Gene capture in archaeal chromosomes.
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Chromosomes, Archaeal↗
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An archaeal chromosomal autonomously replicating sequence element from an extreme halophile, Halobacterium sp. strain NRC-1.
We report on the identification and first cloning of an autonomously replicating sequence element from the chromosome of an archaeon, the extreme halophile Halobacterium strain NRC-1. The putative replication origin was identified by association with the orc7 gene and replication ability in the host strain, demonstrated by cloning into a nonreplicating plasmid. Deletion analysis showed that sequences located up to 750 bp upstream of the orc7 gene translational start, plus the orc7 gene and 50 bp downstream, are sufficient to endow the plasmid with replication ability, as judged by expression of a plasmid-encoded mevinolin resistance selectable marker and plasmid recovery after transformation. Sequences located proximal to the two other chromosomally carried haloarchaeal orc genes (orc6 and orc8) are not able to promote efficient autonomous replication. Located within the 750-bp region upstream of orc7 is a nearly perfect inverted repeat of 31 bp, which flanks an extremely AT-rich (44%) stretch of 189 bp. The replication ability of the plasmid was lost when one copy of the inverted repeat was deleted. Additionally, the inverted repeat structure near orc7 homologs in the genomic sequences of two other halophiles, Haloarcula marismortui and Haloferax volcanii, is highly conserved. Our results indicate that, in halophilic archaea, a chromosomal origin of replication is physically linked to orc7 homologs and that this element is sufficient to promote autonomous replication. We discuss the finding of a functional haloarchaeal origin in relation to the large number of orc1-cdc6 homologs identified in the genomes of all haloarchaea to date.
Base Sequence↗
Atypical recognition of particular DNA sequences by the archaeal chromosomal MC1 protein.
The MC1 protein is a chromosomal protein likely involved in the DNA compaction of some methanogenic archaea. This small and monomeric protein, structurally unrelated to other DNA binding proteins, bends DNA sharply. By studying the protein binding to various kinds of kinked DNA, we have previously shown that MC1 is able to discriminate between different deformations of the DNA helix. Here we investigate its capacity to recognize particular DNA sequences by using a SELEX procedure. We find that MC1 is able to preferentially bind to a 15 base pair motif [AAAAACACAC(A/C)CCCC]. The structural parameters of this sequence are characterized by molecular dynamics simulation experiments, and the binding mode of the protein to the DNA is studied by footprinting experiments. Our results strongly suggest that the protein realizes an indirect readout of the DNA sequence by binding to the DNA minor groove.
Archaeal Proteins↗
Archaeal integrases and mechanisms of gene capture.
Archaeal integrases facilitate the formation of two distinctive types of integrated element within archaeal chromosomes: the SSV type and pNOB8 type. The former carries a smaller N-terminal and a larger C-terminal integrase gene fragment, and the latter an intact integrase gene. All integrated elements overlap tRNA genes that were target sites for integration. It has been demonstrated that SSV (Sulfolobus spindle virus) viruses, carrying an SSV-type integrase gene, and conjugative plasmids, carrying a pNOB8-type integrase, are integrative elements. Two mechanisms have been proposed for stably maintaining an integrated element within archaeal chromosomes. There is also evidence for changes having occurred in the captured integrated elements present in archaeal genomes. Thus we infer that site-specific integration constitutes an important mechanism for horizontal gene transfer and genome evolution.
Archaea↗
Genus-specific protein binding to the large clusters of DNA repeats (short regularly spaced repeats) present in Sulfolobus genomes.
