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Selection Acts on DNA Secondary Structures to Decrease Transcriptional Mutagenesis
Claire Hoede,Erick Denamur,Olivier Tenaillon
PLOS Genetics , 2006, DOI: 10.1371/journal.pgen.0020176
Abstract: Single-stranded DNA is more subject to mutation than double stranded. During transcription, DNA is transiently single stranded and therefore subject to higher mutagenesis. However, if local intra-strand secondary structures are formed, some bases will be paired and therefore less sensitive to mutation than unpaired bases. Using complete genome sequences of Escherichia coli, we show that local intra-strand secondary structures can, as a consequence, be used to define an index of transcription-driven mutability. At gene level, we show that natural selection has favoured a reduced transcription-driven mutagenesis via the higher than expected frequency of occurrence of intra-strand secondary structures. Such selection is stronger in highly expressed genes and suggests a sequence-dependent way to control mutation rates and a novel form of selection affecting the evolution of synonymous mutations.
From Grazing Resistance to Pathogenesis: The Coincidental Evolution of Virulence Factors
Sandrine Adiba,Clément Nizak,Minus van Baalen,Erick Denamur,Frantz Depaulis
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0011882
Abstract: To many pathogenic bacteria, human hosts are an evolutionary dead end. This begs the question what evolutionary forces have shaped their virulence traits. Why are these bacteria so virulent? The coincidental evolution hypothesis suggests that such virulence factors result from adaptation to other ecological niches. In particular, virulence traits in bacteria might result from selective pressure exerted by protozoan predator. Thus, grazing resistance may be an evolutionarily exaptation for bacterial pathogenicity.
aes, the gene encoding the esterase B in Escherichia coli, is a powerful phylogenetic marker of the species
Mathilde Lescat, Claire Hoede, Olivier Clermont, Louis Garry, Pierre Darlu, Pierre Tuffery, Erick Denamur, Bertrand Picard
BMC Microbiology , 2009, DOI: 10.1186/1471-2180-9-273
Abstract: We identified the gene encoding esterase B as the acetyl-esterase gene (aes) using gene disruption. The analysis of aes nucleotide sequences in a panel of 78 reference strains, including the E. coli reference (ECOR) strains, demonstrated that the gene is under purifying selection. The phylogenetic tree reconstructed from aes sequences showed a strong correlation with the species phylogenetic history, based on multi-locus sequence typing using six housekeeping genes. The unambiguous distinction between variants B1 and B2 by electrophoresis was consistent with Aes amino-acid sequence analysis and protein modelling, which showed that substituted amino acids in the two esterase B variants occurred mostly at different sites on the protein surface. Studies in an experimental mouse model of septicaemia using mutant strains did not reveal a direct link between aes and extraintestinal virulence. Moreover, we did not find any genes in the chromosomal region of aes to be associated with virulence.Our findings suggest that aes does not play a direct role in the virulence of E. coli extraintestinal infection. However, this gene acts as a powerful marker of phylogeny, illustrating the extensive divergence of B2 phylogenetic group strains from the rest of the species.In humans, Escherichia coli strains can be commensal (part of the normal intestinal microbiota) and/or the cause of various infectious diseases (intestinal and extraintestinal infections) [1]. The extent of commensal or virulent properties displayed by a strain is determined by a complex balance between the status of the host and the production of virulence factors in the bacteria. The role of the intrinsic virulence of the isolates needs to be clarified and molecular markers of virulence are required to predict the invasiveness of clinical strains isolated during the course of extraintestinal infection or patient colonization.E. coli has a clonal genetic structure and exhibits a low level of recombination [2]. E. col
Influence of hydrological conditions on the Escherichia coli population structure in the water of a creek on a rural watershed
Mehdy Ratajczak, Emilie Laroche, Thierry Berthe, Olivier Clermont, Barbara Pawlak, Erick Denamur, Fabienne Petit
BMC Microbiology , 2010, DOI: 10.1186/1471-2180-10-222
Abstract: It became apparent, after studying the distribution in the four main E. coli phylo-groups (A, B1, B2, D), the presence of the hly (hemolysin) gene and the antibiotic resistance pattern, that the E. coli population structure was modified not only by the hydrological conditions (dry versus wet periods, rainfall events), but also by how the watershed was used (presence or absence of cattle). Isolates of the B1 phylo-group devoid of hly and sensitive to antibiotics were particularly abundant during the dry period. During the wet period and the rainfall events, contamination from human sources was predominantly characterized by strains of the A phylo-group, whereas contamination by cattle mainly involved B1 phylo-group strains resistant to antibiotics and exhibiting hly. As E. coli B1 was the main phylo-group isolated in water, the diversity of 112 E. coli B1 isolates was further investigated by studying uidA