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1.
Front Microbiol ; 5: 140, 2014.
Article in English | MEDLINE | ID: mdl-24782836

ABSTRACT

The Halobacteria are known to engage in frequent gene transfer and homologous recombination. For stably diverged lineages to persist some checks on the rate of between lineage recombination must exist. We surveyed a group of isolates from the Aran-Bidgol endorheic lake in Iran and sequenced a selection of them. Multilocus Sequence Analysis (MLSA) and Average Nucleotide Identity (ANI) revealed multiple clusters (phylogroups) of organisms present in the lake. Patterns of intein and Clustered Regularly Interspaced Short Palindromic Repeats (CRISPRs) presence/absence and their sequence similarity, GC usage along with the ANI and the identities of the genes used in the MLSA revealed that two of these clusters share an exchange bias toward others in their phylogroup while showing reduced rates of exchange with other organisms in the environment. However, a third cluster, composed in part of named species from other areas of central Asia, displayed many indications of variability in exchange partners, from within the lake as well as outside the lake. We conclude that barriers to gene exchange exist between the two purely Aran-Bidgol phylogroups, and that the third cluster with members from other regions is not a single population and likely reflects an amalgamation of several populations.

2.
Mol Biol Evol ; 30(12): 2676-87, 2013 Dec.
Article in English | MEDLINE | ID: mdl-24048585

ABSTRACT

Inteins are self-splicing parasitic genetic elements found in all domains of life. These genetic elements are found in highly conserved positions in conserved proteins. One protein family that has been invaded by inteins is the vacuolar and archaeal catalytic ATPase subunits (vma-1). There are two intein insertion sites in this protein, "a" and "b." The b site was previously thought to be only invaded in archaeal lineages. Here we survey the distribution and evolutionary histories of the b site inteins and show that the intein is present in more lineages than previously annotated, including a bacterial lineage, Mahella australiensis 50-1 BON. We present evidence, through ancestral character state reconstruction and substitution ratios between host genes and inteins, for several transfers of this intein between divergent species, including an interdomain transfer between the archaea and bacteria. Although inteins may persist within a single population or species for long periods of time, transfer of the vma-1b intein between divergent species contributed to the distribution of this intein.


Subject(s)
Archaea/genetics , Bacteria/genetics , Evolution, Molecular , Inteins/genetics , Vacuolar Proton-Translocating ATPases/genetics , Amino Acid Substitution , Archaea/classification , Archaea/enzymology , Bacteria/enzymology , Gene Transfer, Horizontal , Genes, Archaeal , Genes, Bacterial , Phylogeny , Ribosomes/genetics
4.
Appl Environ Microbiol ; 79(22): 7006-12, 2013 Nov.
Article in English | MEDLINE | ID: mdl-24014541

ABSTRACT

We recently reported that the Thermotogales acquired the ability to synthesize vitamin B12 by acquisition of genes from two distantly related lineages, Archaea and Firmicutes (K. S. Swithers et al., Genome Biol. Evol. 4:730-739, 2012). Ancestral state reconstruction suggested that the cobinamide salvage gene cluster was present in the Thermotogales' most recent common ancestor. We also predicted that Thermotoga lettingae could not synthesize B12 de novo but could use the cobinamide salvage pathway to synthesize B12. In this study, these hypotheses were tested, and we found that Tt. lettingae did not synthesize B12 de novo but salvaged cobinamide. The growth rate of Tt. lettingae increased with the addition of B12 or cobinamide to its medium. It synthesized B12 when the medium was supplemented with cobinamide, and no B12 was detected in cells grown on cobinamide-deficient medium. Upstream of the cobinamide salvage genes is a putative B12 riboswitch. In other organisms, B12 riboswitches allow for higher transcriptional activity in the absence of B12. When Tt. lettingae was grown with no B12, the salvage genes were upregulated compared to cells grown with B12 or cobinamide. Another gene cluster with a putative B12 riboswitch upstream is the btuFCD ABC transporter, and it showed a transcription pattern similar to that of the cobinamide salvage genes. The BtuF proteins from species that can and cannot salvage cobinamides were shown in vitro to bind both B12 and cobinamide. These results suggest that Thermotogales species can use the BtuFCD transporter to import both B12 and cobinamide, even if they cannot salvage cobinamide.


