Extrachromosomal element capture and the evolution of multiple replication origins in archaeal chromosomes

Robinson, Nicholas P.; Bell, Stephen D.

doi:10.1073/pnas.0700206104

Cited by 102 publications

(112 citation statements)

References 29 publications

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“…The in vivo replication rates of S. solfataricus and S. acidocaldarius, both of which contain three replica- . The origin recognition boxes associated with the origins in these species (26,27) are also conserved in the S. tokodaii genome sequence (15), and it is therefore likely that this species also harbors three origins, resulting in a replication rate of around 70 bp/s. A. pernix has been shown to contain two origins (26), yielding an in vivo replication rate of 110 bp/s.…”

Section: Discussionmentioning

confidence: 99%

“…The origin recognition boxes associated with the origins in these species (26,27) are also conserved in the S. tokodaii genome sequence (15), and it is therefore likely that this species also harbors three origins, resulting in a replication rate of around 70 bp/s. A. pernix has been shown to contain two origins (26), yielding an in vivo replication rate of 110 bp/s. We have shown that flow cytometry is a convenient tool for genome size determination (4,21), even for the eukaryote Giardia lamblia.…”

Section: Discussionmentioning

confidence: 99%

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Cell Cycle Characteristics of Crenarchaeota : Unity among Diversity

et al. 2008

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The hyperthermophilic archaea Acidianus hospitalis, Aeropyrum pernix, Pyrobaculum aerophilum, Pyrobaculum calidifontis, and Sulfolobus tokodaii representing three different orders in the phylum Crenarchaeota were analyzed by flow cytometry and combined phase-contrast and epifluorescence microscopy. The overall organization of the cell cycle was found to be similar in all species, with a short prereplicative period and a dominant postreplicative period that accounted for 64 to 77% of the generation time. Thus, in all Crenarchaeota analyzed to date, cell division and initiation of chromosome replication occur in close succession, and a long time interval separates termination of replication from cell division. In Pyrobaculum, chromosome segregation overlapped with or closely followed DNA replication, and further genome separation appeared to occur concomitant with cellular growth. Cell division in P. aerophilum took place without visible constriction.All extant cellular organisms can be divided into three main evolutionary lineages, the domains Archaea, Bacteria, and Eukarya (32). The domain Archaea is further subdivided into two main phyla, Crenarchaeota and Euryarchaeota. Additional phyla have also been proposed (2,8,14), although their phylogenetic validities are under discussion (7,25).The cell cycle of organisms belonging to the domain Bacteria is organized into three main stages: the prereplication (B), replication (C), and postreplication (D) periods. In eukaryotes a different nomenclature is used, and the cell cycle is divided into the G 1 (gap 1), S (DNA synthesis), G 2 (gap 2), and M (mitosis) stages. The organization and relative lengths of the cell cycle periods vary greatly between organisms in both domains.The first cell cycle analyses of archaea were performed with organisms belonging to the crenarchaeal genus Sulfolobus. The cell cycle in these organisms is characterized by a short prereplication period and an extensive postreplication stage dominated by a long G 2 period (3a, 5, 12, 24). The organization of the cell cycle in the Euryarchaeota Methanocaldococcus jannaschii and Methanothermobacter thermautotrophicus differs considerably from that in Sulfolobus species. In M. jannaschii, cells with high and uneven numbers of genome copies are present, and asymmetric genome segregation and cell division are observed (22). M. thermautotrophicus grows as filaments consisting of multiple cells, each containing a minimum of two genomes (21). After replication, the two newly formed chromosome pairs rapidly segregate into separate nucleoids without any discernible G 2 stage, resulting in four spatially distinct chromosomes. In contrast to these methanogenic species, the sulfate-reducing euryarchaeon Archaeoglobus fulgidus has a cell cycle organization similar to that of Sulfolobus (20).In stationary-phase Sulfolobus cultures all cells contain two genome copies (5), resulting in an increase in the average cellular DNA content relative to an exponentially growing culture (3a). In contrast, a dramatic reductio...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Cell Cycle Characteristics of Crenarchaeota : Unity among Diversity

et al. 2008

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“…In addition, two-dimensional gel analysis of replicating molecules confirmed the location of the DNA replication origin near the orc1 gene of P. abyssi, with predicted origin binding sequences and AT-rich DNA unwinding elements nearby (18). An investigation of DNA replication in Aeropyrum pernix used a combination of biochemical and two-dimensional gel electrophoresis and identified two potential sites of replication initiation, on opposite sides of the circular genome (14,28). One of these sites (oriC1 Ap ) contained four origin recognition boxes and an AT-rich region and was shown to be bound by the ORC1 gene.…”

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confidence: 99%

“…One of these sites (oriC1 Ap ) contained four origin recognition boxes and an AT-rich region and was shown to be bound by the ORC1 gene. The other site (oriC2 Ap ) contained repeat elements without an intervening AT-rich region and has been shown by two-dimensional gel electrophoresis to contain an active replication origin (28). An examination of replication in two Sulfolobus spp., Sulfolobus solfataricus and Sulfolobus acidocaldarius (16,30), by use of a combination of bioinformatic and two-dimensional gel analysis and of marker frequency by use of DNA microarrays identified three well-separated replication origins per genome.…”

