Defining the Genome Features of Escherichia albertii, an Emerging Enteropathogen Closely Related to Escherichia coli

Abstract

Escherichia albertii is a recently recognized close relative of Escherichia coli. This emerging enteropathogen possesses a type III secretion system (T3SS) encoded by the locus of enterocyte effacement, similar to enteropathogenic and enterohemorrhagic E. coli (EPEC and EHEC). Shiga toxin-producing strains have also been identified. The genomic features of E. albertii, particularly differences from other Escherichia species, have not yet been well clarified. Here, we sequenced the genome of 29 E. albertii strains (3 complete and 26 draft sequences) isolated from multiple sources and performed intraspecies and intragenus genomic comparisons. The sizes of the E. albertii genomes range from 4.5 to 5.1 Mb, smaller than those of E. coli strains. Intraspecies genomic comparisons identified five phylogroups of E. albertii. Intragenus genomic comparison revealed that the possible core genome of E. albertii comprises 3,250 genes, whereas that of the genus Escherichia comprises 1,345 genes. Our analysis further revealed several unique or notable genetic features of E. albertii, including those responsible for known biochemical features and virulence factors and a possibly active second T3SS known as ETT2 (E. coli T3SS 2) that is inactivated in E. coli. Although this organism has been observed to be nonmotile in vitro, genes for flagellar biosynthesis are fully conserved; chemotaxis-related genes have been selectively deleted. Based on these results, we have developed a nested polymerase chain reaction system to directly detect E. albertii. Our data define the genomic features of E. albertii and provide a valuable basis for future studies of this important emerging enteropathogen.

Keywords: Escherichia albertii; core genome; detection system; emerging enteropathogen; genomic comparison; interspecies horizontal gene transfer.

Fig. 1.—

Circular presentation of the genome of Escherichia albertii strain CB9786 and conservation of CB9786 genes in the genomes of E. albertii, E. fergusonii, E. coli, and other Escherichia species. From the outside in: nucleotide positions (in Mb); CDSs transcribed clockwise and counterclockwise, respectively; locations of PPs and IEs (green) and LEE and ETT2 (red); CDSs (purple) conserved in the E. coli strains NA114, SE15, S88, APEC O1, IHE3034, UTI89, UM146, ED1a, CFT073, ABU_83972, LF82, NRG857C, 536, E2348/69, SMS-3-5, CE10, IAI39, UMN026, 042, E24377A, KO11FL, 55989, 2011C-3493, 2009EL-2071, 2009EL-2050, SE11, IAI1, O103_12009, O111_11128, O26_11368, APECO78, HS, ATCC8739, P12b, MG1655, H10407, UMNK88, O157_Xuzhou21, O157_EC4115, O157_EDL933, O157_TW14359, O157_Sakai, O55_RM12579, and O55_CB9615; CDSs (light blue) conserved in the E. fergusonii strains GTA-294-5-RBA-P2, ECD227, B253, GTA-1753-4-RBA-P5, and ATCC35469; CDSs (orange) conserved in the Escherichia cryptic clade strains TW10509 (C-I), TW09276, KTE31, KTE114 (C-III), H605 (C-IV), KTE96, KTE11, E1118, HT073016, KTE52, and KTE159 (C-V); CDSs (red) conserved in the E. albertii strains HIPH08472, EC03-127, 24, 20H38, NIAH_Bird_23, K7394, EC05-44, TW08933, NBRC 107761, TW07627, KF1, CB10113, B156, 4051-6, EC03-195, EC05-81, K7744, NIAH_Bird_16, E2675, NIAH_Bird_8, NIAH_Bird_2, NIAH_Bird_24, NIAH_Bird_13, 94389, EC05-160, KU20110014, EC06-170, NIAH_Bird_3, CB9791, NIAH_Bird_26, NIAH_Bird_5, NIAH_Bird_25, and K7756; CDSs (blue) conserved in the three E. albertii strains fully sequenced in this study; and G+C content.

Fig. 2.—

Genome-wide phylogenetic analysis of Escherichia albertii strains and those belonging to other Escherichia species and clades. A neighbour-joining tree (in box) was constructed using the concatenated nucleotide sequences of 111 single copy genes that are fully conserved in the genomes of 34 E. albertii strains, 44 E. coli strains, 5 E. fergusonii strains, and 15 strains belonging to Escherichia cryptic clades with a low probability of recombination. An enlarged view of the E. albertii lineage is shown. The three strains fully sequenced in this study are indicated by asterisks. G1–G5 indicate five phylogroups of E. albertii.

Fig. 3.—

Intraspecies and interspecies conservation of Escherichia albertii genes. (A) A Venn diagram showing the number of unique or shared CDSs among the three completely sequenced E. albertii strains. (B) Distribution of 3,622 CDSs that are shared by three fully sequenced E. albertii strains among the 34 strains analyzed in this study. The CDSs indicated by asterisks are conserved in all or 33 strains. (C) The presence of homologs for 3,622 CDSs shared by three fully sequenced E. albertii strains among 44 fully sequenced E. coli strains. The CDSs indicated by asterisks are conserved in all or 43 of the E. coli strains.

Fig. 4.—

Structures of the Escherichia albertii ETT2 (E. coli T3SS 2) region. Gene organizations of the ETT2 regions of three fully sequenced E. albertii strains are shown. For comparison, the ETT2 region of the enteroaggregative E. coli strain 042 is also shown. Note that the ETT2 region has been highly degraded in most E. coli strains.

Fig. 5.—

Gene organizations of genomic loci encoding flagellar biosynthesis- and chemotaxis-related genes. Gene organizations of genomic loci encoding flagellar biosynthesis- and chemotaxis-related genes are shown. For comparison, analogous loci from Escherichia coli K-12 MG1655 are shown. While amino acid sequence identities between orthologous genes are presented in panel A, the nucleotide sequence identities of conserved genomic regions are presented in panel B to illustrate the specific deletion of chemotaxis-related genes. The flhA-flhD locus is presented in both panels A and B.