title: Cryptic lineages of the genus Escherichia.
abstract: Extended multilocus sequence typing (MLST) analysis of atypical Escherichia isolates was used to identify five novel phylogenetic clades (CI to CV) among isolates from environmental, human, and animal sources. Analysis of individual housekeeping loci showed that E. coli and its sister clade, CI, remain largely indistinguishable and represent nascent evolutionary lineages. Conversely, clades of similar age (CIII and CIV) were found to be phylogenetically distinct. When all Escherichia lineages (named and unnamed) were evaluated, we found evidence that Escherichia fergusonii has evolved at an accelerated rate compared to E. coli, CI, CIII, CIV, and CV, suggesting that this species is younger than estimated by the molecular clock method. Although the five novel clades were phylogenetically distinct, we were unable to identify a discriminating biochemical marker for all but one of them (CIII) with traditional phenotypic profiling. CIII had a statistically different phenotype from E. coli that resulted from the loss of sucrose and sorbitol fermentation and lysine utilization. The lack of phenotypic distinction has likely hindered the ability to differentiate these clades from typical E. coli, and so their ecological significance and importance for applied and clinical microbiology are yet to be determined. However, our sampling suggests that CIII, CIV, and CV represent environmentally adapted Escherichia lineages that may be more abundant outside the host gastrointestinal tract.
authors.affiliation: Department of Internal Medicine, University of Michigan Health System, 4618 Medical Science Building II, Ann Arbor, MI 48109, USA. sethwalk@umich.edu
authors.forename: Seth T
authors.initials: ST
authors.lastname: Walk
authors.forename: Elizabeth W
authors.initials: EW
authors.lastname: Alm
authors.forename: David M
authors.initials: DM
authors.lastname: Gordon
authors.forename: Jeffrey L
authors.initials: JL
authors.lastname: Ram
authors.forename: Gary A
authors.initials: GA
authors.lastname: Toranzos
authors.forename: James M
authors.initials: JM
authors.lastname: Tiedje
authors.forename: Thomas S
authors.initials: TS
authors.lastname: Whittam
mesh_terms: D000222:Adaptation, Physiological; D000818:Animals; D015373:Bacterial Typing Techniques; D001483:Base Sequence; D017931:DNA Primers / Q000235:genetics; D004269:DNA, Bacterial / Q000235:genetics; D017753:Ecosystem; D004783:Environmental Microbiology; D004925:Escherichia / Q000145:classification* / Q000235:genetics* / Q000302:isolation & purification / Q000502:physiology; D004926:Escherichia coli / Q000145:classification / Q000235:genetics / Q000302:isolation & purification / Q000502:physiology; D019143:Evolution, Molecular; D041981:Gastrointestinal Tract / Q000382:microbiology; D051456:Gene Flow; D005798:Genes, Bacterial; D006801:Humans; D010641:Phenotype; D010802:Phylogeny; D016133:Polymerase Chain Reaction; D013997:Time Factors
chemical_list: D017931:DNA Primers; D004269:DNA, Bacterial
references.citation: Environ Microbiol. 2005 May;7(5):631-40
references.pmid: 15819845
references.citation: Microbes Infect. 2002 Sep;4(11):1125-32
references.pmid: 12361912
references.citation: J Gen Microbiol. 1991 Aug;137(8):1911-21
references.pmid: 1955870
references.citation: Genetics. 2008 Sep;180(1):431-43
references.pmid: 18757947
references.citation: Appl Environ Microbiol. 2006 Nov;72(11):7286-93
references.pmid: 16980418
references.citation: Proc Natl Acad Sci U S A. 2008 Feb 19;105(7):2504-9
references.pmid: 18272490
references.citation: Infect Immun. 2002 Dec;70(12):6853-9
references.pmid: 12438362
references.citation: J Mol Evol. 1987;26(1-2):74-86
references.pmid: 3125340
references.citation: Mol Microbiol. 2006 Jun;60(5):1136-51
references.pmid: 16689791
references.citation: Philos Trans R Soc Lond B Biol Sci. 2006 Nov 29;361(1475):1929-40
references.pmid: 17062412
references.citation: Genetics. 1989 Nov;123(3):585-95
references.pmid: 2513255
references.citation: Genome Biol. 2007;8(8):R164
references.pmid: 17686180
references.citation: Nucleic Acids Res. 2006 Jan 1;34(Database issue):D335-7
