An in silico analysis of osmotolerance in the emerging gastrointestinal pathogen Cronobacter sakazakii

Bioengineered Bugs

Volumn 2, Issue 5, 2011, Pages 260-270

  Feeney, Audrey ^a   Sleator, Roy D ^a  

^a Munster Technological University   (Ireland)

Author keywords

Bioinformatics; Cronobacter sakazakiiwhile survivors; Osmolytes; Osmotolerance; Stress

Indexed keywords

BETAINE; CARNITINE; CHOLINE; PROLINE;

BACTERIAL GENE; BACTERIAL GENOME; COMPUTER MODEL; CRONOBACTER SAKAZAKII; ENTEROBACTERIACEAE; ESCHERICHIA COLI; GENE LOCUS; LISTERIA MONOCYTOGENES; NONHUMAN; OSMOTIC STRESS; OSMOTOLERANCE; PHYSICAL TOLERANCE; REGULATORY MECHANISM; REVIEW;

BACTERIAL PROTEINS; CRONOBACTER SAKAZAKII; ENTEROBACTERIACEAE INFECTIONS; FEMALE; GASTROINTESTINAL DISEASES; GENOME, BACTERIAL; GENOMICS; HUMANS; INFANT FORMULA; INFANT, NEWBORN; MALE; MOLECULAR SEQUENCE DATA; OSMOSIS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; LISTERIA MONOCYTOGENES;

EID: 80054949394     PISSN: 19491018     EISSN: 19491026     Source Type: Journal    
DOI: 10.4161/bbug.2.5.17238     Document Type: Review

References (91)

