The ability to obtain bacterial genomes from the same host has allowed for comparative studies that help in the understanding of the molecular evolution of specific pathotypes. Avian pathogenic Escherichia coli (APEC) is a group of extraintestinal strains responsible for causing colibacillosis in birds. APEC is also suggested to possess a role as a zoonotic agent. Despite its importance, APEC pathogenesis still has several cryptic pathogenic processes that need to be better understood. In this work, a genome-wide survey of eight APEC strains for genes with evidence of recombination revealed that ∼14% of the homologous groups evaluated present signs of recombination. Enrichment analyses revealed that nine Gene Ontology (GO) terms were significantly more represented in recombinant genes. Among these GO terms, several were noted to be ATP-related categories. The search for positive selection in these APEC genomes revealed 32 groups of homologous genes with evidence of positive selection. Among these groups, we found several related to cell metabolism, as well as several uncharacterized genes, beyond the well-known virulence factors ompC, lamB, waaW, waaL, and fliC. A GO term enrichment test showed a prevalence of terms related to bacterial cell contact with the external environment (e.g., viral entry into host cell, detection of virus, pore complex, bacterial-type flagellum filament C, and porin activity). Finally, the genes with evidence of positive selection were retrieved from genomes of non-APEC strains and tested as were done for APEC strains. The result revealed that none of the groups of genes presented evidence of positive selection, confirming that the analysis was effective in inferring positive selection for APEC and not for E. coli in general, which means that the study of the genes with evidence of positive selection identified in this study can contribute for the better understanding of APEC pathogenesis processes.
Get full access to this article
View all access options for this article.
References
1.
AguiletaG, LengelleJ, MartheyS, ChiapelloH, RodolpheF, GendraultA, YocktengR, VerckenE, DevierB, FontaineMC, WinckerP, DossatC, CruaudC, CoulouxA, GiraudT. Finding candidate genes under positive selection in Non-model species: Examples of genes involved in host specialization in pathogens. Mol Ecol, 2010; 19:292–306.
2.
AguiletaG, RefrégierG, YocktengR, FournierE. Giraud T. Rapidly evolving genes in pathogens: Methods for detecting positive selection and examples among fungi, bacteria, viruses and protists. Infect Genet Evol, 2009; 9:656–670.
3.
BarnesHJ, VaillancourtJP, GrossW. Colibacillosis. In: SaifY (ed.). Diseases of Poultry. Ames: Iowa State University Press, 2003, pp. 631–656.
4.
BrissetteJL, RusselM. Secretion and membrane integration of a filamentous phage-encoded morphogenetic protein. J Mol Biol, 1990; 211:565–580.
5.
BruenTC, PhilippeH, BryantD. A simple and robust statistical test for detecting the presence of recombination. Genetics, 2006; 172:2665–2681.
6.
ChenSL, HungC-S, XuJ, ReigstadCS, MagriniV, SaboA, BlasiarD, BieriT, MeyerRR, OzerskyP, ArmstrongJR, FultonRS, LatreilleJP, SpiethJ, HootonTM, MardisER, HultgrenSJ, GordonJI. Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: A comparative genomics approach. Proc Natl Acad Sci U S A, 2006; 103:5977–5982.
7.
ConesaA, GötzS, García-GómezJM, TerolJ, TalónM, RoblesM. Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 2005; 21:3674–3676.
8.
DarwinAJ. The phage-shock-protein response. Mol Microbiol, 2005; 57:621–628.
9.
de PaivaJB, LeiteJL, da SilvaLP, RojasTC, de PaceF, ConceiçãoRA, SperandioV, da SilveiraWD. Influence of the major nitrite transporter NirC on the virulence of a Swollen Head Syndrome avian pathogenic E. coli (APEC) strain. Vet Microbiol, 2015; 175:123–131.
10.
DzivaF, HauserH, ConnorTR, van DiemenPM, PrescottG, LangridgeGC, EckertS, ChaudhuriRR, EwersC, MellataM, MukhopadhyayS, CurtissR, DouganG, WielerLH, ThomsonNR, PickardDJ, StevensMP. Sequencing and functional annotation of avian pathogenic Escherichia coli serogroup O78 strains reveal the evolution of E. coli lineages pathogenic for poultry via distinct mechanisms. Infect Immun, 2013; 81:838–849.
11.
GoodmanMF. The discovery of error-prone DNA polymerase V and its unique regulation by RecA and ATP. J Biol Chem, 2014; 289:26772–26782.
12.
