E. coli Common pili promote the fitness and virulence of a hybrid aEPEC/ExPEC strain within diverse host environments

ABSTRACT

Pathogenic subsets of Escherichia coli include diarrheagenic (DEC) strains that cause disease within the gut and extraintestinal pathogenic E. coli (ExPEC) strains that are linked with urinary tract infections, bacteremia, and other infections outside of intestinal tract. Among DEC strains is an emergent pathotype known as atypical enteropathogenic E. coli (aEPEC), which can cause severe diarrhea. Recent sequencing efforts revealed that some E. coli strains possess genetic features that are characteristic of both DEC and ExPEC isolates. BA1250 is a newly reclassified hybrid strain with characteristics of aEPEC and ExPEC. This strain was isolated from a child with diarrhea, but its genetic features indicate that it might have the capacity to cause disease at extraintestinal sites. The spectrum of adhesins encoded by hybrid strains like BA1250 are expected to be especially important in facilitating colonization of diverse niches. E. coli common pilus (ECP) is an adhesin expressed by many E. coli pathogens, but how it impacts hybrid strains has not been ascertained. Here, using zebrafish larvae as surrogate hosts to model both gut colonization and extraintestinal infections, we found that ECP can act as a multi-niche colonization and virulence factor for BA1250. Furthermore, our results indicate that ECP-related changes in activation of envelope stress response pathways may alter the fitness of BA1250. Using an in silico approach, we also delineated the broader repertoire of adhesins that are encoded by BA1250, and provide evidence that the expression of at least a few of these varies in the absence of functional ECP.

KEYWORDS:

• Escherichia coli
• hybrid
• zebrafish
• adhesin
• colonization, ECP
• ExPEC
• EPEC
• envelope stress

Acknowledgments

We thank Fundação Butantan for financial support and personnel from Centralized Zebrafish Animal Resource (CZAR) at the University of Utah, Salt Lake City, Utah, United States for their advice and help with maintaining the zebrafish breeders. We are also grateful to Dr. Jorge Girón for the kind donation of adhesin antibodies, Dr. T. Raivio luxCDABE reporter constructs, and Dr. Travis Wiles for help with creating pGEN-mCherry.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Author contributions

Conceived and designed the experiments: DDM ACR MAM RMFP. Performed the experiments: DDM ACR FFS. Analyzed the data: DDM ACR FFS MAM RMFP. Contributed reagents/materials/analysis tools: MAM RMFP. Wrote the paper: DDM ACR MAM RMFP.

Data availability statement

Some data underlying this article are available in the GenBank database under the accession number JADPBX000000000, BioProject and SRA data PRJNA678986, at https://www.ncbi.nlm.nih.gov/genbank/, and https://doi.org/10.11606/T.42.2020.tde-04012022–135948.

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/19490976.2023.2190308.

Additional information

Funding

This work was supported in part by NIH grants R21 AI135918 and R01 GM134331 to M.A.M and NIH training grant from T32 AI055434 to A.C.R; Brazilian Federal Agency for Support and Evaluation of Graduate Education – CAPES under Grant PDSE - 88881.186835/2018-01, and CNPq under Grant 140088/2016-4 to D.D.M; and São Paulo Research Foundation under grant FAPESP 2017/25406-0 to R.M.F.P.