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Recombination and positive selection contribute to evolution of Listeria monocytogenes inlA

M. Yeung^3,

K. K. Nightingale^1,

¹ Department of Food Science, Cornell University, Ithaca, NY, USA
² Computational Biology Service Unit, Cornell Theory Center, Cornell University, Ithaca, NY, USA
³ Department of Microbiology and Immunology, Cornell University, Ithaca, NY, USA

Correspondence
M. Wiedmann
mw16{at}cornell.edu

The surface molecule InlA interacts with E-cadherin to promote invasion of Listeria monocytogenes into selected host cells. DNA sequencing of inlA for 40 L. monocytogenes isolates revealed 107 synonymous and 45 nonsynonymous substitutions. A frameshift mutation in a homopolymeric tract encoding part of the InlA signal peptide was identified in three lineage II isolates, which also showed reduced ability to invade human intestinal epithelial cells. Phylogenies showed clear separation of inlA sequences into lineages I and II. Thirteen inlA recombination events, predominantly involving lineage II strains as recipients (12 events), were detected and a number of amino acid residues were shown to be under positive selection. Four of the 45 non-synonymous changes were found to be under positive selection with posterior probabilities >95 %. Mapping of polymorphic and positively selected amino acid sites on the partial crystal structure for InlA showed that the internalin surface of the leucine-rich repeat (LRR) region that faces the InlA receptor E-cadherin does not include any polymorphic sites; all polymorphic and positively selected amino acids mapped to the outer face of the LRR region or to other InlA regions. The data show that (i) inlA is highly polymorphic and evolution of inlA involved a considerable number of recombination events in lineage II isolates; (ii) positive selection at specific amino acid sites appears to contribute to evolution of inlA, including fixation of recombinant events; and (iii) single-nucleotide deletions in a lineage II-specific 3' homopolymeric tract in inlA lead to complete loss of InlA or to production of truncated InlA, which conveys reduced invasiveness. In conclusion, inlA has a complex evolutionary history, which is consistent with L. monocytogenes’ natural history as an environmental pathogen with broad host-range, including its adaptation to environments and hosts where different inlA alleles may provide a selective advantage or where inlA may not be required.

Present address: Biological Sciences Department, Cal Poly State University, San Luis Obispo, CA 93407, USA

Present address: Department of Animal Sciences, 108B Animal Sciences Building, Colorado State University, Fort Collins, CO 80523-11, USA

The GenBank/EMBL/DDBJ accession numbers for the inlA sequences of the isolates used in this study are EF445899–EF445938.

Supplementary tables showing the strains and primers used in this study as well as the details of recombination events in inlA allelic types are available with the online version of this paper.