Phylogenetics of family Enterobacteriaceae and proposal to reclassify Escherichia hermannii and Salmonella subterranea as Atlantibacter hermannii and Atlantibacter subterranea gen. nov., comb. nov.
Abstract:Multilocus sequence analysis based on hypervariable housekeeping proteins was utilized to differentiate closely related species in the family Enterobacteriaceae. Of 150 housekeeping proteins, the top 10 hypervariable proteins were selected and concatenated to obtain distance data. Distances between concatenated proteins within the family were 0.9-41.2%, whereas the 16S rRNA and atpD-gyrB-infB-rpoB concatenated sequence (4MLSA) distances were 0.8-6.0% and 0.9-22.1%, respectively. These data indicate that phylog… Show more
“…The conserved region is completely absent from non-enterobacteriaceal Gram-negative bacteria, such as Acinetobacter, Haemophilus, Pasteurella, Prevotella and Pseudomonas species. Combined with previous studies on the phylogeny of Enterobacteriaceae [19–23], these observations are indicative of an ancient MGI that spread among the enterobacteriaceal ancestry, before genera like Enterobacter, Escherichia , and Klebsiella evolved.10.1080/21505594.2018.1509666-F0002Figure 2.Similarity among MIR17-GI-like MGIs and schematic representation of the P4-like prophage at the 3ʹ end of MIR17-GI. (a) MIR17-GI-like MGIs identified in the four study isolates and E. coli K12 MG1655.…”
The exchange of mobile genomic islands (MGIs) between microorganisms is often mediated by phages, which may provide benefits to the phage’s host. The present study started with the identification of Enterobacter cloacae, Klebsiella pneumoniae and Escherichia coli isolates with exceptional cephalosporin and carbapenem resistance phenotypes from patients in a neonatal ward. To identify possible molecular connections between these isolates and their β-lactam resistance phenotypes, the respective bacterial genome sequences were compared. This unveiled the existence of a family of ancient MGIs that were probably exchanged before the species E. cloacae, K. pneumoniae and E. coli emerged from their common ancestry. A representative MGI from E. cloacae was named MIR17-GI, because it harbors the novel β-lactamase gene variant blaMIR17. Importantly, our observations show that the MIR17-GI-like MGIs harbor genes associated with high-level resistance to cephalosporins. Among them, MIR17-GI stands out because MIR17 also displays carbapenemase activity. As shown by mass spectrometry, the MIR17 carbapenemase is among the most abundantly expressed proteins of the respective E. cloacae isolate. Further, we show that MIR17-GI-like islands are associated with integrated P4-like prophages. This implicates phages in the spread of cephalosporin and carbapenem resistance amongst Enterobacteriaceae. The discovery of an ancient family of MGIs, mediating the spread of cephalosporinase and carbapenemase genes, is of high clinical relevance, because high-level cephalosporin and carbapenem resistance have serious implications for the treatment of patients with enterobacteriaceal infections.
“…The conserved region is completely absent from non-enterobacteriaceal Gram-negative bacteria, such as Acinetobacter, Haemophilus, Pasteurella, Prevotella and Pseudomonas species. Combined with previous studies on the phylogeny of Enterobacteriaceae [19–23], these observations are indicative of an ancient MGI that spread among the enterobacteriaceal ancestry, before genera like Enterobacter, Escherichia , and Klebsiella evolved.10.1080/21505594.2018.1509666-F0002Figure 2.Similarity among MIR17-GI-like MGIs and schematic representation of the P4-like prophage at the 3ʹ end of MIR17-GI. (a) MIR17-GI-like MGIs identified in the four study isolates and E. coli K12 MG1655.…”
The exchange of mobile genomic islands (MGIs) between microorganisms is often mediated by phages, which may provide benefits to the phage’s host. The present study started with the identification of Enterobacter cloacae, Klebsiella pneumoniae and Escherichia coli isolates with exceptional cephalosporin and carbapenem resistance phenotypes from patients in a neonatal ward. To identify possible molecular connections between these isolates and their β-lactam resistance phenotypes, the respective bacterial genome sequences were compared. This unveiled the existence of a family of ancient MGIs that were probably exchanged before the species E. cloacae, K. pneumoniae and E. coli emerged from their common ancestry. A representative MGI from E. cloacae was named MIR17-GI, because it harbors the novel β-lactamase gene variant blaMIR17. Importantly, our observations show that the MIR17-GI-like MGIs harbor genes associated with high-level resistance to cephalosporins. Among them, MIR17-GI stands out because MIR17 also displays carbapenemase activity. As shown by mass spectrometry, the MIR17 carbapenemase is among the most abundantly expressed proteins of the respective E. cloacae isolate. Further, we show that MIR17-GI-like islands are associated with integrated P4-like prophages. This implicates phages in the spread of cephalosporin and carbapenem resistance amongst Enterobacteriaceae. The discovery of an ancient family of MGIs, mediating the spread of cephalosporinase and carbapenemase genes, is of high clinical relevance, because high-level cephalosporin and carbapenem resistance have serious implications for the treatment of patients with enterobacteriaceal infections.