Subject(s)
ATP-Binding Cassette Transporters/metabolism , Bacterial Proteins/metabolism , Cobamides/metabolism , Gram-Negative Anaerobic Straight, Curved, and Helical Rods/genetics , Vitamin B 12/biosynthesis , ATP-Binding Cassette Transporters/genetics , Bacterial Proteins/genetics , Culture Media/chemistry , Genes, Bacterial , Gram-Negative Anaerobic Straight, Curved, and Helical Rods/isolation & purification , Multigene Family , RNA, Bacterial/genetics , Riboswitch/genetics , Up-Regulation
5.
Mol Biol Evol ; 30(11): 2463-74, 2013 Nov.
Article in English | MEDLINE | ID: mdl-23966548

ABSTRACT

Optimal growth temperature is a complex trait involving many cellular components, and its physiology is not yet fully understood. Evolution of continuous characters, such as optimal growth temperature, is often modeled as a one-dimensional random walk, but such a model may be an oversimplification given the complex processes underlying the evolution of continuous characters. Recent articles have used ancestral sequence reconstruction to infer the optimal growth temperature of ancient organisms from the guanine and cytosine content of the stem regions of ribosomal RNA, allowing inferences about the evolution of optimal growth temperature. Here, we investigate the optimal growth temperature of the bacterial phylum Thermotogae. Ancestral sequence reconstruction using a nonhomogeneous model was used to reconstruct the stem guanine and cytosine content of 16S rRNA sequences. We compare this sequence reconstruction method with other ancestral character reconstruction methods, and show that sequence reconstruction generates smaller confidence intervals and different ancestral values than other reconstruction methods. Unbiased random walk simulation indicates that the lower temperature members of the Thermotogales have been under directional selection; however, when a simulation is performed that takes possible mutations into account, it is the high temperature lineages that are, in fact, under directional selection. We find that the evolution of Thermotogales optimal growth temperatures is best fit by a biased random walk model. These findings suggest that it may be easier to evolve from a high optimal growth temperature to a lower one than vice versa.


Subject(s)
Evolution, Molecular , Gram-Negative Anaerobic Straight, Curved, and Helical Rods/growth & development , Gram-Negative Anaerobic Straight, Curved, and Helical Rods/genetics , RNA, Bacterial/genetics , RNA, Ribosomal, 16S/genetics , Base Composition , Cold Temperature , Computer Simulation , Gram-Negative Anaerobic Straight, Curved, and Helical Rods/classification , Models, Biological , Mutation , Phylogeny , RNA, Bacterial/chemistry , RNA, Bacterial/metabolism , RNA, Ribosomal, 16S/chemistry , RNA, Ribosomal, 16S/metabolism , Selection, Genetic
6.
PLoS One ; 8(12): e84300, 2013.
Article in English | MEDLINE | ID: mdl-24391933

ABSTRACT

The bacterial genomes of Thermotoga species show evidence of significant interdomain horizontal gene transfer from the Archaea. Members of this genus acquired many genes from the Thermococcales, which grow at higher temperatures than Thermotoga species. In order to study the functional history of an interdomain horizontally acquired gene we used ancestral sequence reconstruction to examine the thermal characteristics of reconstructed ancestral proteins of the Thermotoga lineage and its archaeal donors. Several ancestral sequence reconstruction methods were used to determine the possible sequences of the ancestral Thermotoga and Archaea myo-inositol-3-phosphate synthase (MIPS). These sequences were predicted to be more thermostable than the extant proteins using an established sequence composition method. We verified these computational predictions by measuring the activities and thermostabilities of purified proteins from the Thermotoga and the Thermococcales species, and eight ancestral reconstructed proteins. We found that the ancestral proteins from both the archaeal donor and the Thermotoga most recent common ancestor recipient were more thermostable than their descendants. We show that there is a correlation between the thermostability of MIPS protein and the optimal growth temperature (OGT) of its host, which suggests that the OGT of the ancestors of these species of Archaea and the Thermotoga grew at higher OGTs than their descendants.