references.pmid: 16381881
references.citation: Microbiology (Reading). 2003 Dec;149(Pt 12):3575-3586
references.pmid: 14663089
references.citation: Science. 2008 Apr 11;320(5873):237-9
references.pmid: 18403712
references.citation: Philos Trans R Soc Lond B Biol Sci. 2006 Nov 29;361(1475):1899-909
references.pmid: 17062409
references.citation: J Clin Microbiol. 1985 Jan;21(1):77-81
references.pmid: 3968204
references.citation: Environ Microbiol. 2007 Sep;9(9):2274-88
references.pmid: 17686024
references.citation: J Mol Evol. 2003 Aug;57(2):140-8
references.pmid: 14562958
references.citation: Semin Pediatr Infect Dis. 2005 Apr;16(2):125-36
references.pmid: 15825143
references.citation: Proc Natl Acad Sci U S A. 2000 Sep 12;97(19):10567-72
references.pmid: 10954745
references.citation: Trends Ecol Evol. 2007 Mar;22(3):148-55
references.pmid: 17129636
references.citation: Science. 1996 Jan 26;271(5248):470-7
references.pmid: 8560259
references.citation: J Clin Microbiol. 1982 Jun;15(6):1133-40
references.pmid: 7107843
references.citation: BMC Biol. 2005 Mar 07;3:6
references.pmid: 15752428
references.citation: Environ Microbiol. 2006 Mar;8(3):504-13
references.pmid: 16478456
references.citation: J Bacteriol. 1998 Apr;180(8):2144-51
references.pmid: 9555898
references.citation: Mol Biol Evol. 2006 Feb;23(2):254-67
references.pmid: 16221896
references.citation: Appl Environ Microbiol. 1996 Sep;62(9):3350-4
references.pmid: 8795225
references.citation: J Hyg (Lond). 1973 Mar;71(1):1-7
references.pmid: 4571611
references.citation: Genetics. 1995 Sep;141(1):413-29
references.pmid: 8536987
references.citation: J Clin Microbiol. 1982 Apr;15(4):703-13
references.pmid: 7040466
references.citation: Water Res. 2003 Sep;37(16):3978-82
references.pmid: 12909116
references.citation: Genetics. 1993 Jun;134(2):401-8
references.pmid: 8325477
references.citation: Science. 2007 Aug 24;317(5841):1093-6
references.pmid: 17717188
references.citation: Appl Environ Microbiol. 2006 Jan;72(1):612-21
references.pmid: 16391098
references.citation: J Mol Evol. 2007 Jan;64(1):71-9
references.pmid: 17160643
references.citation: J Bacteriol. 2005 Jan;187(2):619-28
references.pmid: 15629933
references.citation: Curr Opin Genet Dev. 1992 Dec;2(6):937-42
references.pmid: 1335810
references.citation: Genetics. 1981 Jul;98(3):467-90
references.pmid: 7037535
references.citation: PLoS Genet. 2008 Feb;4(2):e35
references.pmid: 18282111
references.citation: Int J Syst Evol Microbiol. 2005 Sep;55(Pt 5):2013-2025
references.pmid: 16166704
references.citation: Appl Environ Microbiol. 1991 Feb;57(2):592-3
references.pmid: 2014993
references.citation: J Bacteriol. 1991 Nov;173(22):7257-68
references.pmid: 1938920
references.citation: EXS. 1994;69:479-93
references.pmid: 7994120
references.citation: J Clin Microbiol. 1995 May;33(5):1054-9
references.pmid: 7615704
references.citation: Proc Biol Sci. 2008 Feb 7;275(1632):277-84
references.pmid: 18029306
references.citation: Appl Environ Microbiol. 2000 Oct;66(10):4555-8
references.pmid: 11010916
references.citation: Int J Syst Evol Microbiol. 2003 May;53(Pt 3):807-810
references.pmid: 12807204
references.citation: Diagn Microbiol Infect Dis. 2007 Jun;58(2):153-61
references.pmid: 17368802
references.citation: Mol Biol Evol. 2007 Aug;24(8):1596-9
references.pmid: 17488738
references.citation: Philos Trans R Soc Lond B Biol Sci. 2006 Nov 29;361(1475):2045-53
references.pmid: 17062419
references.citation: Mol Microbiol. 2006 Feb;59(3):975-88
references.pmid: 16420365
references.citation: PLoS Genet. 2009 Jan;5(1):e1000344
references.pmid: 19165319
references.citation: Microbes Environ. 2008;23(2):101-8
references.pmid: 21558695
references.citation: Antonie Van Leeuwenhoek. 1989;55(1):23-32
references.pmid: 2662899
references.citation: J Infect Dis. 2000 Jan;181(1):261-72
references.pmid: 10608775
references.citation: Genetics. 1993 Oct;135(2):599-607
references.pmid: 8244016
references.citation: Microbiology (Reading). 2005 Jan;151(Pt 1):15-23
references.pmid: 15632421
references.citation: Microbiology (Reading). 2002 May;148(Pt 5):1513-1522
references.pmid: 11988526