alleles (beta-D-glucuronidase), the presence of hly, the O-type, and antibiotic resistance. Among the forty epidemiolgical types (ETs) identified, five E. coli B1 ETs were more abundant in slightly contaminated water.The structure of an E. coli population in water is not stable, but depends on the hydrological conditions and on current use of the land on the watershed. In our study it was the ratio of A to B1 phylo-groups that changed. However, a set of B1 phylo-group isolates seems to be persistent in water, strengthening the hypothesis that they may correspond to specifically adapted strains.Ensuring the high microbiological quality of environmental water used as a source of recreational or drinking water is an important worldwide problem [1]. Poor microbiological quality of water results from contamination by microorganisms of human or animal fecal origin, and leads to the risk of gastro-enteritis in humans. Such contamination is caused by fecal bacteria from (i) point source pollution, e.g., treated effluents from wastewater treatments plants (WWTPs) which prima
Small variable segments constitute a major type of diversity of bacterial genomes at the species level
Fabrice Touzain, Erick Denamur, Claudine Médigue, Valérie Barbe, Meriem El Karoui, Marie-Agnès Petit
Genome Biology , 2010, DOI: 10.1186/gb-2010-11-4-r45
Abstract: We performed a systematic analysis of the variable segments detected by multiple whole genome alignments at the DNA level on three species for which the greatest number of genomes have been sequenced: Escherichia coli, Staphylococcus aureus, and Streptococcus pyogenes. Among the numerous sites of variability, 62 to 73% were loci of microdiversity, many of which were located within genes. They contribute to phenotypic variations, as 3 to 6% of all genes harbor microdiversity, and 1 to 9% of total genes are located downstream from a microdiversity locus. Microdiversity loci are particularly abundant in genes encoding membrane proteins. In-depth analysis of the E. coli alignments shows that most of the diversity does not correspond to known mobile or repeated elements, and it is likely that they were generated by illegitimate recombination. An intriguing class of microdiversity includes small blocks of highly diverged sequences, whose origin is discussed.This analysis uncovers the importance of this small-sized genome diversity, which we expect to be present in a wide range of bacteria, and possibly also in many eukaryotic genomes.The availability of bacterial genome sequences for closely related strains within a species and software dedicated to multiple genome alignments allow for a novel perspective of bacterial genetic diversity [1-3]. Use of these aligners has led to the notion that bacterial species share a DNA backbone common to all strains interrupted by variable segments (VSs) that are specific to a subset of the aligned strains [4-6]. The most studied category of VSs are genomic islands, which are defined by Vernikos and Parkhill as horizontally acquired mobile elements of limited phylogenetic distribution [7]. These islands are of a large size (30 to 100 kb), and often encode genes critical for pathogenesis [8]. Their integration into genomes presumably occurs by site-specific recombination. Genomic islands may then diffuse from strain to strain by homologou
The CTX-M-15-Producing Escherichia coli Clone O25b: H4-ST131 Has High Intestine Colonization and Urinary Tract Infection Abilities
Sophie Vimont, Anders Boyd, Alexandre Bleibtreu, Marcelle Bens, Jean-Michel Goujon, Louis Garry, Olivier Clermont, Erick Denamur, Guillaume Arlet, Alain Vandewalle
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0046547
Abstract: Increasing numbers of pyelonephritis-associated uropathogenic Escherichia coli (UPEC) are exhibiting high resistance to antibiotic therapy. They include a particular clonal group, the CTX-M-15-producing O25b:H4-ST131 clone, which has been shown to have a high dissemination potential. Here we show that a representative isolate of this E. coli clone, referred to as TN03, has enhanced metabolic capacities, acts as a potent intestine- colonizing strain, and displays the typical features of UPEC strains. In a modified streptomycin-treated mouse model of intestinal colonization where streptomycin was stopped 5 days before inoculation, we show that TN03 outcompetes the commensal E. coli strains K-12 MG1655, IAI1, and ED1a at days 1 and 7. Using an experimental model of ascending UTI in C3H/HeN mice, we then show that TN03 colonized the urinary tract. One week after the transurethral inoculation of the TN03 isolates, the bacterial loads in the bladder and kidneys were significantly greater than those of two other UPEC strains (CFT073 and HT7) belonging to the same B2 phylogenetic group. The differences in bacterial loads did not seem to be directly linked to differences in the inflammatory response, since the intrarenal expression of chemokines and cytokines and the number of polymorphonuclear neutrophils attracted to the site of inflammation was the same in kidneys colonized by TN03, CFT073, or HT7. Lastly, we show that in vitro TN03 has a high maximum growth rate in both complex (Luria-Bertani and human urine) and minimum media. In conclusion, our findings indicate that TN03 is a potent UPEC strain that colonizes the intestinal tract and may persist in the kidneys of infected hosts.
