The emergence and fate of horizontally acquired genes in Escherichia coli

Bacterial species, and even strains within species, can vary greatly in their gene contents and metabolic capabilities. We examine the evolution of this diversity by assessing the distribution and ancestry of each gene in 13 sequenced isolates of Escherichia coli and Shigella. We focus on the emergence and demise of two specific classes of genes, ORFans (genes with no homologs in present databases) and HOPs (genes with distant homologs), since these genes, in contrast to most conserved ancestral sequences, are known to be a major source of the novel features in each strain. We find that the rates of gain and loss of these genes vary greatly among strains as well as through time, and that ORFans and HOPs show very different behavior with respect to their emergence and demise. Although HOPs, which mostly represent gene acquisitions from other bacteria, originate more frequently, ORFans are much more likely to persist. This difference suggests that many adaptive traits are conferred by completely novel genes that do not originate in other bacterial genomes. With respect to the demise of these acquired genes, we find that strains of Shigella lose genes, both by disruption events and by complete removal, at accelerated rates

Mainstreams of Horizontal Gene Exchange in Enterobacteria: Consideration of the Outbreak of Enterohemorrhagic E. coli O104:H4 in Germany in 2011

Escherichia coli O104:H4 caused a severe outbreak in Europe in 2011. The strain TY-2482 sequenced from this outbreak allowed the discovery of its closest relatives but failed to resolve ways in which it originated and evolved. On account of the previous statement, may we expect similar upcoming outbreaks to occur recurrently or spontaneously in the future? The inability to answer these questions shows limitations of the current comparative and evolutionary genomics methods.status: publishe

Fate of the H-NS–Repressed bgl Operon in Evolution of Escherichia coli

In the enterobacterial species Escherichia coli and Salmonella enterica, expression of horizontally acquired genes with a higher than average AT content is repressed by the nucleoid-associated protein H-NS. A classical example of an H-NS–repressed locus is the bgl (aryl-β,D-glucoside) operon of E. coli. This locus is “cryptic,” as no laboratory growth conditions are known to relieve repression of bgl by H-NS in E. coli K12. However, repression can be relieved by spontaneous mutations. Here, we investigated the phylogeny of the bgl operon. Typing of bgl in a representative collection of E. coli demonstrated that it evolved clonally and that it is present in strains of the phylogenetic groups A, B1, and B2, while it is presumably replaced by a cluster of ORFans in the phylogenetic group D. Interestingly, the bgl operon is mutated in 20% of the strains of phylogenetic groups A and B1, suggesting erosion of bgl in these groups. However, bgl is functional in almost all B2 isolates and, in approximately 50% of them, it is weakly expressed at laboratory growth conditions. Homologs of bgl genes exist in Klebsiella, Enterobacter, and Erwinia species and also in low GC-content Gram-positive bacteria, while absent in E. albertii and Salmonella sp. This suggests horizontal transfer of bgl genes to an ancestral Enterobacterium. Conservation and weak expression of bgl in isolates of phylogenetic group B2 may indicate a functional role of bgl in extraintestinal pathogenic E. coli

Genomic characterisation of an endometrial pathogenic <i>Escherichia coli</i> strain reveals the acquisition of genetic elements associated with extra-intestinal pathogenicity