Short regularly spaced repeats (SRSRs) occur in multiple large clusters in archaeal chromosomes and as smaller clusters in some archaeal conjugative plasmids and bacterial chromosomes. The sequence, size, and spacing of the repeats are generally constant within a cluster but vary between clusters. For the crenarchaeon Sulfolobus solfataricus P2, the repeats in the genome fall mainly into two closely related sequence families that are arranged in seven clusters containing a total of 441 repeats which constitute ca. 1% of the genome. The Sulfolobus conjugative plasmid pNOB8 contains a small cluster of six repeats that are identical in sequence to one of the repeat variants in the S. solfataricus chromosome. Repeats from the pNOB8 cluster were amplified and tested for protein binding with cell extracts from S. solfataricus. A 17.5-kDa SRSR-binding protein was purified from the cell extracts and sequenced. The protein is N terminally modified and corresponds to SSO454, an open reading frame of previously unassigned function. It binds specifically to DNA fragments carrying double and single repeat sequences, binding on one side of the repeat structure, and producing an opening of the opposite side of the DNA structure. It also recognizes both main families of repeat sequences in S. solfataricus. The recombinant protein, expressed in Escherichia coli, showed the same binding properties to the SRSR repeat as the native one. The SSO454 protein exhibits a tripartite internal repeat structure which yields a good sequence match with a helix-turn-helix DNA-binding motif. Although this putative motif is shared by other archaeal proteins, orthologs of SSO454 were only detected in species within the Sulfolobus genus and in the closely related Acidianus genus. We infer that the genus-specific protein induces an opening of the structure at the center of each DNA repeat and thereby produces a binding site for another protein, possibly a more conserved one, in a process that may be essential for higher-order stucturing of the SRSR clusters.
Amino Acid Sequence↗
Archaeal integrative genetic elements and their impact on genome evolution.
Integrases encoded in archaeal genomes can be classified into seven families on the basis of their sequences. They constitute a super-family of tyrosine DNA recombinases together with a number of bacterial integrases and they are likely to be responsible for the formation of integrated elements in archaeal chromosomes. An integrated element is defined as possessing an integrase, a block of foreign genes, and a direct repeat at the two ends with one repeat unit overlapping a tRNA gene. There are two types of archaeal integrated elements, the SSV viral type, including those that carry the partitioned integrase gene, intN and intC, and the pNOB8 type, including those with a tRNA gene overlapping the attL site 5' prior to an integrase gene. Both known and unknown genes are present in these integrated elements and their encoded proteins may have facilitated the adaptation of archaea during evolution.
Chromosomes, Archaeal↗
Archaea and the cell cycle.
Sequence similarity data suggest that archaeal chromosome replication is eukaryotic in character. Putative nucleoid-processing proteins display similarities to both eukaryotic and bacterial counterparts, whereas cell division may occur through a predominantly bacterial mechanism. Insights into the organization of the archaeal cell cycle are therefore of interest, not only for understanding archaeal biology, but also for investigating how components from the other two domains interact and work in concert within the same cell; in addition, archaea may have the potential to provide insights into eukaryotic initiation of chromosome replication.
Archaea↗
Chromosome packaging by archaeal histones.
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Amino Acid Sequence↗
Quantifying intrachromosomal GC heterogeneity in prokaryotic genomes.
The sequencing of prokaryotic genomes covering a wide taxonomic range has sparked renewed interest in intrachromosomal compositional (GC) heterogeneity, largely in view of lateral transfers. We present here a brief overview of some methods for visualizing and quantifying GC variation in prokaryotes. We used these methods to examine heterogeneity levels in sequenced prokaryotes, for a range of scales or stringencies. Some species are consistently homogeneous, whereas others are markedly heterogeneous in comparison, in particular Aeropyrum pernix, Xylella fastidiosa, Mycoplasma genitalium, Enterococcus faecalis, Bacillus subtilis, Pyrobaculum aerophilum, Vibrio vulnificus chromosome I, Deinococcus radiodurans chromosome II and Halobacterium. As we discuss here, the wide range of heterogeneities calls for reexamination of an accepted belief, namely that the endogenous DNA of bacteria and archaea should typically exhibit low intrachromosomal GC contrasts. Supplementary results for all species analyzed are available at our website: http://bioinfo2.ugr.es/prok.
Algorithms↗
Genome update: alignment of bacterial chromosomes.
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Bacillus anthracis↗
Evolutionary implications of microbial genome tetranucleotide frequency biases.
We compared nucleotide usage pattern conservation for related prokaryotes by examining the representation of DNA tetranucleotide combinations in 27 representative microbial genomes. For each of the organisms studied, tetranucleotide usage departures from expectations (TUD) were shared between related organisms using both Markov chain analysis and a zero-order Markov method. Individual strains, multiple chromosomes, plasmids, and bacteriophages share TUDs within a species. TUDs varied between coding and noncoding DNA. Grouping prokaryotes based on TUD profiles resulted in relationships with important differences from those based on 16S rRNA phylogenies, which may reflect unequal rates of evolution of nucleotide usage patterns following divergence of particular organisms from a common ancestor. By both symmetrical tree distance and likelihood analysis, phylogenetic trees based on TUD profiles demonstrate a level of congruence with 16S rRNA trees similar to that of both RpoA and RecA trees. Congruence of these trees indicates that there exists phylogenetic signal in TUD patterns, most prominent in coding region DNA. Because relationships demonstrated in TUD-based analyses utilize whole genomes, they should be considered complementary to phylogenies based on single genetic elements, such as 16S rRNA.