Subject(s)
Adaptation, Biological/genetics , Computational Biology/methods , Evolution, Molecular , Hot Temperature , Intramolecular Lyases/genetics , Thermococcales/enzymology , Thermotoga maritima/enzymology , Archaea/enzymology , Archaea/genetics , Gene Transfer, Horizontal/genetics , Likelihood Functions , Models, Genetic , Phylogeny , Species Specificity , Thermococcales/genetics , Thermotoga maritima/genetics
7.
Int J Evol Biol ; 2012: 418964, 2012.
Article in English | MEDLINE | ID: mdl-22844638

ABSTRACT

Reticulate evolution encompasses processes that conflict with traditional Tree of Life efforts. These processes, horizontal gene transfer (HGT), gene and whole-genome duplications through allopolyploidization, are some of the main driving forces for generating innovation and complexity. HGT has a profound impact on prokaryotic and eukaryotic evolution. HGTs can lead to the invention of new metabolic pathways and the expansion and enhancement of previously existing pathways. It allows for organismal adaptation into new ecological niches and new host ranges. Although many HGTs appear to be selected for because they provide some benefit to their recipient lineage, other HGTs may be maintained by chance through random genetic drift. Moreover, some HGTs that may initially seem parasitic in nature can cause complexity to arise through pathways of neutral evolution. Another mechanism for generating innovation and complexity, occurring more frequently in eukaryotes than in prokaryotes, is gene and genome duplications, which often occur through allopolyploidizations. We discuss how these different evolutionary processes contribute to generating innovation and complexity.

8.
PLoS One ; 7(6): e40236, 2012.
Article in English | MEDLINE | ID: mdl-22768259

ABSTRACT

The unifying structural characteristic of members of the bacterial order Thermotogales is their toga, an unusual cell envelope that includes a loose-fitting sheath around each cell. Only two toga-associated structural proteins have been purified and characterized in Thermotoga maritima: the anchor protein OmpA1 (or Ompα) and the porin OmpB (or Ompß). The gene encoding OmpA1 (ompA1) was cloned and sequenced and later assigned to TM0477 in the genome sequence, but because no peptide sequence was available for OmpB, its gene (ompB) was not annotated. We identified six porin candidates in the genome sequence of T. maritima. Of these candidates, only one, encoded by TM0476, has all the characteristics reported for OmpB and characteristics expected of a porin including predominant ß-sheet structure, a carboxy terminus porin anchoring motif, and a porin-specific amino acid composition. We highly enriched a toga fraction of cells for OmpB by sucrose gradient centrifugation and hydroxyapatite chromatography and analyzed it by LC/MS/MS. We found that the only porin candidate that it contained was the TM0476 product. This cell fraction also had ß-sheet character as determined by circular dichroism, consistent with its enrichment for OmpB. We conclude that TM0476 encodes OmpB. A phylogenetic analysis of OmpB found orthologs encoded in syntenic locations in the genomes of all but two Thermotogales species. Those without orthologs have putative isofunctional genes in their place. Phylogenetic analyses of OmpA1 revealed that each species of the Thermotogales has one or two OmpA homologs. T. maritima has two OmpA homologs, encoded by ompA1 (TM0477) and ompA2 (TM1729), both of which were found in the toga protein-enriched cell extracts. These annotations of the genes encoding toga structural proteins will guide future examinations of the structure and function of this unusual lineage-defining cell sheath.


Subject(s)
Bacterial Outer Membrane Proteins/genetics , Cell Membrane/genetics , Evolution, Molecular , Genes, Bacterial/genetics , Proteomics/methods , Thermotoga maritima/genetics , Amino Acid Sequence , Bacterial Outer Membrane Proteins/isolation & purification , Base Sequence , Centrifugation, Density Gradient , Chromatography , Circular Dichroism , Durapatite , Likelihood Functions , Molecular Sequence Data , Phylogeny , Porins/chemistry , Porins/genetics , Protein Multimerization , Sequence Homology, Nucleic Acid , Species Specificity , Synteny/genetics , Thermotoga maritima/cytology
9.
Genome Biol Evol ; 4(8): 700-8, 2012.
Article in English | MEDLINE | ID: mdl-22798451

