Emergence of host-adapted Salmonella Enteritidis through rapid evolution in an immunocompromised host

Nature Microbiology

Volumn 1, Issue 3, 2016, Pages

  Klemm, Elizabeth J ^a   Gkrania Klotsas, Effrossyni ^b,c   Hadfield, James ^a   Forbester, Jessica L ^a   Harris, Simon R ^a   Hale, Christine ^a   Heath, Jennifer N ^d   Wileman, Thomas ^a   Clare, Simon ^a   Kane, Leanne ^a   Goulding, David ^a   Otto, Thomas D ^a   Kay, Sally ^a   Doffinger, Rainer ^e   Cooke, Fiona J ^e   Carmichael, Andrew ^b   Lever, Andrew M L ^f   Parkhill, Julian ^a   MacLennan, Calman A ^a,d   Kumararatne, Dinakantha ^e   Dougan, Gordon ^a,f   Kingsley, Robert A ^a,g   more..

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b CAMBRIDGE UNIVERSITY HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^e ADDENBROOKE S HOSPITAL   (United Kingdom)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^g NORWICH RESEARCH PARK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 12 RECEPTOR BETA1; PROTEIN MUTS;

ARTICLE; BACTERIAL GENE; BACTERIUM ISOLATE; BIODEGRADATION; GENE MUTATION; GENE TARGETING; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOCOMPROMISED PATIENT; MUTS GENE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PHYLOGENY; PRIORITY JOURNAL; SALMONELLA ENTERICA SEROVAR ENTERITIDIS; SINGLE NUCLEOTIDE POLYMORPHISM; TYPHOID FEVER; ADAPTATION; BACTEREMIA; BACTERIAL GENOME; CLASSIFICATION; DEFICIENCY; GENE DELETION; GENETIC VARIATION; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR EVOLUTION; MUTATION RATE; SALMONELLOSIS; TIME FACTOR; ADULT; CASE REPORT; CHRONIC DISEASE; COMPLICATION; HOST RANGE; IMMUNE DEFICIENCY; MUTATION; PATHOGENICITY; VIRULENCE;

ADAPTATION, BIOLOGICAL; BACTEREMIA; EVOLUTION, MOLECULAR; GENE DELETION; GENETIC VARIATION; GENOME, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOCOMPROMISED HOST; MUTATION RATE; MUTS DNA MISMATCH-BINDING PROTEIN; PHYLOGENY; SALMONELLA ENTERITIDIS; SALMONELLA INFECTIONS; TIME FACTORS; ADAPTATION, PHYSIOLOGICAL; ADULT; CHRONIC DISEASE; HOST SPECIFICITY; IMMUNOLOGIC DEFICIENCY SYNDROMES; INTERLEUKIN-12 RECEPTOR BETA 1 SUBUNIT; MUTATION; VIRULENCE;

EID: 84958186684     PISSN: None     EISSN: 20585276     Source Type: Journal    
DOI: 10.1038/nmicrobiol.2015.23     Document Type: Article

References (35)