1. Kucerova E, Clifton SW, Xia XQ, Long F, Porwollik S, Fulton L, et al. Genome sequence of Cronobacter sakazakii BAA-894 and comparative genomic hybridization analysis with other Cronobacter species. PLoS ONE 2010; 5:9556.
2. Farmer JJ, III, Asbury MA, Hickman FW, Brenner DJ. The Enterobacteriaceae Study Group. Enterobacter sakazakii: a new species of "Enterobacteriaceae" isolated from clinical specimens. Int J Syst Bacteriol 1980; 30:569-84.
3. Iversen C, Lehner A, Mullane N, Bidlas E, Cleenwerck I, Marugg J, et al. The taxonomy of Enterobacter sakazakii: proposal of a new genus Cronobacter gen. nov. and descriptions of Cronobacter sakazakii comb. nov. Cronobacter sakazakii subsp. sakazakii, comb. nov., Cronobacter sakazakii subsp. malonaticus subsp. nov., Cronobacter turicensis sp. nov., Cronobacter muytjensii sp. nov., Cronobacter dublinensis sp. nov. and Cronobacter genomospecies 1. BMC Evol Biol 2007; 7:64.
4. Nazarowec-White M, Farber JM. Enterobacter sakazakii: a review. Int J Food Microbiol 1997; 34:103-13.
5. van Acker J, de Smet F, Muyldermans G, Bougatef A, Naessens A, Lauwers S. Outbreak of necrotizing enterocolitis associated with Enterobacter sakazakii in powdered milk formula. J Clin Microbiol 2001; 39:293-7.
6. Ray P, Das A, Gautam V, Jain N, Narang A, Sharma M. Enterobacter sakazakii in infants: novel phenomenon in India. Indian J Med Microbiol 2007; 25:408-10.
7. Iversen C, Forsythe S. Risk profile of Enterobacter sakazakii, an emergent pathogen associated with infant milk formula. Trends Food Sci Technol 2003; 14:443-54.
8. Forsythe SJ. Enterobacter sakazakii and other bacteria in powdered infant milk formula. Matern Child Nutr 2005; 1:44-50.
9. Pangalos G. Sur un bacille chromogene isole par hemoculture. Comptes Rendus Seances Soc Biol 1929; 1097.
10. Urmenyi AM, Franklin AW. Neonatal death from pigmented coliform infection. Lancet 1961; 1:313-5.
11. Fiore A, Casale M, Aureli P. Enterobacter sakazakii: epidemiology, clinical presentation, prevention and control. Ann Ist Super Sanita 2008; 44:275-80.
12. Friedemann M. Epidemiology of invasive neonatal Cronobacter (Enterobacter sakazakii) infections. Eur J Clin Microbiol Infect Dis 2009; 28:1297-304.
13. Jaradat Z, Ababneh Q, Saadoun I, Samara N, Rashdan A. Isolation of Cronobacter spp. (formerly Enterobacter sakazakii) from infant food, herbs and environmental samples and the subsequent identification and confirmation of the isolates using biochemical, chromogenic assays, PCR and 16S rRNA sequencing. BMC Microbiol 2009; 9:225.
14. Pagotto FJ, Farber JM, Lenati R. Pathogenicity of Enterobacter sakazakii In Enterobacter sakazakii. ASM Press, Washington, DC 2008.
15. Li Q, Zhao WD, Zhang K, Fang WG, Hu Y, Wu SH, et al. PI3K-dependent host cell actin rearrangements are required for Cronobacter sakazakii invasion of human brain microvascular endothelial cells. Med Microbiol Immunol 2010; 199:333-40.
16. Townsend SM, Hurrell E, Gonzalez-Gomez I, Lowe J, Frye JG, Forsythe S, et al. Enterobacter sakazakii invades brain capillary endothelial cells, persists in human macrophages influencing cytokine secretion and induces severe brain pathology in the neonatal rat. Microbiol 2007; 153:3538-47.
17. Townsend S, Hurrell E, Forsythe S. Virulence studies of Enterobacter sakazakii isolates associated with a neonatal intensive care unit outbreak. BMC Microbiol 2008; 8:64.
18. Pagotto FJ, Nazarowec-White M, Bidawid S, Farber JM. Enterobacter sakazakii: infectivity and enterotoxin production in vitro and in vivo. J Food Prot 2003; 66:370-5.
19. Barron JC, Forsythe SJ. Dry stress and survival time of Enterobacter sakazakii and other Enterobacteriaceae in dehydrated powdered infant formula. J Food Prot 2007; 70:2111-7.
20. Nazarowec-White M, Farber JM. Incidence, survival and growth of Enterobacter sakazakii in infant formula. J Food Prot 1997; 60:226-30.