ABSTRACT

Here we describe the genome of Mesotoga prima MesG1.Ag4.2, the first genome of a mesophilic Thermotogales bacterium. Mesotoga prima was isolated from a polychlorinated biphenyl (PCB)-dechlorinating enrichment culture from Baltimore Harbor sediments. Its 2.97 Mb genome is considerably larger than any previously sequenced Thermotogales genomes, which range between 1.86 and 2.30 Mb. This larger size is due to both higher numbers of protein-coding genes and larger intergenic regions. In particular, the M. prima genome contains more genes for proteins involved in regulatory functions, for instance those involved in regulation of transcription. Together with its closest relative, Kosmotoga olearia, it also encodes different types of proteins involved in environmental and cell-cell interactions as compared with other Thermotogales bacteria. Amino acid composition analysis of M. prima proteins implies that this lineage has inhabited low-temperature environments for a long time. A large fraction of the M. prima genome has been acquired by lateral gene transfer (LGT): a DarkHorse analysis suggests that 766 (32%) of predicted protein-coding genes have been involved in LGT after Mesotoga diverged from the other Thermotogales lineages. A notable example of a lineage-specific LGT event is a reductive dehalogenase gene-a key enzyme in dehalorespiration, indicating M. prima may have a more active role in PCB dechlorination than was previously assumed.


Subject(s)
Genome, Bacterial , Gram-Negative Bacteria/genetics , Bacterial Proteins/genetics , Base Sequence , Gene Transfer, Horizontal , Genome Size , Gram-Negative Bacteria/classification , Molecular Sequence Data , Phylogeny
10.
Genome Biol Evol ; 4(8): 730-9, 2012.
Article in English | MEDLINE | ID: mdl-22798452

ABSTRACT

The availability of genome sequences of Thermotogales species from across the order allows an examination of the evolutionary origins of phenotypic characteristics in this lineage. Several studies have shown that the Thermotogales have acquired large numbers of genes from distantly related lineages, particularly Firmicutes and Archaea. Here, we report the finding that some Thermotogales acquired the ability to synthesize vitamin B(12) by acquiring the requisite genes from these distant lineages. Thermosipho species, uniquely among the Thermotogales, contain genes that encode the means to synthesize vitamin B(12) de novo from glutamate. These genes are split into two gene clusters: the corrinoid synthesis gene cluster, that is unique to the Thermosipho and the cobinamide salvage gene cluster. The corrinoid synthesis cluster was acquired from the Firmicutes lineage, whereas the salvage pathway is an amalgam of bacteria- and archaea-derived proteins. The cobinamide salvage gene cluster has a patchy distribution among Thermotogales species, and ancestral state reconstruction suggests that this pathway was present in the common Thermotogales ancestor. We show that Thermosipho africanus can grow in the absence of vitamin B(12), so its de novo pathway is functional. We detected vitamin B(12) in the extracts of T. africanus cells to verify the synthetic pathway. Genes in T. africanus with apparent B(12) riboswitches were found to be down-regulated in the presence of vitamin B(12) consistent with their roles in B(12) synthesis and cobinamide salvage.


Subject(s)
Bacteria/genetics , Bacteria/metabolism , Bacterial Proteins/genetics , Biosynthetic Pathways , Gene Transfer, Horizontal , Vitamin B 12/biosynthesis , Bacteria/classification , Bacterial Proteins/metabolism , Cobamides/biosynthesis , Molecular Sequence Data , Multigene Family , Phylogeny
11.
Biol Direct ; 6: 45, 2011 Sep 21.
Article in English | MEDLINE | ID: mdl-21936906