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confidence: 99%

Multiple Replication Origins ofHalobacteriumsp. Strain NRC-1: Properties of the Conservedorc7-DependentoriC1

et al. 2009

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The eukaryote-like DNA replication system of the model haloarchaeon Halobacterium NRC-1 is encoded within a circular chromosome and two large megaplasmids or minichromosomes, pNRC100 and pNRC200. We previously showed by genetic analysis that 2 (orc2 and orc10) of the 10 genes coding for Orc-Cdc6 replication initiator proteins were essential, while a third (orc7), located near a highly conserved autonomously replicating sequence, oriC1, was nonessential for cell viability. Here we used whole-genome marker frequency analysis (MFA) and found multiple peaks, indicative of multiple replication origins. The largest chromosomal peaks were located proximal to orc7 (oriC1) and orc10 (oriC2), and the largest peaks on the extrachromosomal elements were near orc9 (oriP1) in both pNRC100 and -200 and near orc4 (oriP2) in pNRC200. MFA of deletion strains containing different combinations of chromosomal orc genes showed that replication initiation at oriC1 requires orc7 but not orc6 and orc8. The initiation sites at oriC1 were determined by replication initiation point analysis and found to map divergently within and near an AT-rich element flanked by likely Orc binding sites. The oriC1 region, Orc binding sites, and orc7 gene orthologs were conserved in all sequenced haloarchaea. Serial deletion of orc genes resulted in the construction of a minimal strain containing not only orc2 and orc10 but also orc9. Our results suggest that replication in this model system is intriguing and more complex than previously thought. We discuss these results from the perspective of the replication strategy and evolution of haloarchaeal genomes.Archaea are of considerable interest due to their unusual phylogenetic position and the similarity of their information transfer system to that of eukaryotes. In particular, studies of DNA replication in archaea have revealed characteristics of both bacterial and eukaryotic systems (1). While genome sequencing has shown that archaeal and bacterial genomes are composed of a single or few circular chromosomes, comparative genomic studies have found that most components of the archaeal DNA replication machinery, such as the origin recognition proteins, DNA polymerases, helicases, and primases, are similar to eukaryotic proteins. The hybrid nature of archaeal DNA replication systems raises important questions regarding the mechanism by which they select an origin(s) for initiation and coordinate orderly DNA replication and segregation into daughter cells.

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“…Additionally, they are not easily manipulated. Typically, crenarchaeotes, like Sulfolobus, Aeropyrum, and Pyrobaculum species have multiple origins (24,(35)(36)(37). Euryarchaeota, however, have either one origin, like Pyrococcus and Archaeoglobus species (38,39), or multiple origins, like Methanocaldococcus (39), Halobacterium (5,40), and Haloferax (41) species.…”

Section: Discussionmentioning

confidence: 99%

Characterization of the Replication Initiator Orc1/Cdc6 from the Archaeon Picrophilus torridus

Arora

Goswami

Saha

2013

Journal of Bacteriology

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Eukaryotic DNA replication is preceded by the assembly of prereplication complexes (pre-RCs) at or very near origins in G 1 phase, which licenses origin firing in S phase. The archaeal DNA replication machinery broadly resembles the eukaryal apparatus, though simpler in form. The eukaryotic replication initiator origin recognition complex (ORC), which serially recruits Cdc6 and other pre-RC proteins, comprises six components, Orc1-6. In archaea, a single gene encodes a protein similar to both the eukaryotic Cdc6 and the Orc1 subunit of the eukaryotic ORC, with most archaea possessing one to three Orc1/Cdc6 orthologs. Genome sequence analysis of the extreme acidophile Picrophilus torridus revealed a single Orc1/Cdc6 (PtOrc1/Cdc6). Biochemical analyses show MBP-tagged PtOrc1/Cdc6 to preferentially bind ORB (origin recognition box) sequences. The protein hydrolyzes ATP in a DNA-independent manner, though DNA inhibits MBP-PtOrc1/Cdc6-mediated ATP hydrolysis. PtOrc1/Cdc6 exists in stable complex with PCNA in Picrophilus extracts, and MBP-PtOrc1/Cdc6 interacts directly with PCNA through a PIP box near its C terminus. Furthermore, PCNA stimulates MBP-PtOrc1/Cdc6-mediated ATP hydrolysis in a DNA-dependent manner. This is the first study reporting a direct interaction between Orc1/Cdc6 and PCNA in archaea. The bacterial initiator DnaA is converted from an active to an inactive form by ATP hydrolysis, a process greatly facilitated by the bacterial ortholog of PCNA, the ␤ subunit of Pol III. The stimulation of PtOrc1/Cdc6-mediated ATP hydrolysis by PCNA and the conservation of PCNAinteracting protein motifs in several archaeal PCNAs suggest the possibility of a similar mechanism of regulation existing in archaea. This mechanism may involve other yet to be identified archaeal proteins.

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Extrachromosomal element capture and the evolution of multiple replication origins in archaeal chromosomes

Cited by 102 publications

References 29 publications

Cell Cycle Characteristics of Crenarchaeota : Unity among Diversity

Cell Cycle Characteristics of Crenarchaeota : Unity among Diversity

Multiple Replication Origins ofHalobacteriumsp. Strain NRC-1: Properties of the Conservedorc7-DependentoriC1

Characterization of the Replication Initiator Orc1/Cdc6 from the Archaeon Picrophilus torridus

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