Conserved indels in essential proteins that are distinctive characteristics of Chlamydiales and provide novel means for their identification

Griffiths, Emma; Petrich, Astrid; Gupta, Radhey S.

doi:10.1099/mic.0.28057-0

Cited by 38 publications

(32 citation statements)

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“…The presence of these Clostridium-specific signatures in these species would provide a strong case for their transfer to the genus Clostridium. Because all of the conserved indels described here are found in highly conserved regions, it should be possible to obtain sequence information for these signatures from other species by using degenerate PCR primers flanking the indel-containing regions, as described in our other work (Griffiths et al, 2005;Gao & Gupta, 2005).…”

Section: Discussionmentioning

confidence: 99%

Phylogenomic analyses of clostridia and identification of novel protein signatures that are specific to the genus Clostridium sensu stricto (cluster I)

Gupta

Gao

2009

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLO

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The species of Clostridium comprise a very heterogeneous assemblage of bacteria that do not form a phylogenetically coherent group. It has been proposed previously that only a subset of the species of Clostridium that form a distinct cluster in the 16S rRNA tree (cluster I) should be regarded as the true representatives of the genus Clostridium (i.e. Clostridium sensu stricto). However, this cluster is presently defined only in phylogenetic terms, and no biochemical, molecular or phenotypic characteristic is known that is unique to species from this cluster. We report here phylogenomic and comparative analyses based on sequenced clostridial genomes in an attempt to bridge this gap and to clarify the evolutionary relationships among species of clostridia. In phylogenetic trees for species of clostridia based on concatenated sequences for 37 highly conserved proteins, the species of Clostridium cluster I formed a strongly supported clade that was separated from all other clostridia by a long branch. Several other Clostridium species that are not part of this cluster grouped reliably with other species of clostridia in a number of wellresolved clades. Our comparative genomic analyses have identified three conserved indels in three highly conserved proteins (a 4 aa insert in DNA gyrase A, a 1 aa deletion in ATP synthase beta subunit and a 1 aa insert in ribosomal protein S2) that are unique to the species of Clostridium cluster I and are not found in any other bacteria. BLASTP searches on various proteins in the genomes of Clostridium tetani E88 and Clostridium perfringens SM101 have also identified more than 10 proteins that are found uniquely in the cluster I species. These results provide evidence that the species of Clostridium cluster I not only are phylogenetically distinct but also share many unique molecular characteristics. These newly identified molecular markers provide useful tools to define and circumscribe the genus Clostridium sensu stricto in more definitive terms. We have also identified a 7-9 aa conserved insert in the enzyme phosphoglycerate dehydrogenase that is uniquely found in the Clostridium thermocellum, Thermoanaerobacter pseudethanolicus, Thermoanaerobacter tengcogensis and Caldicellulosiruptor saccharolyticus homologues, and is absent from all other bacteria. These species form a well-defined clade in the phylogenetic trees and this indel provides a potential molecular marker for this clostridial cluster. INTRODUCTIONThe species belonging to the genus Clostridium comprise a heterogeneous assemblage that does not form a monophyletic grouping in phylogenetic trees based on different gene/protein sequences (Cato et al., 1986;Lawson et al., 1993;Stackebrandt et al., 1999;Finegold et al., 2002;Wiegel et al., 2006). Many species were originally assigned to this genus based on their being Gram-positive, anaerobic rods that are capable of endospore formation (Cato et al., 1986;Cato & Stackebrandt, 1989;Lawson et al., 1993;Finegold et al., 2002;Rood, 2006). However, these criteria led to the place...

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Section: Discussionmentioning

confidence: 99%

Phylogenomic analyses of clostridia and identification of novel protein signatures that are specific to the genus Clostridium sensu stricto (cluster I)

Gupta

Gao

2009

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLO

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“…indels or signature sequences) in gene/protein sequences that are uniquely shared by particular groups of species provide valuable markers for taxonomic and evolutionary studies (Gupta & Griffiths, 2006). We recently described a number of conserved indels in proteins such as RpoA, EFTu, EF-P, gyrase B and LysRS, that based upon the available information were distinctive characteristics of the Chlamydiales species (Griffiths et al, 2005). Due to lack of sequence information, the presence of these signatures in Verrucomicrobium was not determined.…”

Section: Conserved Inserts In Lysrs and Rpob Proteins That Are Uniquementioning

confidence: 99%

“…indels) in protein sequences provides a powerful tool for evolutionary relationships among distantly related groups (Gupta & Griffiths, 2006). In earlier work, we have described many conserved indels in protein sequences that are either specific for the chlamydiae species or provide information regarding their branching relative to other bacterial phyla (Griffiths & Gupta, 2001;Griffiths et al, 2005;Gupta & Griffiths, 2006). In this work, we have examined the evolutionary relationships among chlamydiae, Verrucomicrobia and Planctomycetes by traditional phylogenetic methods as well as by identifying conserved indels in protein sequences that are uniquely shared by species from these groups.…”

