Genome-wide association reveals host-specific genomic traits in Escherichia coli

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dc.contributor.authorTiwari, Sumeet K.
dc.contributor.authorvan der Putten, Boas C. L.
dc.contributor.authorFuchs, Thilo M.
dc.contributor.authorVinh, Trung N.
dc.contributor.authorBootsma, Martin
dc.contributor.authorOldenkamp, Rik
dc.contributor.authorLa Ragione, Roberto
dc.contributor.authorMatamoros, Sebastien
dc.contributor.authorHoa, Ngo T.
dc.contributor.authorBerens, Christian
dc.contributor.authorLeng, Joy
dc.contributor.authorÁlvarez Sánchez, Julio
dc.contributor.authorFerrandis Vila, Marta
dc.contributor.authorRitchie, Jenny M.
dc.contributor.authorFruth, Angelika
dc.contributor.authorSchwarz, Stefan
dc.contributor.authorDomínguez Rodríguez, Lucas José
dc.contributor.authorUgarte Ruiz, María
dc.contributor.authorBethe, Astrid
dc.contributor.authorHuber, Charlotte
dc.contributor.authorJohanns, Vanessa
dc.contributor.authorStamm, Ivonne
dc.contributor.authorWieler, Lothar H.
dc.contributor.authorEwers, Christa
dc.contributor.authorFivian Hughes, Amanda
dc.contributor.authorSchmidt, Herbert
dc.contributor.authorMenge, Christian
dc.contributor.authorSemmler, Torsten
dc.contributor.authorSchultsz, Constance
dc.date.accessioned2024-08-21T06:01:40Z
dc.date.available2024-08-21T06:01:40Z
dc.date.issued2023-04-11
dc.descriptionAuthors’ contributions: Conceptualization: S.K.T., B.C.L.v.d.P., T.N.V., S.M., N.T.H., T.S., and C.S. Data curation: S.K.T. and B.C.L.v.d.P. Formal analysis: S.K.T., B.C.L.v.d.P., and T.M.F. Funding acquisition: T.N.V., M.B., R.L.R., S.M., N.T.H., C.B., J.A., J.M.R., S.S., L.D., M.U.-R., A.F.-H., C.M., T.S., and C.S. Investigation: S.K.T., B.C.L.v.d.P., T.M.F., M.B., A.F., and H.S. Methodology: S.K.T., B.C.L.v.d.P., and T.M.F. Project administration: S.K.T., B.C.L.v.d.P., T.S., and C.S. Resources: S.K.T., B.C.L.v.d.P., T.M.F., T.N.V., M.B., R.O., R.L.R., S.M., N.T.H., C.B., J.L., J.A., M.F.-V., J.M.R., A.F., S.S., L.D., M.U.-R., A.B., C.H., V.J., I.S., L.H.W., C.E., A.F.-H., H.S., C.M., T.S., and C.S. Software: S.K.T., B.C.L.v.d.P., and T.S. Supervision: C.M., T.S., and C.S. Visualization: S.K.T., B.C.L.v.d.P., and T.M.F. Writing—original draft: S.K.T., B.C.L.v.d.P., and T.M.F. Writing—review and editing: S.K.T., B.C.L.v.d.P., T.M.F., T.N.V., M.B., R.O., R.L.R., S.M., N.T.H., C.B., J.L., J.A., M.F.-V., J.M.R., A.F., S.S., L.D., M.U.-R., A.B., C.H., V.J., I.S., L.H.W., C.E., A.F.-H., H.S., C.M., T.S., and C.S. All authors read and approved the final manuscript. Availability of data and materials The raw reads of the 1090 E. coli isolates sequenced in this study were submitted to NCBI SRA with the Bioproject accession number PRJNA739205 [83], and the SRA accession of 108 isolates [84], that was taken from other studies, was provided in Additional fle 2: Table S1.