21. Muytjens HL, Roelofs-Willemse H, Jaspar GH. Quality of powdered substitutes for breast milk with regard to members of the family Enterobacteriaceae. J Clin Microbiol 1988; 26:743-6.
22. Simmons BP, Gelfand MS, Haas M, Metts L, Ferguson J. Enterobacter sakazakii infections in neonates associated with intrinsic contamination of a powdered infant formula. Infect Control Hosp Epidemiol 1989; 10:398-401.
23. Osaili T, Forsythe S. Desiccation resistance and persistence of Cronobacter species in infant formula. Int J Food Microbiol 2009; 136:214-20.
24. Al-Nabulsi AA, Osaili TM, Al-Holy MA, Shaker RR, Ayyash MM, Olaimat AN, et al. Influence of desiccation on the sensitivity of Cronobacter spp. to lactoferrin or nisin in broth and powdered infant formula. Int J Food Microbiol 2009; 136:221-6.
25. Riedel K, Lehner A. Identification of proteins involved in osmotic stress response in Enterobacter sakazakii by proteomics. Proteomics 2007; 7:1217-31.
26. Dancer GI, Mah JH, Rhee MS, Hwang IG, Kang DH. Resistance of Enterobacter sakazakii (Cronobacter spp.) to environmental stresses. J Appl Microbiol 2009; 107:1606-14.
27. Gurtler JB, Kornacki JL, Beuchat LR. Enterobacter sakazakii: a coliform of increased concern to infant health. Int J Food Microbiol 2005; 104:1-34.
28. Himelright IHE, Lorch V, Anderson M. Enterobacter sakazakii infections associated with the use of powdered infant formula-Tennessee 2001. JAMA 2002; 287:2204-5.
29. Grant JR, Stothard P. The CGView Server: a comparative genomics tool for circular genomes. Nucleic Acid Res 2008; 36:181-4.
30. Wood JM, Bremer E, Csonka LN, Kraemer R, Poolman B, van der Heide T, et al. Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comp Biochem Physiol A Mol Integr Physiol 2001; 130:437-60.
31. Gralla JD, Vargas DR. Potassium glutamate as a transcriptional inhibitor during bacterial osmoregulation. EMBO J 2006; 25:1515-21.
32. Sleator RD, Wouters J, Gahan CG, Abee T, Hill C. Analysis of the role of OpuC, an osmolyte transport system, in salt tolerance and virulence potential of Listeria monocytogenes. Appl Environ Microbiol 2001; 67:2692-8.
33. Poolman B, Glaasker E. Regulation of compatible solute accumulation in bacteria. Mol Microbiol 1998; 29:397-407.
34. Bakker EP. pH-dependent transport of rubidium by the constitutive potassium uptake system TrkA of Escherichia coli K-12. FEMS Microbiol Lett 1983; 16:229-33.
35. Dosch DC, Helmer GL, Sutton SH, Salvacion FF, Epstein W. Genetic analysis of potassium transport loci in Escherichia coli: evidence for three constitutive systems mediating uptake potassium. J Bacteriol 1991; 173:687-96.
36. Bossemeyer D, Schlosser A, Bakker EP. Specific cesium transport via the Escherichia coli Kup (TrkD) K+ uptake system. J Bacteriol 1989; 171:2219-21.
37. Schleyer M, Bakker EP. Nucleotide sequence and 3'-end deletion studies indicate that the K(+)-uptake protein kup from Escherichia coli is composed of a hydrophobic core linked to a large and partially essential hydrophilic C terminus. J Bacteriol 1993; 175:6925-31.
38. Schleyer M, Schmid R, Bakker EP. Transient, specific and extremely rapid release of osmolytes from growing cells of Escherichia coli K-12 exposed to hypoosmotic shock. Arch Microbiol 1993; 160:424-31.
39. Trchounian A, Kobayashi H. Kup is the major K+ uptake system in Escherichia coli upon hyper-osmotic stress at a low pH. FEBS Lett 1999; 447:144-8.
40. Roe AJ, McLaggan D, O'Byrne CP, Booth IR. Rapid inactivation of the Escherichia coli Kdp K+ uptake system by high potassium concentrations. Mol Microbiol 2000; 35:1235-43.
41. Sardesai AA, Gowrishankar J. Trans-acting mutations in loci other than kdpDE that affect kdp operon regulation in Escherichia coli: effects of cytoplasmic thiol oxidation status and nucleoid protein H-NS on kdp expression. J Bacteriol 2001; 183:86-93.
42. Polarek JW, Williams G, Epstein W. The products of the kdpDE operon are required for expression of the Kdp ATPase of Escherichia coli. J Bacteriol 1992; 174:2145-51.