Section: Introductionmentioning

confidence: 99%

“…The final alignment file, which contained 5093 positions, is available as Supplementary Data with online version of this paper. Bootstrapped phylogenetic trees for this alignment were constructed by neighbour-joining (NJ), maximum-likelihood (ML) and maximum-parsimony (MP) methods, as described in our recent work (Gupta & Sneath, 2006).The conserved insert in RpoB that is specific for the chlamydiae and Verrucomicrobia was identified by visual inspection of different sequence alignments (Griffiths et al, 2005). The insert in the lysyltRNA synthetase (LysRS) was previously identified as a Chlamydialesspecific signature (Griffiths et al, 2005).…”

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confidence: 99%

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Phylogeny and shared conserved inserts in proteins provide evidence that Verrucomicrobia are the closest known free-living relatives of chlamydiae

Griffiths

Gupta

2007

Microbiology

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The evolutionary relationships of Chlamydiales, Verrucomicrobia and Planctomycetes were studied based on phylogenetic trees for a concatenated dataset of 11 widely distributed proteins, as well as conserved inserts in several proteins. In phylogenetic trees, a close relationship of chlamydiae to Verrucomicrobium was supported by different phylogenetic methods. Although the Planctomycetes branched close to the chlamydiae-Verrucomicrobia clade, their specific affiliation to these groups was generally not supported. Results are also presented for two conserved inserts, a 6 aa insert in the lysyl-tRNA synthetase and a 3 aa insert in the RNA polymerase b subunit (RpoB), that are uniquely shared by Verrucomicrobium spinosum and all available Chlamydiales homologues, but which are not found in any of the available Planctomycetes or other bacterial homologues. Signature sequences in a number of other proteins [including a large insert (.150 aa) in DNA gyrase B] provide information regarding the branching position of these groups relative to other bacterial phyla. A close and specific relationship of V. spinosum to the Chlamydiales species, seen both in phylogenetic trees and by means of uniquely shared inserts in protein sequences, strongly indicates that these two groups of species shared a common ancestor exclusive of all other known bacteria. These results suggest that Verrucomicrobia may be the closest free-living relatives of the parasitic chlamydiae. INTRODUCTIONThe Chlamydiales, Verrucomicrobia and Planctomycetes are presently recognized as three main phyla within Bacteria (Everett et al., 1999;Garrity et al., 2005;Schelsner et al., 2006;Ward et al., 2006). Of these, all known chlamydiae species are obligate intracellular parasites of eukaryotic hosts and they are responsible for a wide spectrum of diseases in humans and animals (Everett et al., 1999;Corsaro & Greub, 2006). The verrucomicrobia and planctomycetes species are found in a wide variety of terrestrial and aquatic environments (Strous et al., 2006;Schelsner et al., 2006;Ward et al., 2006). Although most of them are free-living bacteria, several live in close association with eukaryotic hosts, including some verrucomicrobia species that are endosymbionts of nematodes and ciliates (Wagner & Horn, 2006;Schelsner et al., 2006;Ward et al., 2006). Of these three groups, chlamydiae and planctomycetes, unlike most other bacteria, contain no detectable peptidoglycan in their cell envelopes (Konig et al., 1984; Fox et al., 1990;Ward et al., 2006). The evolutionary relationships among these three lineages are presently not resolved (Ward et al., 2000;Jenkins & Fuerst, 2001;Teeling et al., 2004; Ciccarelli et al., 2006;Wagner & Horn, 2006;Strous et al., 2006;Schelsner et al., 2006;Ward et al., 2006). Wagner & Horn (2006) reported a monophyletic grouping of these three lineages in the 16S rRNA trees, but the bootstrap support of the combined clade was not high. A grouping of the Planctomycetes with chlamydiae was also seen in phylogenetic trees based on concatenated...

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“…In this context it is important to know that new environmental Chlamydia species are steadily described. 8,9 There is ample evidence for a huge diversity and wide distribution of Chlamydiae in nature-and we are exposed to that diversity of species. For example, until recently the recovery of a novel environmental Chlamydia strain from activated sludge by cocultivation with Acanthamoeba species was reported, 8 and it was shown that it is also able to invade mammalian cells.…”

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confidence: 99%

Chlamydia pneumoniae , Stroke, and Serological Associations

Apfalter

2006

Stroke

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There are now more arguments against than for a causal relationship between C. pneumoniae and atherosclerosis. Seroepidemiologic results are largely technique-dependent; PCR results show intra-and interlaboratory variability; methodological factors contribute to bias; and detection of C. pneumoniae fails when the specificity of the reaction is optimized. Immunohistochemical staining detects nonspecific compounds in atherosclerotic lesions, and secondary prevention trials are unsuccessful. The evidence for an association between a pathogen and a chronic disease should be based on concordance of evidence arising from different approaches applied by different groups, at different times, in different places, and under different circumstances. None of these conditions have been fulfilled in the case of C. pneumoniae and atherosclerosis. 1

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Conserved indels in essential proteins that are distinctive characteristics of Chlamydiales and provide novel means for their identification

Cited by 38 publications

References 49 publications

Phylogenomic analyses of clostridia and identification of novel protein signatures that are specific to the genus Clostridium sensu stricto (cluster I)

Phylogenomic analyses of clostridia and identification of novel protein signatures that are specific to the genus Clostridium sensu stricto (cluster I)

Phylogeny and shared conserved inserts in proteins provide evidence that Verrucomicrobia are the closest known free-living relatives of chlamydiae

Chlamydia pneumoniae , Stroke, and Serological Associations

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