Genome evolution and plasticity of serratia marcescens, an important multidrug-resistant nosocomial pathogen

Genome Biology and Evolution

Volumn 6, Issue 8, 2014, Pages 2096-2110

  Iguchi, Atsushi ^a   Nagaya, Yutaka ^b,k   Pradel, Elizabeth ^c,d,l   Ooka, Tadasuke ^e   Ogura, Yoshitoshi ^a,e   Katsura, Keisuke ^a   Kurokawa, Ken ^f   Oshima, Kenshiro ^g   Hattori, Masahira ^g   Parkhill, Julian ^h   Sebaihia, Mohamed ^h   Coulthurst, Sarah J ⁱ   Gotoh, Naomasa ^b   Thomson, Nicholas R ^h,j   Ewbank, Jonathan J ^c,d   Hayashi, Tetsuya ^a,e  

^a UNIVERSITY OF MIYAZAKI   (Japan)

^b KYOTO PHARMACEUTICAL UNIVERSITY   (Japan)

^c CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^d INSERM   (France)

^e UNIVERSITY OF MIYAZAKI   (Japan)

^f TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^g UNIVERSITY OF TOKYO   (Japan)

^h WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

ⁱ UNIVERSITY OF DUNDEE   (United Kingdom)

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

^k EISAI CO LTD   (Japan)

^l INSERM U1019   (France)

more..

Author keywords

Genome plasticity; Multidrug resistance; Serratia marcescens; Virulence

Indexed keywords

ANTIINFECTIVE AGENT;

ANIMAL; BACTERIAL GENOME; DRUG EFFECTS; GENETIC VARIATION; GENETICS; HUMAN; INSECT; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR EVOLUTION; MULTIDRUG RESISTANCE; PATHOGENICITY; SERRATIA INFECTIONS; SERRATIA MARCESCENS;

ANIMALS; ANTI-BACTERIAL AGENTS; DRUG RESISTANCE, MULTIPLE; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENOME, BACTERIAL; HUMANS; INSECTS; SERRATIA INFECTIONS; SERRATIA MARCESCENS;

EID: 84920033476     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evu160     Document Type: Article

References (75)