43. Voelkner P, Puppe W, Altendorf K. Characterization of the KdpD protein, the sensor kinase of the K+-translocating Kdp system of Escherichia coli. Eur J Biochem 1993; 217:1019-26.
44. Galinski EA. Osmoadaptation in bacteria. In: Poole RK, Ed. Advances in Microbial Physiology: Academic Press 1995; 273-328.
45. Purvis JE, Yomano LP, Ingram LO. Enhanced trehalose production improves growth of Escherichia coli under osmotic stress. Appl Environ Microbiol 2005; 71:3761-9.
46. Perroud B, Le Rudulier D. Glycine betaine transport in Escherichia coli: osmotic modulation. J Bacteriol 1985; 161:393-401.
47. Grothe S, Krogsrud RL, McClellan DJ, Milner JL, Wood JM. Proline transport and osmotic stress response in Escherichia coli K-12. J Bacteriol 1986; 166:253-9.
48. Verheul A, Wouters JA, Rombouts FM, Abee T. A possible role of ProP, ProU and CaiT in osmoprotection of Escherichia coli by carnitine. J Appl Microbiol 1998; 85:1036-46.
49. Wood JM. Proline porters effect the utilization of proline as nutrient or osmoprotectant for bacteria. J Membr Biol 1988; 106:183-202.
50. Barron A, Jung JU, Villarejo M. Purification and characterization of a glycine betaine binding protein from Escherichia coli. J Biol Chem 1987; 262:11841-6.
51. Cairney J, Booth IR, Higgins CF. Osmoregulation of gene expression in Salmonella typhimurium: proU encodes an osmotically induced betaine transport system. J Bacteriol 1985; 164:1224-32.
52. Cairney J, Booth IR, Higgins CF. Salmonella typhimurium proP gene encodes a transport system for the osmoprotectant betaine. J Bacteriol 1985; 164:1218-23.
53. Gowrishankar J. Identification of osmoresponsive genes in Escherichia coli: evidence for participation of potassium and proline transport systems in osmoregulation. J Bacteriol 1985; 164:434-45.
54. Jebbar M, Talibart R, Gloux K, Bernard T, Blanco C. Osmoprotection of Escherichia coli by ectoine: uptake and accumulation characteristics. J Bacteriol 1992; 174:5027-35.
55. Saier MH. Computer-aided analyses of transport protein sequences: gleaning evidence concerning function, structure, biogenesis and evolution. Microbiol Rev 1994; 58:71-93.
56. Culham DE, Lasby B, Marangoni AG, Milner JL, Steer BA, van Nues RW, et al. Isolation and sequencing of Escherichia coli gene proP reveals unusual structural features of the osmoregulatory proline/betaine transporter, ProP. J Mol Biol 1993; 229:268-76.
57. Mellies J, Wise A, Villarejo M. Two different Escherichia coli proP promoters respond to osmotic and growth phase signals. J Bacteriol 1995; 177:144-51.
58. Dunlap VJ, Csonka LN. Osmotic regulation of L-proline transport in Salmonella typhimurium. J Bacteriol 1985; 163:296-304.
59. Chaulk S, Smith-Frieday MN, Arthur DC, Culham DE, Edwards RA, Soo P, et al. ProQ is an RNA chaperone that controls ProP levels in Escherichia coli. Biochemistry 2011; 50:3095-106.
60. Doige CA, Luzzi Ames GF. ATP-dependent transport systems in bacteria and humans: relevance to cystic fibrosis and multidrug resistance. Annu Rev Microbiol 1993; 47:291-319.
61. Gowrishankar J. Nucleotide sequence of the osmoregulatory proU operon of Escherichia coli. J Bacteriol 1989; 171:1923-31.
62. Dattananda CS, Gowrishankar J. Osmoregulation in Escherichia coli: complementation analysis and gene-protein relationships in the proU locus. J Bacteriol 1989; 171:1915-22.
63. Manna D, Gowrishankar J. Evidence for involvement of proteins HU and RpoS in transcription of the osmoresponsive proU operon in Escherichia coli. J Bacteriol 1994; 176:5378-84.
64. Sleator RD, Banville N, Hill C. Carnitine enhances the growth of Listeria monocytogenes in infant formula at 7 degrees C. J Food Prot 2009; 72:1293-5.
65. Lamark T, Kaasen I, Eshoo MW, Falkenberg P, McDougall J, Strøm AR. DNA sequence and analysis of the bet genes encoding the osmoregulatory choline-glycine betaine pathway of Escherichia coli. Mol Microbiol 1991; 5:1049-64.
66. Lamark T, Styrvold OB, Strøm AR. Efflux of choline and glycine betaine from osmoregulating cells of Escherichia coli. FEMS Microbiol Lett 1992; 96:149-54.