HongoJA, de CastroGM, CintraLC, ZerlotiniA, LoboFP. POTION: An end-to-end pipeline for positive Darwinian selection detection in genome-scale data through phylogenetic comparison of protein-coding genes. BMC Genomics, 2015; 16:567.
13.
JohnsonTJ, JohnsonSJ, NolanLK. Complete DNA sequence of a ColBM plasmid from avian pathogenic Escherichia coli suggests that it evolved from closely related ColV virulence plasmids. J Bacteriol, 2006a;188:5975–83.
14.
JohnsonTJ, KariyawasamS, WannemuehlerY, MangiameleP, JohnsonSJ, DoetkottC, SkybergJA, LynneAM, JohnsonJR, NolanLK. The genome sequence of avian pathogenic Escherichia coli strain O1:K1:H7 shares strong similarities with human extraintestinal pathogenic E. coli genomes. J Bacteriol, 2007; 189:3228–36.
15.
JohnsonTJ, WannemeuhlerYM, ScaccianoceJA, JohnsonSJ, NolanLK. Complete DNA sequence, comparative genomics, and prevalence of an IncHI2 plasmid occurring among extraintestinal pathogenic Escherichia coli isolates. Antimicrob Agents Chemother, 2006b;50:3929–33.
16.
JovanovicG, LloydLJ, StumpfMP, MayhewAJ, BuckM. Induction and function of the phage shock protein extracytoplasmic stress response in Escherichia coli. J Biol Chem, 2006; 281:21147–21161.
KooninEV. Orthologs, paralogs, and evolutionary genomics. Annu Rev Genet, 2005; 39:309–338.
19.
LefébureT, StanhopeMJ. Evolution of the core and pan-genome of Streptococcus: Positive selection, recombination, and genome composition. Genome Biol, 2007; 8:R71.
20.
LefébureT, StanhopeMJ. Pervasive, genome-wide positive selection leading to functional divergence in the bacterial genus Campylobacter. Genome Res, 2009; 19:1224–1232.
21.
LiL, StoeckertCJJr., RoosDS. OrthoMCL: Identification of ortholog groups for eukaryotic genomes. Genome Res, 2003; 13:2178–2189.
22.
LöytynojaA, GoldmanN. webPRANK: A phylogeny-aware multiple sequence aligner with interactive alignment browser. BMC Bioinformatics, 2010; 11:579.
23.
MalutaRP, LogueCM, Tiba CasasMR, MengT, Lopes GuastalliEA, Galvao RojasTC, MontelliAC, SadatsuneT, RamosMdC, NolanLK, da SilveiraWD. Overlapped sequence types (STs) and serogroups of avian pathogenic (APEC) and human extra-intestinal pathogenic (ExPEC) Escherichia coli isolated in Brazil. PLoS One, 2014; 9:e105016.
MaturanaVG, de PaceF, CarlosC, Mistretta PiresM, Amabile de CamposT, NakazatoG, Guedes SthelingE, LogueCM, NolanLK, Dias da SilveiraW. Subpathotypes of avian pathogenic Escherichia coli (APEC) exist as defined by their syndromes and virulence traits. Open Microbiol J, 2011; 5:55–64.
26.
McGrathBC, OsbornMJ. Localization of the terminal steps of O-antigen synthesis in Salmonella Typhimurium. J Bacteriol, 1991; 173:649–654.
MulfordCA, OsbornMJ. An intermediate step in translocation of lipopolysaccharide to the outer membrane of Salmonella Typhimurium. Proc Natl Acad Sci U S A, 1983; 80:1159–1163.
29.
NewtonSM, KlebbaPE, MichelV, HofnungM, CharbitA. Topology of the membrane protein LamB by epitope tagging and a comparison with the X-ray model. J Bacteriol, 1996; 178:3447–3456.
NikaidoH. Porins and specific diffusion channels in bacterial outer membranes. J Biol Chem, 1994; 269:3905–3908.
32.
OrsiRH, MaronSB, NightingaleKK, JeromeM, TaborH, WiedmannM. Lineage specific recombination and positive selection in coding and intragenic regions contributed to evolution of the main Listeria monocytogenes virulence gene cluster. Infect Genet Evol, 2008; 8:566–576.
33.
OrskovI, OrskovF, JannB, JannK. Serology, chemistry, and genetics of O and K antigens of Escherichia coli. Bacteriol Rev, 1977; 41:667–710.
34.