ABSTRACT

Phylogenetic reconstruction using DNA and protein sequences has allowed the reconstruction of evolutionary histories encompassing all life. We present and discuss a means to incorporate much of this rich narrative into a single model that acknowledges the discrete evolutionary units that constitute the organism. Briefly, this Rooted Net of Life genome phylogeny is constructed around an initial, well resolved and rooted tree scaffold inferred from a supermatrix of combined ribosomal genes. Extant sampled ribosomes form the leaves of the tree scaffold. These leaves, but not necessarily the deeper parts of the scaffold, can be considered to represent a genome or pan-genome, and to be associated with members of other gene families within that sequenced (pan)genome. Unrooted phylogenies of gene families containing four or more members are reconstructed and superimposed over the scaffold. Initially, reticulations are formed where incongruities between topologies exist. Given sufficient evidence, edges may then be differentiated as those representing vertical lines of inheritance within lineages and those representing horizontal genetic transfers or endosymbioses between lineages.


Subject(s)
Genome, Archaeal , Genome, Bacterial , Models, Genetic , Phylogeny , Ribosomes/genetics , Archaea/genetics , Bacteria/genetics , Biological Evolution , Gene Transfer, Horizontal , Genes, rRNA , Multigene Family , Ribosomal Proteins/genetics
12.
J Bacteriol ; 193(19): 5566-7, 2011 Oct.
Article in English | MEDLINE | ID: mdl-21914881

ABSTRACT

Kosmotoga olearia strain TBF 19.5.1 is a member of the Thermotogales that grows best at 65°C and very well even at 37°C. Information about this organism is important for understanding the evolution of mesophiles from thermophiles. Its genome sequence reveals extensive gene gains and a large content of mobile genetic elements. It also contains putative hydrogenase genes that have no homologs in the other member of the Thermotogales.


Subject(s)
Bacteria/genetics , Bacteria/growth & development , Molecular Sequence Data , North Sea , Petroleum/microbiology , Temperature
13.
J Bacteriol ; 193(20): 5869-70, 2011 Oct.
Article in English | MEDLINE | ID: mdl-21952543

ABSTRACT

Thermotoga sp. strain RQ2 is probably a strain of Thermotoga maritima. Its complete genome sequence allows for an examination of the extent and consequences of gene flow within Thermotoga species and strains. Thermotoga sp. RQ2 differs from T. maritima in its genes involved in myo-inositol metabolism. Its genome also encodes an apparent fructose phosphotransferase system (PTS) sugar transporter. This operon is also found in Thermotoga naphthophila strain RKU-10 but no other Thermotogales. These are the first reported PTS transporters in the Thermotogales.


Subject(s)
Genome, Bacterial , Seawater/microbiology , Thermotoga maritima/genetics , Thermotoga maritima/isolation & purification , Azores , Bacterial Proteins/genetics , Bacterial Proteins/metabolism , Base Sequence , Fructose/metabolism , Hot Temperature , Molecular Sequence Data , Operon , Phosphotransferases/genetics , Phosphotransferases/metabolism , Thermotoga maritima/enzymology , Thermotoga maritima/metabolism
14.
PLoS One ; 6(8): e23774, 2011.
Article in English | MEDLINE | ID: mdl-21876769

ABSTRACT

In 2009, James Lake introduced a new hypothesis in which reticulate phylogeny reconstruction is used to elucidate the origin of gram-negative bacteria (Nature 460: 967-971). The presented data supported the gram-negative bacteria originating from an ancient endosymbiosis between the Actinobacteria and Clostridia. His conclusion was based on a presence-absence analysis of protein families that divided all prokaryotes into five groups: Actinobacteria, Double Membrane bacteria (DM), Clostridia, Archaea and Bacilli. Of these five groups, the DM are by far the largest and most diverse group compared to the other groupings. While the fusion hypothesis for the origin of double membrane bacteria is enticing, we show that the signal supporting an ancient symbiosis is lost when the DM group is broken down into smaller subgroups. We conclude that the signal detected in James Lake's analysis in part results from a systematic artifact due to group size and diversity combined with low levels of horizontal gene transfer.


Subject(s)
Bacteria/genetics , Cell Membrane/metabolism , Membrane Fusion , Models, Biological , Phylogeny , Bacterial Proteins/metabolism
15.
J Biol ; 8(6): 54, 2009.
Article in English | MEDLINE | ID: mdl-19664165

ABSTRACT

Reconstructing the 'Tree of Life' is complicated by extensive horizontal gene transfer between diverse groups of organisms. While numerous conceptual and technical obstacles remain, a report in this issue of Journal of Biology from Koonin and colleagues on the largest-scale prokaryotic genomic reconstruction yet attempted shows that such a tree is discernible, although its branches cannot be traced.


