492-4501.
51. Holden VI, Bachman MA (2015) Diverging roles of bacterial siderophores during infection. Metallomics, 10.1039/c4mt00333k.
52. Croucher NJ, et al. (2013) Population genomics of post-vaccine changes in pneumococcal epidemiology. Nat Genet 45(6):656-663.
53. Ibarz-Pavón AB, et al. (2011) Changes in serogroup and genotype prevalence among carried meningococci in the United Kingdom during vaccine implementation. J Infect Dis 204(7):1046-1053.
54. Turton JF, et al. (2007) Genetically similar isolates of Klebsiella pneumoniae serotype K1 causing liver abscesses in three continents. J Med Microbiol 56(Pt 5):593-597.
55. Liao CH, Huang YT, Chang CY, Hsu HS, Hsueh PR (2014) Capsular serotypes and multilocus sequence types of bacteremic Klebsiella pneumoniae isolates associated with different types of infections. Eur J Clin Microbiol Infect Dis 33(3):365-369.
56. Siu LK, 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(11): 3761-3765.
57. Yu WL, et al. (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):1-6.
58. Richards VP, et al. (2011) Comparative genomics and the role of lateral gene transfer in the evolution of bovine adapted Streptococcus agalactiae. Infect Genet Evol 11(6): 1263-1275.
59. Carattoli A, et al. (2014) In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 58(7): 3895-3903.
60. Bachman MA, Lenio S, Schmidt L, Oyler JE, Weiser JN (2012) Interaction of lipocalin 2, transferrin, and siderophores determines the replicative niche of Klebsiella pneumoniae during pneumonia. MBio 3(6):e00224-11.
61. Shin J, Soo Ko K (2014) Single origin of three plasmids bearing blaCTX-M-15 from different Klebsiella pneumoniae clones. J Antimicrob Chemother 69(4):969-972.
62. Liu YM, et al. (2014) Clinical and molecular characteristics of emerging hypervirulent Klebsiella pneumoniae bloodstream infections in mainland China. Antimicrob Agents Chemother 58(9):5379-5385.
63. Cejas D, et al. (2014) First isolate of KPC-2-producing Klebsiella pneumonaie sequence type 23 from the Americas. J Clin Microbiol 52(9):3483-3485.
64. Conlan S, et al. (2014) Single-molecule sequencing to track plasmid diversity of hospital- associated carbapenemase-producing Enterobacteriaceae. Sci Transl Med 6(254): 254ra126.
65. Gaiarsa S, et al. (2014) Genomic epidemiology of Klebsiella pneumoniae: The Italian scenario, and novel insights into the origin and global evolution of resistance to carbapenem antibiotics. Antimicrob Agents Chemother 59(1):389-396.
66. Köser CU, Ellington MJ, Peacock SJ (2014) Whole-genome sequencing to control antimicrobial resistance. Trends Genet 30(9):401-407.
67. Stoesser N, et al. (2014) Genome sequencing of an extended series of NDM-producing Klebsiella pneumoniae isolates from neonatal infections in a Nepali hospital characterizes the extent of community- versus hospital-associated transmission in an endemic setting. Antimicrob Agents Chemother 58(12):7347-7357.
68. Inouye M, et al. (2014) SRST2: Rapid genomic surveillance for public health and hospital microbiology labs. Genome Med 6(11):90-106.
69. Meyer F, et al. (2008) The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9: 386-396.
70. Gupta SK, et al. (2014) ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother 58(1):212-220.
71. Brisse S, et al. (2013) wzi Gene sequencing, a rapid method for determination of capsular type for Klebsiella strains. J Clin Microbiol 51(12):4073-4078.