1. Andrews SC, Robinson AK, Rodriguez-Quinones F. 2003. Bacterial iron homeostasis. FEMS Microbiol Rev. 27:215-237
2. Aoki SK, et al. 2010. A widespread family of polymorphic contact-dependent toxin delivery systems in bacteria. Nature 468:439-442
3. Aucken HM, Pitt TL. 1991. Serological relationships of the O antigens of Klebsiella pneumoniae O5, Escherichia coli O8 and a new O serotype of Serratia marcescens. FEMS Microbiol Lett. 64:93-97
4. Chain PS, et al. 2009. Genomics. Genome project standards in a new era of sequencing. Science 326:236-237
5. Chen J, Kuroda T, Huda MN,Mizushima T, Tsuchiya T. 2003. An RND-type multidrug efflux pump SdeXY from Serratia marcescens. J Antimicrob Chemother. 52:176-179
6. Chen YT, et al. 2007. Sequencing and comparative genomic analysis of pK29, a 269-kilobase conjugative plasmid encoding CMY-8 and CTXM- 3 beta-lactamases in Klebsiella pneumoniae. Antimicrob Agents Chemother. 51:3004-3007
7. Cheng KC, Chuang YC, Wu LT, Huang GC, Yu WL. 2006. Clinical experiences of the infections caused by extended-spectrum beta-lactamase- producing Serratia marcescens at a medical center in Taiwan. Jpn J Infect Dis. 59:147-152
8. Coderch N, et al. 2004. Genetic and structural characterization of the core region of the lipopolysaccharide from Serratia marcescens N28b (serovar O4). J Bacteriol. 186:978-988
9. Coulthurst SJ. 2013. The Type VI secretion system-A widespread and versatile cell targeting system. Res Microbiol. 164:640-654
10. Coulthurst SJ, Williamson NR, Harris AK, Spring DR, Salmond GP. 2006. Metabolic and regulatory engineering of Serratia marcescens: mimicking phage-mediated horizontal acquisition of antibiotic biosynthesis and quorum-sensing capacities. Microbiology 152:1899-1911
11. Cusa E, Obradors N, Baldoma L, Badia J, Aguilar J. 1999. Genetic analysis of a chromosomal region containing genes required for assimilation of allantoin nitrogen and linked glyoxylate metabolism in Escherichia coli. J Bacteriol. 181:7479-7484
12. Eberl L, Christiansen G, Molin S, Givskov M. 1996. Differentiation of Serratia liquefaciens into swarm cells is controlled by the expression of the flhD master operon. J Bacteriol. 178:554-559
13. Eberl L, Winson MK, et al. 1996. Involvement of N-Acyl-L-hormoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Mol Microbiol. 20:127-136
14. English G, et al. 2012. New secreted toxins and immunity proteins encoded within the Type VI secretion system gene cluster of Serratia marcescens. Mol Microbiol. 86:921-936
15. Flyg C, Kenne K, Boman HG. 1980. Insect pathogenic properties of Serratia marcescens: phage-resistant mutants with a decreased resistance to Cecropia immunity and a decreased virulence to Drosophila. J Gen Microbiol. 120:173-181
16. Fritsch MJ, et al. 2013. Proteomic identification of novel secreted antibacterial toxins of the Serratia marcescens type VI secretion system. Mol Cell Proteomics. 12:2735-2749
17. Garvis S, et al. 2009. Caenorhabditis elegans semi-Automated liquid screen reveals a specialized role for the chemotaxis gene cheB2 in Pseudomonas aeruginosa virulence. PLoS Pathog. 5:e1000540
18. Gerc AJ, Song L, Challis GL, Stanley-Wall NR, Coulthurst SJ. 2012. The insect pathogen Serratia marcescens Db10 uses a hybrid nonribosomal peptide synthetase-polyketide synthase to produce the antibiotic althiomycin. PLoS One 7:e44673
19. Goluszko P, NowackiMR. 1989. Extracellular haemolytic activity of Serratia marcescens. FEMS Microbiol Lett. 52:207-211
20. Grijpstra J, Arenas J, Rutten L, Tommassen J. 2013. Autotransporter secretion: varying on a theme. Res Microbiol. 164:562-582
21. Harris AK, et al. 2004. The Serratia gene cluster encoding biosynthesis of the red antibiotic, prodigiosin, shows species- and strain-dependent genome context variation. Microbiology 150:3547-3560
22. Herbert S, et al. 2007. Large outbreak of infection and colonization with gram-negative pathogens carrying the metallo- beta -lactamase gene blaIMP-4 at a 320-bed tertiary hospital in Australia. Infect Control Hosp Epidemiol. 28:98-101
23. Horng YT, et al. 2002. The LuxR family protein SpnR functions as a negative regulator of N-Acylhomoserine lactone-dependent quorum sensing in Serratia marcescens. Mol Microbiol. 45:1655-1671