Role of Intraspecies Recombination in the Spread of Pathogenicity Islands within the Escherichia coli Species
S?ren Schubert ,Pierre Darlu,Olivier Clermont,Andreas Wieser,Giuseppe Magistro,Christiane Hoffmann,Kirsten Weinert,Olivier Tenaillon,Ivan Matic,Erick Denamur
PLOS Pathogens , 2009, DOI: 10.1371/journal.ppat.1000257
Abstract: Horizontal gene transfer is a key step in the evolution of bacterial pathogens. Besides phages and plasmids, pathogenicity islands (PAIs) are subjected to horizontal transfer. The transfer mechanisms of PAIs within a certain bacterial species or between different species are still not well understood. This study is focused on the High-Pathogenicity Island (HPI), which is a PAI widely spread among extraintestinal pathogenic Escherichia coli and serves as a model for horizontal transfer of PAIs in general. We applied a phylogenetic approach using multilocus sequence typing on HPI-positive and -negative natural E. coli isolates representative of the species diversity to infer the mechanism of horizontal HPI transfer within the E. coli species. In each strain, the partial nucleotide sequences of 6 HPI–encoded genes and 6 housekeeping genes of the genomic backbone, as well as DNA fragments immediately upstream and downstream of the HPI were compared. This revealed that the HPI is not solely vertically transmitted, but that recombination of large DNA fragments beyond the HPI plays a major role in the spread of the HPI within E. coli species. In support of the results of the phylogenetic analyses, we experimentally demonstrated that HPI can be transferred between different E. coli strains by F-plasmid mediated mobilization. Sequencing of the chromosomal DNA regions immediately upstream and downstream of the HPI in the recipient strain indicated that the HPI was transferred and integrated together with HPI–flanking DNA regions of the donor strain. The results of this study demonstrate for the first time that conjugative transfer and homologous DNA recombination play a major role in horizontal transfer of a pathogenicity island within the species E. coli.
Phylogenetic and genomic diversity of human bacteremic Escherichia coli strains
Fran?oise Jaureguy, Luce Landraud, Virginie Passet, Laure Diancourt, Eric Frapy, Ghislaine Guigon, Etienne Carbonnelle, Olivier Lortholary, Olivier Clermont, Erick Denamur, Bertrand Picard, Xavier Nassif, Sylvain Brisse
BMC Genomics , 2008, DOI: 10.1186/1471-2164-9-560
Abstract: Recombination-insensitive phylogenetic analysis of MLST data in combination with the ECOR collection revealed that bacteremic E. coli isolates were highly diverse and distributed into five major lineages, corresponding to the classical E. coli phylogroups (A+B1, B2, D and E) and group F, which comprises strains previously assigned to D. Compared to other strains of phylogenetic group B2, strains belonging to MLST-derived clonal complexes (CCs) CC1 and CC4 were associated (P < 0.05) with a urinary origin. In contrast, no CC appeared associated with severe sepsis or unfavorable outcome of the bacteremia. CGH analysis revealed genomic characteristics of the distinct CCs and identified genomic regions associated with CC1 and/or CC4.Our results demonstrate that human bacteremia strains distribute over the entire span of E. coli phylogenetic diversity and that CCs represent important phylogenetic units for pathogenesis and comparative genomics.Escherichia coli is the most abundant facultative anaerobic bacteria of the human intestinal flora. Whereas E. coli usually appears to be a harmless commensal, in other circumstances, E. coli strains can be pathogenic to humans and were grouped into various pathotypes [1]. Among these, extraintestinal pathogenic Escherichia coli (ExPEC) are responsible for urinary tract, intra-abdominal and soft tissue infections, meningitis, pneumonia and osteomyelitis often associated to bacteremia [2]. Bacteremia represents the tenth major cause of death in developed countries and among Gram-negative bacteria, Escherichia coli represents the first cause of bacteremia, with 30% of the total number of bacteremias being due to this pathogen [3].Among bacteremic isolates, those that are characterized by specific virulence factors (VFs) such as adhesins, capsule, cytotoxins and siderophores are considered as extraintestinal pathogenic E. coli (ExPEC) [2], as these VFs are classically described as being necessary to overcome host defenses, invade host