Chromosome Mapping↗
Viral eukaryogenesis: was the ancestor of the nucleus a complex DNA virus?
In the theory of viral eukaryogenesis I propose here, the eukaryotic nucleus evolved from a complex DNA virus. It is proposed that the virus established a persistent presence in the cytoplasm of a methanogenic mycoplasma and evolved into the eukaryotic nucleus by acquiring a set of essential genes from the host genome and eventually usurping its role. It is proposed that several characteristic features of the eukaryotic nucleus derive from its viral ancestry. These include mRNA capping, linear chromosomes, and separation of transcription from translation. In the model, phagocytosis and other membrane fusion-based processes are derived from viral membrane fusion processes and evolved in concert with the nucleus. The coevolution of phagocytosis and the nucleus rendered much of the host archaeal genome redundant since the protoeukaryote could obtain raw materials and energy by engulfing bacterial syntrophs/prey. This redundancy allowed loss of the archaeal chromosome, generating an organism with eukaryotic features. The evolution of phagocytosis allowed the eukaryotes to be the first organisms to occupy the niche of predator.
Amino Acid Sequence↗
Methods for comparing sources of strand compositional asymmetry in microbial chromosomes.
Significant compositional biases in bacterial chromosomes have been explained by replication- and transcription-coupled repair mechanisms, the latter causing GC skew to indicate the direction of replication when gene polarity is correspondingly entrained. Correlations between indicators of replication direction, skew, and transcription polarity are computed for the complete nucleotide sequences of 20 microbial chromosomes and interpreted through statistical tests. A second quantitative method, previously applied to the first complete draft of the Escherichia coli K12 genome, characterizes the sequences by average skew and net skew due to replication. These methods generally agree in finding the coexistence of replication- and translation-coupled effects and in identifying atypical sequences in which one influence is clearly dominant. The replication-dominated class is exemplified by two chlamydial sequences and the transcription-dominated class by three archaea. The preference for leading-strand transcription in two mycoplasmas is stronger than the skew implies. These concordant methods provide an objective framework for comparing sources of strand compositional asymmetry and interpreting skew diagrams.
Base Composition↗
GISMO--gene identification using a support vector machine for ORF classification.
We present the novel prokaryotic gene finder GISMO, which combines searches for protein family domains with composition-based classification based on a support vector machine. GISMO is highly accurate; exhibiting high sensitivity and specificity in gene identification. We found that it performs well for complete prokaryotic chromosomes, irrespective of their GC content, and also for plasmids as short as 10 kb, short genes and for genes with atypical sequence composition. Using GISMO, we found several thousand new predictions for the published genomes that are supported by extrinsic evidence, which strongly suggest that these are very likely biologically active genes. The source code for GISMO is freely available under the GPL license.
Algorithms↗
Genometric analyses of the organization of circular chromosomes: a universal pressure determines the direction of ribosomal RNA genes transcription relative to chromosome replication.
Selective pressures related to gene function and chromosomal architecture are acting on genome sequences and can be revealed, for instance, by appropriate genometric methods. Cumulative nucleotide skew analyses, i.e., GC, TA, and ORF orientation skews, predict the location of the origin of DNA replication for 88 out of 100 completely sequenced bacterial chromosomes. These methods appear fully reliable for proteobacteria, Gram-positives, and spirochetes as well as for euryarchaeotes. Based on this genome architecture information, coorientation analyses reveal that in prokaryotes, ribosomal RNA (rRNA) genes encoding the small and large ribosomal subunits are all transcribed in the same direction as DNA replication; that is, they are located along the leading strand. This result offers a simple and reliable method for circumscribing the region containing the origin of the DNA replication and reveals a strong selective pressure acting on the orientation of rRNA genes similar to the weaker one acting on the orientation of ORFs. Rate of coorientation of transfer RNA (tRNA) genes with DNA replication appears to be taxon-specific. Analyzing nucleotide biases such as GC and TA skews of genes and plotting one against the other reveals a taxonomic clusterization of species. All ribosomal RNA genes are enriched in Gs and depleted in Cs, the only so far known exception being the rRNA genes of deuterostomian mitochondria. However, this exception can be explained by the fact that in the chromosome of the human mitochondrion, the model of the deuterostomian organelle genome, DNA replication, and rRNA transcription proceed in opposite directions. A general rule is deduced from prokaryotic and mitochondrial genomes: ribosomal RNA genes that are transcribed in the same direction as the DNA replication are enriched in Gs, and those transcribed in the opposite direction are depleted in Gs.