24. Jacob-Dubuisson F, Guerin J, Baelen S, Clantin B. 2013. Two-partner secretion: As simple as it soundš Res Microbiol. 164:583-595
25. Kanehisa M, Goto S. 2000. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28:27-30
26. Kanonenberg K, Schwarz CK, Schmitt L. 2013. Type I secretion systems-A story of appendices. Res Microbiol. 164:596-604
27. Kim M, Oh H-S, Park S-C, Chun J. 2014. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol. 64:346-351
28. Korner RJ, Nicol A, Reeves DS, MacGowan AP, Hows J. 1994. Ciprofloxacin resistant Serratia marcescens endocarditis as a complication of non-Hodgkin's lymphoma. J Infect. 29:73-76
29. Korotkov KV, Sandkvist M, Hol WG. 2012. The type II secretion system: biogenesis, molecular architecture and mechanism. Nat RevMicrobiol. 10:336-351
30. Kucken D, Feucht H, Kaulfers P. 2000. Association of qacE and qacEDelta1 with multiple resistance to antibiotics and antiseptics in clinical isolates of Gram-negative bacteria. FEMS Microbiol Lett. 183:95-98
31. Kulkarni R, et al. 2009. Roles of putative type II secretion and type IV pilus systems in the virulence of uropathogenic Escherichia coli. PLoS One 4: e4752
32. Kumar A, Worobec EA. 2005. Cloning, sequencing, and characterization of the SdeAB multidrug efflux pump of Serratia marcescens. Antimicrob Agents Chemother. 49:1495-1501
33. Kurz CL, et al. 2003. Virulence factors of the human opportunistic pathogen Serratia marcescens identified by in vivo screening. EMBO J. 22: 1451-1460
34. Kurz CL, Ewbank JJ. 2007. Infection in a dish: high-throughput analyses of bacterial pathogenesis. Curr Opin Microbiol. 10:10-16
35. Labbate M, et al. 2007. Quorum-sensing regulation of adhesion in Serratia marcescens MG1 is surface dependent. J Bacteriol. 189: 2702-2711
36. Letoffe S, Ghigo JM, Wandersman C. 1994. Iron acquisition from heme and hemoglobin by a Serratia marcescens extracellular protein. Proc Natl Acad Sci U S A. 91:9876-9880
37. Li H, Toleman MA, Bennett PM, Jones RN, Walsh TR. 2008. Complete sequence of p07-406, a 24,179-base-pair plasmid harboring the blaVIM-7 metallo-beta-lactamase gene in a Pseudomonas aeruginosa isolate from the United States. Antimicrob Agents Chemother. 52: 3099-3105
38. Lyerly D, Gray L, Kreger A. 1981. Characterization of rabbit corneal damage produced by Serratia keratitis and by a serratia protease. Infect Immun. 33:927-932
39. Lyerly DM, Kreger AS. 1983. Importance of serratia protease in the pathogenesis of experimental Serratia marcescens pneumonia. Infect Immun. 40:113-119
40. Mahlen SD. 2011. Serratia infections: from military experiments to current practice. Clin Microbiol Rev. 24:755-791
41. Maki DG, Hennekens CG, Phillips CW, Shaw WV, Bennett JV. 1973. Nosocomial urinary tract infection with Serratia marcescens: An epidemiologic study. J Infect Dis. 128:579-587
42. Makimura Y, Asai Y, Sugiyama A, Ogawa T. 2007. Chemical structure and immunobiological activity of lipid A from Serratia marcescens LPS. J Med Microbiol. 56:1440-1446
43. Masuda N, et al. 2000. Contribution of the MexX-MexY-OprM efflux system to intrinsic resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 44:2242-2246
44. Matsuo T, et al. 2008. SmdAB, a heterodimeric ABC-Type multidrug efflux pump, in Serratia marcescens. J Bacteriol. 190: 648-654
45. Minato Y, Shahcheraghi F, Ogawa W, Kuroda T, Tsuchiya T. 2008. Functional gene cloning and characterization of the SsmE multidrug efflux pump from Serratia marcescens. Biol Pharm Bull. 31:516-519
46. Muller I, Kube M, Reinhardt R, Jelkmann W, Geider K. 2011. Complete genome sequences of three Erwinia amylovora phages isolated in North America and a bacteriophage induced from an Erwinia tasmaniensis strain. J Bacteriol. 193:795-796
47. Murdoch SL, et al. 2011. The opportunistic pathogen Serratia marcescens utilizes type VI secretion to target bacterial competitors. J Bacteriol. 193:6057-6069
48. Nakamura T, et al. 2002. IMP-1 type metalo-beta-lactamase producing Serratia marcescens strains isolated from blood culture between 1991 to 2000. Kansenshogaku Zasshi 76:246-253
49. Nastro M, et al. 2013. First nosocomial outbreak of VIM-16- producing Serratia marcescens in Argentina. Clin Microbiol Infect. 19:617-619