Variation in endogenous oxidative stress in Escherichia coli natural isolates during growth in urine
Cécile Aubron, Jéremy Glodt, Corine Matar, Oliver Huet, Didier Borderie, Ulrich Dobrindt, Jacques Duranteau, Erick Denamur, Marc Conti, Odile Bouvet
BMC Microbiology , 2012, DOI: 10.1186/1471-2180-12-120
Abstract: During exponential growth in urine, TBARS level differs between strains, without correlation with the ability to grow in urine which was similarly limited for commensal, ABU and uropathogenic strains. In addition, no correlation between TBARS level and the phylogroup or pathogenic group is apparent. The growth of ABU strain 83972 was associated with a high level of TBARS and more active antioxidant defenses that reduce the imbalance.Our results indicate that growth capacity in urine is not a property of ABU strains. However, E. coli isolates respond very differently to this stressful environment. In strain ABU 83972, on one hand, the increased level of endogenous reactive oxygen species may be responsible for adaptive mutations. On the other hand, a more active antioxidant defense system could increase the capacity to colonize the bladder.
Virulence Patterns in a Murine Sepsis Model of ST131 Escherichia coli Clinical Isolates Belonging to Serotypes O25b:H4 and O16:H5 Are Associated to Specific Virotypes
Azucena Mora, Ghizlane Dahbi, Cecilia López, Rosalía Mamani, Juan Marzoa, Sara Dion, Bertrand Picard, Miguel Blanco, María Pilar Alonso, Erick Denamur, Jorge Blanco
PLOS ONE , 2014, DOI: 10.1371/journal.pone.0087025
Abstract: Escherichia coli sequence type (ST)131 is an emerging disseminated public health threat implicated in multidrug-resistant extraintestinal infections worldwide. Although the majority of ST131 isolates belong to O25b:H4 serotype, new variants with different serotypes, STs using the discriminative multilocus sequence typing scheme of Pasteur Institute, and virulence-gene profiles (virotypes) have been reported with unknown implications on the pattern of spread, persistence and virulence. The aim of the present study was to compare virulence in a mouse subcutaneous sepsis model of representative ST131 clinical isolates belonging to 2 serotypes (O25b:H4, O16:H5) and nine virotypes and subtypes (A, B, C, D1, D2, D3, D4, D5 and E). Fourteen out of the 23 ST131 isolates tested (61%) killed 90 to 100% of mice challenged, and 18 of 23 (78%) at least 50%. Interestingly, different virulence patterns in association with virotypes were observed, from highly rapid lethality (death in less than 24 h) to low final lethality (death at 7 days) but with presence of an acute inflammation. This is the first study to assess virulence of ST131 isolates belonging to serotype O16:H5, which exhibited virotype C. In spite of their low virulence-gene score, O16:H5 isolates did not show significant differences in final lethality compared with highly virulent O25b:H4 isolates of virotypes A, B and C, but killed mice less rapidly. Significant differences were found, however, between virotypes A, B, C (final lethality ≥80% of mice challenged) and virotypes D, E. Particularly unexpected was the low lethality of the newly assigned virotype E taking into account that it exhibited high virulence-gene score, and the same clonotype H30 as highly virulent O25b:H4 isolates of virotypes A, B and C. In vivo virulence diversity reported in this study would reflect the genetic variability within ST131 clonal group evidenced by molecular typing.
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