&lt;b&gt;Background&lt;/b&gt;&lt;p&gt;&lt;/p&gt; Strains of &lt;i&gt;Escherichia coli&lt;/i&gt; cause a wide variety of intestinal and extra-intestinal diseases in both humans and animals, and are also often found in healthy individuals or the environment. Broadly, a strong phylogenetic relationship exists that distinguishes most &lt;i&gt;E. Coli&lt;/i&gt; causing intestinal disease from those that cause extra-intestinal disease, however, isolates within a recently described subclass of Extra-Intestinal Pathogenic &lt;i&gt;E. Coli&lt;/i&gt; (ExPEC), termed endometrial pathogenic &lt;i&gt;E. Coli&lt;/i&gt;, tend to be phylogenetically distant from the vast majority of characterised ExPECs, and more closely related to human intestinal pathogens. In this work, we investigate the genetic basis for ExPEC infection in the prototypic endometrial pathogenic &lt;i&gt;E. Coli&lt;/i&gt; strain MS499.&lt;p&gt;&lt;/p&gt; &lt;b&gt;Results&lt;/b&gt;&lt;p&gt;&lt;/p&gt; By investigating the genome of MS499 in comparison with a range of other E. coli sequences, we have discovered that this bacterium has acquired substantial lengths of DNA which encode factors more usually associated with ExPECs and less frequently found in the phylogroup relatives of MS499. Many of these acquired factors, including several iron acquisition systems and a virulence plasmid similar to that found in several ExPECs such as APEC O1 and the neonatal meningitis &lt;i&gt;E. Coli&lt;/i&gt; S88, play characterised roles in a variety of typical ExPEC infections and appear to have been acquired recently by the evolutionary lineage leading to MS499.&lt;p&gt;&lt;/p&gt; &lt;b&gt;Conclusions&lt;/b&gt;&lt;p&gt;&lt;/p&gt; Taking advantage of the phylogenetic relationship we describe between MS499 and several other closely related &lt;i&gt;E. Coli&lt;/i&gt; isolates from across the globe, we propose a step-wise evolution of a novel clade of sequence type 453 ExPECs within phylogroup B1, involving the recruitment of ExPEC virulence factors into the genome of an ancestrally non-extraintestinal &lt;i&gt;E. Coli&lt;/i&gt;, which has repurposed this lineage with the capacity to cause extraintestinal disease. These data reveal the genetic components which may be involved in this phenotype switching, and argue that horizontal gene exchange may be a key factor in the emergence of novel lineages of ExPECs.&lt;p&gt;&lt;/p&gt

Fate of the H-NS-Repressed bgl Operon in Evolution of Escherichia coli

In the enterobacterial species Escherichia coli and Salmonella enterica, expression of horizontally acquired genes with a higher than average AT content is repressed by the nucleoid-associated protein H-NS. A classical example of an H-NS-repressed locus is the bgl (aryl-beta,D-glucoside) operon of E. coli. This locus is "cryptic,'' as no laboratory growth conditions are known to relieve repression of bgl by H-NS in E. coli K12. However, repression can be relieved by spontaneous mutations. Here, we investigated the phylogeny of the bgl operon. Typing of bgl in a representative collection of E. coli demonstrated that it evolved clonally and that it is present in strains of the phylogenetic groups A, B1, and B2, while it is presumably replaced by a cluster of ORFans in the phylogenetic group D. Interestingly, the bgl operon is mutated in 20% of the strains of phylogenetic groups A and B1, suggesting erosion of bgl in these groups. However, bgl is functional in almost all B2 isolates and, in approximately 50% of them, it is weakly expressed at laboratory growth conditions. Homologs of bgl genes exist in Klebsiella, Enterobacter, and Erwinia species and also in low GC-content Gram-positive bacteria, while absent in E. albertii and Salmonella sp. This suggests horizontal transfer of bgl genes to an ancestral Enterobacterium. Conservation and weak expression of bgl in isolates of phylogenetic group B2 may indicate a functional role of bgl in extraintestinal pathogenic E. coli

Evolution of commensal bacteria in the intestinal tract of mice

The deposited article is a post-print version and has been submitted to peer review.This deposit is composed by the main article, and it hasn't any supplementary materials associated.This publication hasn't any creative commons license associated.Hundreds of different bacterial species inhabit our intestines and contribute to our health status, with significant loss of species diversity typically observed in disease conditions. Within each microbial species a great deal of diversity is hidden and such intra-specific variation is also key to the proper homeostasis between the host and its microbial inhabitants. Indeed, it is at this level that new mechanisms of antibiotic resistance emerge and pathogenic characteristics evolve. Yet, our knowledge on intra-species variation in the gut is still limited and an understanding of the evolutionary mechanisms acting on it is extremely reduced. Here we review recent work that has begun to reveal that adaptation of commensal bacteria to the mammalian intestine may be fast and highly repeatable, and that the time scales of evolutionary and ecological change can be very similar in these ecosystems.Deutsche Forschungsgemeinschaft Grant SFB 680 and the Portuguese Science and Technology Foundation FCT (SFRH/BPD/111725/2015 and UID/BIM/04501/2013 support to AS, SFRH/BPD/110750/2015 support to NF).info:eu-repo/semantics/publishedVersio