67. Landfald B, Strom AR. Choline-glycine betaine pathway confers a high level of osmotic tolerance in Escherichia coli. J Bacteriol 1986; 165:849-55.
68. Lamark T, Rokenes TP, McDougall J, Strom AR. The complex bet promoters of Escherichia coli: regulation by oxygen (ArcA), choline (BetI) and osmotic stress. J Bacteriol 1996; 178:1655-62.
69. Kempf B, Bremer E. Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch Microbiol 1998; 170:319-30.
70. Breeuwer P, Lardeau A, Peterz M, Joosten HM. Desiccation and heat tolerance of Enterobacter sakazakii. J Appl Microbiol 2003; 95:967-73.
71. Strom AR, Kaasen I. Trehalose metabolism in Escherichia coli: stress protection and stress regulation of gene expression. Mol Microbiol 1993; 8:205-10.
72. Kung C, Martinac B, Sukharev S. Mechanosensitive channels in microbes. Annu Rev Microbiol 2010; 64:313-29.
73. Martinac B, Buechner M, Delcour AH, Adler J, Kung C. Pressure-sensitive ion channel in Escherichia coli. PNAS 1987; 84:2297-301.
74. Storz GRHA. Bacterial stress responses. ASM Press, Washington, DC 2000.
75. Schumann U, Edwards MD, Rasmussen T, Bartlett W, van West P, Booth IR. YbdG in Escherichia coli is a threshold-setting mechanosensitive channel with MscM activity. PNAS 2010; 107:12664-9.
76. Glaasker E, Konings W, Poolman B. Osmotic regulation of intracellular solute pools in Lactobacillus plantarum. J Bacteriol 1996; 178:575-82.
77. Ruffert S, Lambert C, Peter H, Wendisch VF, KrÄmer R. Efflux of compatible solutes in Corynebacterium glutamicum mediated by osmoregulated channel activity. Eur J Biochem 1997; 247:572-80.
78. Sleator RD, Hill C. Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol Rev 2002; 26:49-71.
79. Roosild TP, Castronovo S, Healy J, Miller S, Pliotas C, Rasmussen T, et al. Mechanism of ligand-gated potassium efflux in bacterial pathogens. PNAS 2010.
80. Xin L, Su H, Nielsen CH, Tang C, Torres J, Mu Y. Water permeation dynamics of AqpZ: A tale of two states. Biochimica et Biophysica Acta (BBA)-Biomembranes 2011; 1808:1581-6.
81. Hachez C, Chaumont F. Aquaporins: a family of highly regulated multifunctional channels. New York NY, ETATS-UNIS: Springer Science + Business Media 2010.
82. Rychlik I, Barrow PA. Salmonella stress management and its relevance to behaviour during intestinal colonisation and infection. FEMS Microbiol Rev 2005; 29:1021-40.
83. Verheul A, Rombouts F, Beumer R, Abee T. An ATP-dependent L-carnitine transporter in Listeria monocytogenes Scott A is involved in osmoprotection. J Bacteriol 1995; 177:3205-12.
84. Dubnau DA. Translational specificity in Bacillus subtillus In The molecular biology of the bacilli. Academic Press Inc., New York, NY 1985.
85. Ambulos NP Jr, Smith T, Mulbry W, Lovett PS. CUG as a mutant start codon for cat-86 and xylE in Bacillus subtilis. Gene 1990; 94:125-8.
86. Higgins CF. ABC transporters: from microorganisms to man. Annu Rev Cell Biol 1992; 8:67-113.
87. Sleator RD, Gahan CG, Hill C. A postgenomic appraisal of osmotolerance in Listeria monocytogenes. Appl Environ Microbiol 2003; 69:1-9.
88. Sleator RD, Wood JM, Hill C. Transcriptional regulation and posttranslational activity of the betaine transporter BetL in Listeria monocytogenes are controlled by environmental salinity. J Bacteriol 2003; 185:7140-4.
89. Culham DE, Vernikovska Y, Tschowri N, Keates RAB, Wood JM, Boggs JM. Periplasmic loops of osmosensory transporter ProP in Escherichia coli are sensitive to osmolality. Biochemistry 2008; 47:13584-93.
90. Keates RAB, Culham DE, Vernikovska YI, Zuiani AJ, Boggs JM, Wood JM. Transmembrane helix I and periplasmic loop 1 of Escherichia coli ProP are involved in osmosensing and osmoprotectant transport. Biochemistry 2010; 49:8847-56.
91. Sander C, Schneider R. Database of homology-derived protein structures and the structural meaning of sequence alignment. Proteins: Struct, Funct, Bioinf 1991; 9:56-68.