“…The listing of microbiome taxa was organized in rows that followed as close as possible the sequence derived from detailed phylogenetic analysis, from late diverging down to deep branching organisms in each class of proteobacteria. The phylogenetic position of the various taxa was evaluated by combining relevant studies on the phylogenesis of alpha [57–59], gamma [60–62] and delta proteobacteria [63–65] with detailed analysis of conserved proteins carried out as described earlier [37,38,49,62,66]. The proteins include the catalytic subunit of aa3- and bd-type oxidases, which are not present in all proteobacteria [37,62], the NuoD and NuoL subunits of complex I [38,49], the catalytic subunit of [FeFe]-hydrogenase [6,57], cytochrome b of the bc1 complex [66], the flavoprotein subunit SdhA of succinate dehydrogenase and its related protein of fumarate reductase [67].…”
Many studies on the microbiome of animals have been reported but a comprehensive analysis is lacking. Here we present a meta-analysis on the microbiomes of arthropods and their terrestrial habitat, focusing on the functional profile of bacterial communities derived from metabolic traits that are essential for microbial life. We report a detailed analysis of probably the largest set of biochemically defined functional traits ever examined in microbiome studies. This work deals with the phylum proteobacteria, which is usually dominant in marine and terrestrial environments and covers all functions associated with microbiomes. The considerable variation in the distribution and abundance of proteobacteria in microbiomes has remained fundamentally unexplained. This analysis reveals discrete functional groups characteristic for adaptation to anaerobic conditions, which appear to be defined by environmental filtering of taxonomically related taxa. The biochemical diversification of the functional groups suggests an evolutionary trajectory in the structure of arthropods’ microbiome, from metabolically versatile to specialized proteobacterial organisms that are adapted to complex environments such as the gut of social insects. Bacterial distribution in arthropods’ microbiomes also shows taxonomic clusters that do not correspond to functional groups and may derive from other factors, including common contaminants of soil and reagents.
“…In the absence of an isolated organism, putative novel species can be determined by genetic content alone but are termed genomospecies. In addition, recognized species can also be reclassified such as Escherichia hermannii and Salmonella subterranea to Atlantibacter hermannii and Atlantibacter subterranea, respectively (10 ). Given the previous analysis on Gardnerella, we used multiple in silico taxonomic classification tools to bin publicly available Gardnerella genomes into different genomospecies and then performed comparative analysis between the genomospecies.…”
BACKGROUND
Gardnerella vaginalis is implicated as one of the causative agents of bacterial vaginosis, but it can also be isolated from the vagina of healthy women. Previous efforts to study G. vaginalis identified 4 to 6 clades, but average nucleotide identity analysis indicates that G. vaginalis may be multiple species. Recently, Gardnerella was determined to be 13 genomospecies, with Gardnerella piottii, Gardnerella leopoldii, and Gardnerella swidsinkii delineated as separate species.
METHODS
We accessed 103 publicly available genomes annotated as G. vaginalis. We performed comprehensive taxonomic and phylogenomic analysis to quantify the number of species called G. vaginalis, the similarity of their core genes, and their burden of their accessory genes. We additionally analyzed publicly available metatranscriptomic data sets of bacterial vaginosis to determine whether the newly delineated genomospecies are present, and to identify putative conserved features of Gardnerella pathogenesis.
RESULTS
Gardnerella could be classified into 8 to 14 genomospecies depending on the in silico classification tools used. Consensus classification identified 9 different Gardnerella genomospecies, here annotated as GS01 through GS09. The genomospecies could be readily distinguished by the phylogeny of their shared genes and burden of accessory genes. All of the new genomospecies were identified in metatranscriptomes of bacterial vaginosis.
CONCLUSIONS
Multiple Gardnerella genomospecies operating in isolation or in concert with one another may be responsible for bacterial vaginosis. These results have important implications for future efforts to understand the evolution of the Gardnerella genomospecies, host–pathogen interactions of the genomospecies during bacterial vaginosis, diagnostic assay development for bacterial vaginosis, and metagenomic investigations of the vaginal microbiota.
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