Chemoreceptor Gene Loss and Acquisition via Horizontal Gene Transfer in Escherichia coli

Abstract

Ridge, Tennessee, USA b Chemotaxis allows bacteria to more efficiently colonize optimal microhabitats within their larger environment. Chemotaxis in Escherichia coli is the best-studied model system, and a large number of E. coli strains have been sequenced. The Escherichia/ Shigella genus encompasses a great variety of commensal and pathogenic strains, but the role of chemotaxis in their association with the host remains poorly understood. Here we show that the core chemotaxis genes are lost in many, but not all, nonmotile strains but are well preserved in all motile strains. The genes encoding the Tar, Tsr, and Aer chemoreceptors, which mediate chemotaxis to a broad spectrum of chemical and physical cues, are also nearly uniformly conserved in motile strains. In contrast, the clade of extraintestinal pathogenic E. coli strains apparently underwent an ancestral loss of Trg and Tap chemoreceptors, which sense sugars, dipeptides, and pyrimidines. The broad range of time estimated for the loss of these genes (1 to 3 million years ago) corresponds to the appearance of the genus Homo. Escherichia coli strains are ubiquitous colonizers of the intestines of mammals and birds (1). There are several highly adapted E. coli clones that have acquired virulence traits and cause a broad spectrum of disease, including enteric/diarrheal disease, urinary tract infections (UTIs), and sepsis/meningitis (2). Depending on the site of infection, pathogenic strains are classified as intestinal E. coli (IPEC) or extraintestinal pathogenic E. coli (ExPEC), and distinct pathotypes (based on clinical manifestation) are recognized within both categories. The most common ExPEC pathotypes include uropathogenic E. coli (UPEC), meningitis-associated E. coli (MNEC), and avian-pathogenic E. coli (APEC) (2, 3). Motility was shown to be important for the colonization of both commensal and pathogenic E. coli strains, as well as for the pathogenesis of the latter (4, 5): however, the exact role of motility and the underlying chemotaxis system in these processes remain poorly understood. The molecular machinery that controls chemotaxis in E. coli has been the subject of intensive investigation (6, 7). Its components include chemoreceptors, also known as methyl-accepting chemotaxis proteins (MCPs), a histidine kinase (CheA), an adaptor protein (CheW), a methyltransferase (CheR), and a methylesterase (CheB), as well as a response regulator (CheY) and its phosphatase (CheZ). E. coli has five chemoreceptors. Tsr mediates attractant responses to serine and quorum autoinducer AI-2 (8, 9), as well as responses to oxygen, redox, and oxidizable substrates (10, 11). It was also recently shown to mediate taxis to 3,4-dihydroxymandelic acid, a metabolite of norepinephrine that is produced by human cells (Mike Manson, personal communication). Tar mediates attractant responses to aspartate and maltose (9, 12) and negative responses to metal ions (13). Trg mediates attractant responses to ribose and galactose (14), and Tap mediates attractant responses to di...

Evolutionary Genomics Suggests That CheV Is an Additional Adaptor for Accommodating Specific Chemoreceptors within the Chemotaxis Signaling Complex

“…The largest cluster of chemoreceptors (COG1) contains Tsr, Tar and Tap, whereas the other two E . coli chemoreceptors belong to separate groups: Trg in COG6 and Aer in COG3, which is consistent with recent phylogenetic studies [ 44 ]. The citrate sensor Tcp in S .…”

Extensive Strain-Level Copy-Number Variation across Human Gut Microbiome Species

“…Specifically, in this cluster 7 of the 38 highly variable KCs were bacterial motility proteins, of which 4 were structural flagellar components, 2 were involved in chemotaxis, and 1 was essential for twitching motility (Han et al, 2008). Motility proteins, and especially flagellar proteins, are widely associated with virulence and immunostimulation, and the gain or loss of flagellar components is believed to be an important adaptive mechanism for individual organisms (Borziak et al, 2013; Heikkinen et al, 2007; Al Mamun et al, 1997). Moreover, variation in these 7 KCs was highly consistent within samples; most samples contained either detectable copies of all 7 KCs or no (or low number of) copies of all of these KCs (Fig.…”

Sensory Repertoire of Bacterial Chemoreceptors

“…The Aer chemoreceptor mediates responses to oxygen as well as energy taxis (18,19,62). Many pathogenic E. coli strains lack either Trg, Tap, or both (67).…”