50. Naumiuk L, et al. 2004. Molecular epidemiology of Serratia marcescens in two hospitals in Gdansk, Poland, over a 5-year period. J ClinMicrobiol. 42:3108-3116
51. Neupane S, et al. 2012. Complete genome sequence of the rapeseed plant-growth promoting Serratia plymuthica strain AS9. Stand Genomic Sci. 6:54-62
52. Okuda T, Endo N, Osada Y, Zen-Yoji H. 1984. Outbreak of nosocomial urinary tract infections caused by Serratiamarcescens. J Clin Microbiol. 20:691-695
53. Osano E, et al. 1994. Molecular characterization of an enterobacterial metallo beta-lactamase found in a clinical isolate of Serratia marcescens that shows imipenem resistance. Antimicrob Agents Chemother. 38:71-78
54. Parment PA, et al. 1992. Hemagglutination (fimbriae) and hydrophobicity in adherence of Serratia marcescens to urinary tract epithelium and contact lenses. Curr Microbiol. 25:113-118
55. Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 8:785-786
56. Petty NK, Foulds IJ, Pradel E, Ewbank JJ, Salmond GP. 2006. A generalized transducing phage (phiIF3) for the genomically sequenced Serratia marcescens strain Db11: A tool for functional genomics of an opportunistic human pathogen. Microbiology 152: 1899-1911
57. Poole SJ, et al. 2011. Identification of functional toxin/immunity genes linked to contact-dependent growth inhibition (CDI) and rearrangement hotspot (Rhs) systems. PLoS Genet. 7: e1002217
58. Pouttu R, et al. 2001. matB, a common fimbrillin gene of Escherichia coli, expressed in a genetically conserved, virulent clonal group. J Bacteriol. 183:4727-4736
59. Pradel E, et al. 2007. Detection and avoidance of a natural product from the pathogenic bacterium Serratia marcescens by Caenorhabditis elegans. Proc Natl Acad Sci U S A. 104:2295-2300
60. RendonMA, et al. 2007. Commensal and pathogenic Escherichia coli use a common pilus adherence factor for epithelial cell colonization. Proc Natl Acad Sci U S A. 104:10637-10642
61. Richter M, Rossello-Mora R. 2009. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A. 106: 19126-19131
62. Sauvonnet N, Gounon P, Pugsley AP. 2000. PpdD type IV pilin of Escherichia coli K-12 can Be assembled into pili in Pseudomonas aeruginosa. J Bacteriol. 182:848-854
63. Shahcheraghi F, et al. 2007. Molecular cloning and characterization of a multidrug efflux pump, SmfY, from Serratia marcescens. Biol Pharm Bull. 30:798-800
64. Shanks RM, et al. 2007. A Serratia marcescens OxyR homolog mediates surface attachment and biofilm formation. J Bacteriol. 189: 7262-7272
65. Shimuta K, et al. 2009. The hemolytic and cytolytic activities of Serratia marcescens phospholipase A (PhlA) depend on lysophospholipid production by PhlA. BMC Microbiol. 9:261
66. Su LH, et al. 2003. Extended epidemic of nosocomial urinary tract infections caused by Serratia marcescens. J Clin Microbiol. 41:4726-4732
67. Sugawara H, Ohyama A, Mori H., Kurokawa K. 2009. Microbial Genome Annotation Pipeline (MiGAP) for diverse users, software demonstration S001-1-2. In: The 20th International Conference on Genome Informatics (Yokohama). Tokyo (Japan): Japanese Society for Bioinformatics
68. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 24:1596-1599
69. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680
70. Thorsted PB, et al. 1998. Complete sequence of the IncPbeta plasmid R751: implications for evolution and organisation of the IncP backbone. J Mol Biol. 282:969-990
71. Wachino J, et al. 2011. SMB-1, a novel subclass B3 metallo-betalactamase, associated with ISCR1 and a class 1 integron, from a carbapenem- resistant Serratia marcescens clinical isolate. Antimicrob Agents Chemother. 55:5143-5149
72. Weigel LM, Steward CD, Tenover FC. 1998. gyrA mutations associated with fluoroquinolone resistance in eight species of Enterobacteriaceae. 42:2661-2667
73. Weise T, et al. 2014. VOC emission of various Serratia species and isolates and genome analysis of Serratia plymuthica 4Rx13. FEMS Microbiol Lett. 352:45-53
74. Xicohtencatl-Cortes J, et al. 2009. The type 4 pili of enterohemorrhagic Escherichia coli O157:H7 are multipurpose structures with pathogenic attributes. J Bacteriol. 191:411-421
75. Yu VL. 1979. Serratiamarcescens: historical perspective and clinical review. N Engl J Med. 300:887-893