1. Baumler, A. & Fang, F. C. Host specificity of bacterial pathogens. Cold Spring Harb. Perspect. Med. 3, a010041 (2013).
2. Parkhill, J. et al. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413, 848-852 (2001).
3. McClelland, M. et al. Comparison of genome degradation in Paratyphi A and Typhi, human-restricted serovars of Salmonella enterica that cause typhoid. Nature Genet. 36, 1268-1274 (2004).
4. Zhou, Z. et al. Transient Darwinian selection in Salmonella enterica serovar Paratyphi A during 450 years of global spread of enteric fever. Proc. Natl Acad. Sci. USA 111, 12199-12204 (2014).
5. Holt, K. E. et al. Pseudogene accumulation in the evolutionary histories of Salmonella enterica serovars Paratyphi A and Typhi. BMC Genomics 10, 36 (2009).
6. Celum, C. L., Chaisson, R. E., Rutherford, G. W., Barnhart, J. L. & Echenberg, D. F. Incidence of salmonellosis in patients with AIDS. J. Infect. Dis. 156, 998-1002 (1987).
7. De Beaucoudrey, L. et al. Revisiting human IL-12Rβ1 deficiency: a survey of 141 patients from 30 countries. Medicine 89, 381-402 (2010).
8. MacLennan, C. et al. Interleukin (IL)-12 and IL-23 are key cytokines for immunity against Salmonella in humans. J. Infect. Dis. 190, 1755-1757 (2004).
9. Altare, F. et al. Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency. Science 280, 1432-1435 (1998).
10. Okoro, C. K. et al. Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa. Nature Genet. 44, 1215-1221 (2012).
11. Mather, A. E. et al. Distinguishable epidemics of multidrug-resistant Salmonella Typhimurium DT104 in different hosts. Science 341, 1514-1517 (2013).
12. Schaaper, R. M. Base selection, proofreading, and mismatch repair during DNA replication in Escherichia coli. J. Biol. Chem. 268, 23762-23765 (1993).
13. Denamur, E. & Matic, I. Evolution of mutation rates in bacteria. Mol. Microbiol. 60, 820-827 (2006).
14. Funchain, P. et al. The consequences of growth of a mutator strain of Escherichia coli as measured by loss of function among multiple gene targets and loss of fitness. Genetics 154, 959-970 (2000).
15. Rocha, E. P. C. et al. Comparisons of dN/dS are time dependent for closely related bacterial genomes. J. Theor. Biol. 239, 226-235 (2006).
16. Kingsley, R. A. et al. Genome and transcriptome adaptation accompanying emergence of the definitive type 2 host-restricted Salmonella enterica serovar Typhimurium pathovar. mBio 4, e00565-13 (2013).
17. Nuccio, S. P. & Baumler, A. J. Comparative analysis of Salmonella genomes identifies a metabolic network for escalating growth in the inflamed gut. mBio 5, e00929-14 (2014).
18. Kingsley, R. A. et al. Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res. 19, 2279-2287 (2009).
19. Gong, J. et al. Spontaneous conversion between mutL and 6 bpΔmutL in Salmonella typhimurium LT7: association with genome diversification and possible roles in bacterial adaptation. Genomics 90, 542-549 (2007).
20. Thomson, N. R. et al. Comparative genome analysis of Salmonella Enteritidis PT4 and Salmonella Gallinarum 287/91 provides insights into evolutionary and host adaptation pathways. Genome Res. 18, 1624-1637 (2008).
21. SMALT v.0.7.4 (TheWellcome Trust Sanger Institute); http://www.sanger.ac.uk/ science/tools/smalt-0
22. Kurtz, S. et al. Versatile and open software for comparing large genomes. Genome Biol. 5, R12 (2004).
23. Kurtz, S. et al. REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res. 29, 4633-4642 (2001).
24. Holt, K. E. et al. High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nature Genet. 40, 987-993 (2008).
25. He, M. et al. Evolutionary dynamics of Clostridium difficile over short and long time scales. Proc. Natl Acad. Sci. USA 107, 7527-7532 (2010).
26. Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688-2690 (2006).
27. Zerbino, D. & Birney, E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821-829 (2008).
28. BEAST v.1.7.5 (University of Edinburgh); http://beast.bio.ed.ac.uk/
29. BEAGLE v.4 (University of Washington); https://faculty.washington.edu/ browning/beagle/b3.html
30. HGAP v.3.0 (PacBio); https://github.com/PacificBiosciences/Bioinformatics-Training/wiki/HGAP
31. Otto, T. D., Dillon, G. P., Degrave,W. S. & Berriman, M. RATT: rapid annotation transfer tool. Nucleic Acids Res. 39, e57 (2011).
32. Carver, T. J. et al. ACT: the Artemis comparison tool. Bioinformatics 21, 3422-3423 (2005).
33. Alexa, A. & Rahnenfuhrer, J. R package version 2.20.0, topGO: Enrichment analysis for Gene Ontology (2010).
34. Huntley, R. P. et al. The GOA database: Gene Ontology annotation updates for 2015. Nucleic Acids Res. 43, D1057-D1063 (2015).
35. Tsai, C. M. & Frasch, C. E. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal. Biochem. 119, 115-119 (1982).