Base Composition↗
A putative viral defence mechanism in archaeal cells.
Clusters of regularly spaced direct repeats, separated by unconserved spacer sequences, are ubiquitous in archaeal chromosomes and occur in some plasmids. Some clusters constitute around 1% of chromosomal DNA. Similarly structured clusters, generally smaller, also occur in some bacterial chromosomes. Although early studies implicated these clusters in segregation/partition functions, recent evidence suggests that the spacer sequences derive from extrachromosomal elements, and, primarily, viruses. This has led to the proposal that the clusters provide a defence against viral propagation in cells, and that both the mode of inhibition of viral propagation and the mechanism of adding spacer-repeat units to clusters, are dependent on RNAs transcribed from the clusters. Moreover, the putative inhibitory apparatus (piRNA-based) may be evolutionarily related to the interference RNA systems (siRNA and miRNA), which are common in eukarya. Here, we analyze all the current data on archaeal repeat clusters and provide some new insights into their diverse structures, transcriptional properties and mode of structural development. The results are consistent with larger cluster transcripts being processed at the centers of the repeat sequences and being further trimmed by exonucleases to yield a dominant, intracellular RNA species, which corresponds approximately to the size of a spacer. Furthermore, analysis of the extensive clusters of Sulfolobus solfataricus strains P1 and P2B provides support for the presence of a flanking sequence adjoining a cluster being a prerequisite for the incorporation of new spacer-repeat units, which occurs between the flanking sequence and the cluster. An archaeal database summarizing the data will be maintained at http://dac.molbio.ku.dk/dbs/SRSR/.
Archaea↗
Three-base periodicity patterns and self-similarity in whole bacterial chromosomes.
It has been reported that in a collection of mRNAs the triplets GhN or RNY had a higher propensity to be separated by either three/six/nine, etc., bases than by two/four/five, etc., bases. This has been called three-base periodicity (TBP). In this work the frequency distribution of distances (FDDs) for all triplets in the Borrelia burgdorferi chromosome and selected triplets in other model sequences were determined. The FDDs produced oscillatory decaying patterns with TBP for most triplets and not only for those encompassed by the above formulas. Furthermore, we also found TBP for di- and mononucleotides. However, TBP was not observed for intergenic regions, sequences with a low content of coding regions or when the coding potential of sequences was disrupted by base shuffling. Excluding closely related species the FDDs between bacterial genomes were different and appeared characteristic of the analyzed genome. FDDs also showed self-similarity, since 1Mb sequences rendered FDDs that were very similar to those for the entire sequence.
Base Composition↗
Bias of purine stretches in sequenced chromosomes.
We examined more than 700 DNA sequences (full length chromosomes and plasmids) for stretches of purines (R) or pyrimidines (Y) and alternating YR stretches; such regions will likely adopt structures which are different from the canonical B-form. Since one turn of the DNA helix is roughly 10 bp, we measured the fraction of each genome which contains purine (or pyrimidine) tracts of lengths of 10 bp or longer (hereafter referred to as 'purine tracts'), as well as stretches of alternating pyrimidines/purine (pyr/pur tracts') of the same length. Using this criteria, a random sequence would be expected to contain 1.0% of purine tracts and also 1.0% of the alternating pyr/pur tracts. In the vast majority of cases, there are more purine tracts than would be expected from a random sequence, with an average of 3.5%, significantly larger than the expectation value. The fraction of the chromosomes containing pyr/pur tracts was slightly less than expected, with an average of 0.8%. One of the most surprising findings is a clear difference in the length distributions of the regions studied between prokaryotes and eukaryotes. Whereas short-range correlations can explain the length distributions in prokaryotes, in eukaryotes there is an abundance of long stretches of purines or alternating purine/pyrimidine tracts, which cannot be explained in this way; these sequences are likely to play an important role in eukaryotic chromosome organisation.
Animals↗