Subject(s)
Bacteria/genetics , Evolution, Molecular , Gene Transfer, Horizontal , Genome, Bacterial , Genes, rRNA , Phylogeny , Species Specificity
16.
Proc Natl Acad Sci U S A ; 106(14): 5865-70, 2009 Apr 07.
Article in English | MEDLINE | ID: mdl-19307556

ABSTRACT

Since publication of the first Thermotogales genome, Thermotoga maritima strain MSB8, single- and multi-gene analyses have disagreed on the phylogenetic position of this order of Bacteria. Here we present the genome sequences of 4 additional members of the Thermotogales (Tt. petrophila, Tt. lettingae, Thermosipho melanesiensis, and Fervidobacterium nodosum) and a comprehensive comparative analysis including the original T. maritima genome. While ribosomal protein genes strongly place Thermotogales as a sister group to Aquificales, the majority of genes with sufficient phylogenetic signal show affinities to Archaea and Firmicutes, especially Clostridia. Indeed, on the basis of the majority of genes in their genomes (including genes that are also found in Aquificales), Thermotogales should be considered members of the Firmicutes. This result highlights the conflict between the taxonomic goal of assigning every species to a unique position in an inclusive Linnaean hierarchy and the evolutionary goal of understanding phylogenesis in the presence of pervasive horizontal gene transfer (HGT) within prokaryotes. Amino acid compositions of reconstructed ancestral sequences from 423 gene families suggest an origin of this gene pool even more thermophilic than extant members of this order, followed by adaptation to lower growth temperatures within the Thermotogales.


Subject(s)
Phylogeny , Thermotoga maritima/classification , Thermotoga maritima/genetics , Environment , Gene Transfer, Horizontal , Genes, Bacterial , Genome, Bacterial , Molecular Sequence Data , Temperature
17.
BMC Evol Biol ; 9: 303, 2009 Dec 31.
Article in English | MEDLINE | ID: mdl-20043855

ABSTRACT

BACKGROUND: Inteins and introns are genetic elements that are removed from proteins and RNA after translation or transcription, respectively. Previous studies have suggested that these genetic elements are found in conserved parts of the host protein. To our knowledge this type of analysis has not been done for group II introns residing within a gene. Here we provide quantitative statistical support from an analyses of proteins that host inteins, group I introns, group II introns and spliceosomal introns across all three domains of life. RESULTS: To determine whether or not inteins, group I, group II, and spliceosomal introns are found preferentially in conserved regions of their respective host protein, conservation profiles were generated and intein and intron positions were mapped to the profiles. Fisher's combined probability test was used to determine the significance of the distribution of insertion sites across the conservation profile for each protein. For a subset of studied proteins, the conservation profile and insertion positions were mapped to protein structures to determine if the insertion sites correlate to regions of functional activity. All inteins and most group I introns were found to be preferentially located within conserved regions; in contrast, a bacterial intein-like protein, group II and spliceosomal introns did not show a preference for conserved sites. CONCLUSIONS: These findings demonstrate that inteins and group I introns are found preferentially in conserved regions of their respective host proteins. Homing endonucleases are often located within inteins and group I introns and these may facilitate mobility to conserved regions. Insertion at these conserved positions decreases the chance of elimination, and slows deletion of the elements, since removal of the elements has to be precise as not to disrupt the function of the protein. Furthermore, functional constrains on the targeted site make it more difficult for hosts to evolve immunity to the homing endonuclease. Therefore, these elements will better survive and propagate as molecular parasites in conserved sites. In contrast, spliceosomal introns and group II introns do not show significant preference for conserved sites and appear to have adopted a different strategy to evade loss.


Subject(s)
Evolution, Molecular , Inteins , Introns , Protein Splicing , RNA Splice Sites , Conserved Sequence , RNA Splicing
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