PetersenL, BollbackJP, DimmicM, HubiszM, NielsenR. Genes under positive selection in Escherichia coli. Genome Res, 2007; 17:1336–1343.
35.
PilattiL, Boldrin de PaivaJ, RojasTC, LeiteJL, ConceiçãoRA, NakazatoG, Dias da SilveiraW. The virulence factor ychO has a pleiotropic action in an Avian Pathogenic Escherichia coli (APEC) strain. BMC Microbiol, 2016; 16:35.
36.
PolleySD, ChokejindachaiW, ConwayDJ. Allele frequency-based analyses robustly map sequence sites under balancing selection in a malaria vaccine candidate antigen. Genetics, 2003; 165:555–561.
37.
RaetzCR, WhitfieldC. Lipopolysaccharide endotoxins. Annu Rev Biochem, 2002; 71:635–700.
38.
Randall-HazelbauerL, SchwartzM. Isolation of the bacteriophage lambda receptor from Escherichia coli. J Bacteriol, 1973; 116:1436–1446.
39.
RetiefJD. Phylogenetic analysis using PHYLIP. Methods Mol Biol, 2000; 132:243–258.
40.
RojasTC, MalutaRP, ParizziLP, KoenigkanLV, YangJ, YuJ, PereiraGA, Dias da SilveiraW. Genome Sequences of Avian Pathogenic Escherichia coli Strains Isolated from Brazilian Commercial Poultry. Genome Announc, 2013; 1:e0011013.
41.
RojasTC, ParizziLP, TibaMR, ChenL, PereiraGA, SangalV, YangJ, YuJ, Dias da SilveiraW. Draft genome of a Brazilian avian-pathogenic Escherichia coli strain and in silico characterization of virulence-related genes. J Bacteriol, 2012; 194:3023.
42.
RuanX, LoyolaDE, MaroldaCL, Perez-DonosoJM, ValvanoMA. The WaaL O-antigen lipopolysaccharide ligase has features in common with metal ion-independent inverting glycosyltransferases. Glycobiology, 2012; 22:288–299.
43.
RussoTA, JohnsonJR. Proposal for a new inclusive designation for extraintestinal pathogenic isolates of Escherichia coli: ExPEC. J Infect Dis, 2000; 181:1753–1754.
44.
SchirmerT. General and specific porins from bacterial outer membranes. J Struct Biol, 1998; 121:101–109.
45.
ValvanoMA. Common themes in glycoconjugate assembly using the biogenesis of O-antigen lipopolysaccharide as a model system. Biochemistry (Mosc), 2011; 76:729–735.
46.
VandammeAM. Basic concepts of molecular evolution. In SalemiM, VandammeAM (eds.): The Phylogenetic Handbook: A Pratical Approach to DNA and Protein Phylogeny. Cambridge: Cambridge University Press, 2003, pp 1–21.
47.
VermaR, RojasTC, MalutaRP, LeiteJL, da SilvaLP, NakazatoG, Dias da SilveiraW. Fimbria-encoding gene yadC has a pleiotropic effect on several biological characteristics and plays a role in avian pathogenic Escherichia coli pathogenicity. Infect Immun, 2016; 84:187–193.
48.
WangYF, DutzlerR, RizkallahPJ, RosenbuschJP, SchirmerT. Channel specificity: Structural basis for sugar discrimination and differential flux rates in maltoporin. J Mol Biol, 1997; 272:56–63.
49.
WielerLH, McDanielTK, WhittamTS, KaperJB. Insertion site of the locus of enterocyte effacement in enteropathogenic and enterohemorrhagic Escherichia coli differs in relation to the clonal phylogeny of the strains. FEMS Microbiol Lett, 1997; 156:49–53.
50.
WuJC, ChiangTY, ShiueWK, WangSY, SheenIJ, HuangYH, SyuWJ. Recombination of hepatitis D virus RNA sequences and its implications. Mol Biol Evol, 1999; 16:1622–1632.
51.
XuZ, ChenH, ZhouR. Genome-wide evidence for positive selection and recombination in Actinobacillus pleuropneumoniae. BMC Evol Biol, 2011; 11:203.
52.
YangZ. PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol, 2007; 24:1586–1591.
YangZ, NielsenR. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol, 2002; 19:908–917.
55.
YuSL, KoKL, ChenCS, ChangYC, SyuWJ. Characterization of the distal tail fiber locus and determination of the receptor for phage AR1, which specifically infects Escherichia coli O157:H7. J Bacteriol, 2000; 182:5962–5968.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