dc.description.abstractBackground: Escherichia coli is an opportunistic pathogen which colonizes various host species. However, to what extent genetic lineages of E. coli are adapted or restricted to specific hosts and the genomic determinants of such adaptation or restriction is poorly understood. Results: We randomly sampled E. coli isolates from four countries (Germany, UK, Spain, and Vietnam), obtained from five host species (human, pig, cattle, chicken, and wild boar) over 16 years, from both healthy and diseased hosts, to construct a collection of 1198 whole-genome sequenced E. coli isolates. We identified associations between specific E. coli lineages and the host from which they were isolated. A genome-wide association study (GWAS) identified several E. coli genes that were associated with human, cattle, or chicken hosts, whereas no genes associated with the pig host could be found. In silico characterization of nine contiguous genes (collectively designated as nan-9) associated with the human host indicated that these genes are involved in the metabolism of sialic acids (Sia). In contrast, the previously described sialic acid regulon known as sialoregulon (i.e. nanRATEK-yhcH, nanXY, and nanCMS) was not associated with any host species. In vitro growth experiments with a Δnan-9 E. coli mutant strain, using the sialic acids 5-N-acetylneuraminic acid (Neu5Ac) and N-glycolylneuraminic acid (Neu5Gc) as sole carbon source, showed impaired growth behaviour compared to the wild-type. Conclusions: This study provides an extensive analysis of genetic determinants which may contribute to host specificity in E. coli. Our findings should inform risk analysis and epidemiological monitoring of (antimicrobial resistant) E. coli.
dc.description.departmentDepto. de Sanidad Animal
dc.description.facultyCentro de Vigilancia Sanitaria Veterinaria (VISAVET)
dc.description.refereedTRUE
dc.description.sponsorshipMinisterio de Ciencia, Innovación y Universidades
dc.description.sponsorshipNetherlands Organisation for Health Research and Development
dc.description.sponsorshipFederal Ministry of Education and Research
dc.description.sponsorshipMedical Research Council
dc.description.statuspub
dc.identifier.citationTiwari SK, van der Putten BCL, Fuchs TM, Vinh TN, Bootsma M, Oldenkamp R, La Ragione RM, Matamoros S, Hoa NT, Berens C, Leng J, Alvarez J, Ferrandis- Vila M, Ritchie JM, Fruth A, Schwarz S, Dominguez L, Ugarte-Ruiz M, Bethe A, Huber C, Johanns V, Stamm I, Wieler LH, Ewers C, Fivian-Hughes A, Schmitt H, Menge C, Semmler T and Schultsz C*. Genome-wide association reveals host-specific genomic traits in Escherichia coli. BMC Biology, 21(1):76. 2023. (A). ISSN: 1741-7007. Impact factor: 4.400. Category: Biology, Quartile: 1, Position: 15 of 109. DOI: 10.1186/s12915-023-01562-w
dc.identifier.doi10.1186/s12915-023-01562-w
dc.identifier.issn1741-7007
dc.identifier.officialurlhttps://doi.org/10.1186/s12915-023-01562-w
dc.identifier.pmid37038177
dc.identifier.relatedurlhttps://bmcbiol.biomedcentral.com/articles/10.1186/s12915-023-01562-w
dc.identifier.urihttps://hdl.handle.net/20.500.14352/107539
dc.issue.number76
dc.journal.titleBMC Biology
dc.language.isoeng
dc.relation.projectIDDEAL
dc.relation.projectIDBMBF/DLR
dc.relation.projectIDPCIN-2016-096
dc.relation.projectIDMR/ R002762/1
dc.rightsAttribution 4.0 Internationalen
dc.rights.accessRightsopen access
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/
dc.subject.cdu636.09
dc.subject.keywordEscherichia coli
dc.subject.keywordGWAS
dc.subject.keywordHost-specificity
dc.subject.keywordSialic acid
dc.subject.ucmVeterinaria
dc.subject.unesco3109 Ciencias Veterinarias
dc.titleGenome-wide association reveals host-specific genomic traits in Escherichia coli
dc.typejournal article
dc.type.hasVersionAM
dc.volume.number21
dspace.entity.typePublication
relation.isAuthorOfPublication7a0cfc93-a3f1-45bf-b529-403f216cf8f7
relation.isAuthorOfPublication5d5c3513-e6d9-451a-ba7d-ba0634c84bcf
relation.isAuthorOfPublication1cdbd911-1dfe-4f9c-b9ad-d9c8f03d2956
relation.isAuthorOfPublication.latestForDiscovery7a0cfc93-a3f1-45bf-b529-403f216cf8f7
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