The Impact of Recombination on dN/dS within Recently Emerged Bacterial Clones

The development of next-generation sequencing platforms is set to reveal an unprecedented level of detail on short-term molecular evolutionary processes in bacteria. Here we re-analyse genome-wide single nucleotide polymorphism (SNP) datasets for recently emerged clones of methicillin resistant Staphylococcus aureus (MRSA) and Clostridium difficile. We note a highly significant enrichment of synonymous SNPs in those genes which have been affected by recombination, i.e. those genes on mobile elements designated “non-core” (in the case of S. aureus), or those core genes which have been affected by homologous replacements (S. aureus and C. difficile). This observation suggests that the previously documented decrease in dN/dS over time in bacteria applies not only to genomes of differing levels of divergence overall, but also to horizontally acquired genes of differing levels of divergence within a single genome. We also consider the role of increased drift acting on recently emerged, highly specialised clones, and the impact of recombination on selection at linked sites. This work has implications for a wide range of genomic analyses

Obscured phylogeny and possible recombinational dormancy in Escherichia coli

<p>Abstract</p> <p>Background</p> <p><it>Escherichia coli </it>is one of the best studied organisms in all of biology, but its phylogenetic structure has been difficult to resolve with current data and analytical techniques. We analyzed single nucleotide polymorphisms in chromosomes of representative strains to reconstruct the topology of its emergence.</p> <p>Results</p> <p>The phylogeny of <it>E. coli </it>varies according to the segment of chromosome analyzed. Recombination between extant <it>E. coli </it>groups is largely limited to only three intergroup pairings.</p> <p>Conclusions</p> <p>Segment-dependent phylogenies most likely are legacies of a complex recombination history. However, <it>E. coli </it>are now in an epoch in which they no longer broadly share DNA. Using the definition of species as organisms that freely exchange genetic material, this recombinational dormancy could reflect either the end of <it>E. coli </it>as a species, or herald the coalescence of <it>E. coli </it>groups into new species.</p

The impact of horizontal gene transfer in shaping operons and protein interaction networks – direct evidence of preferential attachment

<p>Abstract</p> <p>Background</p> <p>Despite the prevalence of horizontal gene transfer (HGT) in bacteria, to this date there were few studies on HGT in the context of gene expression, operons and protein-protein interactions. Using the recently available data set on the <it>E. coli </it>protein-protein interaction network, we sought to explore the impact of HGT on genome structure and protein networks.</p> <p>Results</p> <p>We classified the <it>E. coli </it>genes into three categories based on their evolutionary conservation: a set of 2158 <it>Core </it>genes that are shared by all <it>E. coli </it>strains, a set of 1044 <it>Non-core </it>genes that are strain-specific, and a set of 1053 genes that were putatively acquired by horizontal transfer. We observed a clear correlation between gene expressivity (measured by Codon Adaptation Index), evolutionary rates, and node connectivity between these categories of genes. Specifically, we found the <it>Core </it>genes are the most highly expressed and the most slowly evolving, while the <it>HGT </it>genes are expressed at the lowest level and evolve at the highest rate. <it>Core </it>genes are the most likely and <it>HGT </it>genes are the least likely to be member of the operons. In addition, we found the <it>Core </it>genes on average are more highly connected than <it>Non-core </it>and <it>HGT </it>genes in the protein interaction network, however the <it>HGT </it>genes displayed a significantly higher mean node degree than the <it>Core </it>and <it>Non-core </it>genes in the defence COG functional category. Interestingly, <it>HGT </it>genes are more likely to be connected to <it>Core </it>genes than expected by chance, which suggest a model of differential attachment in the expansion of cellular networks.</p> <p>Conclusion</p> <p>Results from our analysis shed light on the mode and mechanism of the integration of horizontally transferred genes into operons and protein interaction networks.</p