Low-resolution sequencing of Rhodobacter sphaeroides 2.A.1T: chromosome II is a true chromosome

Choudhary, Madhu; MacKenzie, Cameron A.; Nereng, Kirsten S.; Sodergren, Erica; Weinstock, George M.; Kaplan, Samuel

doi:10.1099/00221287-143-10-3085

Cited by 36 publications

(21 citation statements)

References 55 publications

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“…Since early genetic work on Escherichia coli established the dogma of a single circular chromosome in prokaryotes, essentially all smaller replicons in cells have been relegated to the status of extrachromosomal elements or plasmids, irrespective of the species (Drlica and Riley 1990). Of the many plasmids that have been characterized, several are megaplasmids from a hundred kilobases to megabase sizes, including F (fertility) and R (resistance) factors, and toxin-bearing plasmids in E. coli and other pathogenic bacteria (Proter 1991), tumor-inducing plasmids and symbiotic plasmids in Agrobacterium and Rhizobium species (Van Larebeke et al 1974;Banfalvi et al 1985), and a variety of aromatic hydrocarbon degradation plasmids in Pseudomonas species and related bacteria (Franz and Chakrabarty 1986;Choudhary et al 1997;Mouncey et al 1997).…”

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confidence: 99%

Snapshot of a Large Dynamic Replicon in a Halophilic Archaeon: Megaplasmid or Minichromosome?

Ng¹,

Ciufo²,

Smith³

et al. 1998

Genome Res.

107

101

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Extremely halophilic archaea, which flourish in hypersaline environments, are known to contain a variety of large dynamic replicons. Previously, the analysis of one such replicon, pNRC100, in Halobacterium sp. strain NRC-1, showed that it undergoes high-frequency insertion sequence (IS) element-mediated insertions and deletions, as well as inversions via recombination between 39-kb-long inverted repeats (IRs). Now, the complete sequencing of pNRC100, a 191,346-bp circle, has shown the presence of 27 IS elements representing eight families. A total of 176 ORFs or likely genes of 850-bp average size were found, 39 of which were repeated within the large IRs. More than one-half of the ORFs are likely to represent novel genes that have no known homologs in the databases. Among ORFs with previously characterized homologs, three different copies of putative plasmid replication and four copies of partitioning genes were found, suggesting that pNRC100 evolved from IS element-mediated fusions of several smaller plasmids. Consistent with this idea, putative genes typically found on plasmids, including those encoding a restriction-modification system and arsenic resistance, as well as buoyant gas-filled vesicles and a two-component regulatory system, were found on pNRC100. However, additional putative genes not expected on an extrachromosomal element, such as those encoding an electron transport chain cytochrome d oxidase, DNA nucleotide synthesis enzymes thioredoxin and thioredoxin reductase, and eukaryotic-like TATA-binding protein transcription factors and a chromosomal replication initiator protein were also found. A multi-step IS element-mediated process is proposed to account for the acquisition of these chromosomal genes.

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mentioning

confidence: 99%

Snapshot of a Large Dynamic Replicon in a Halophilic Archaeon: Megaplasmid or Minichromosome?

Ng¹,

Ciufo²,

Smith³

et al. 1998

Genome Res.

107

101

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“…Studies from our laboratory revealed that R. sphaeroides 2.4.1 T possesses two different circular chromosomes, of ϳ3.0 Mbp (CI) and ϳ0.9 Mbp (CII) (42,43). A number of genes have been shown to be duplicated between CI and CII (5). In contrast, we have previously shown by Tn5 mutagenesis that some pathways, e.g., p-aminobenzoic acid, uracil, histidine, and thymine biosynthesis, are partitioned rather than duplicated between CI and CII (4).…”

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confidence: 99%

“…Recently, we used a low-redundancy sequencing strategy for analysis of the genetic content of CII (5). We analyzed ϳ300 kb of unique DNA which identified approximately 200 putative open reading frames (ORFs) representing a wide variety of functions, e.g., amino acid biosynthesis, nutrient transporters, redox-active systems, and a number of regulatory functions, indicating that CII does not contain genes specialized for any particular metabolic function, physiologic state, or growth condition.…”

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confidence: 99%

Characterization of genes encoding dimethyl sulfoxide reductase of Rhodobacter sphaeroides 2.4.1T: an essential metabolic gene function encoded on chromosome II

1997

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Rhodobacter sphaeroides is a gram-negative purple nonsulfur bacterium belonging to the alpha-3 subdivision of the Proteobacteria (49). This organism is capable of a wide range of metabolic lifestyles, exhibiting growth chemoautotrophically, photoautotrophically, photoheterotrophically, chemoheterotrophically, and diazotrophically (reviewed in reference 24). The ability of purple nonsulfur bacteria, as well as other bacterial species, to utilize dimethyl sulfoxide (DMSO) and trimethylamine N-oxide (TMAO) as terminal electron acceptors in the absence of oxygen for chemoheterotrophic growth has been well documented (12,23,52). Both DMSO and TMAO are commonly occurring compounds in nature and play roles in sulfur and nitrogen cycling (1).Under anoxic conditions in the presence of DMSO or TMAO and in the absence of light, R. sphaeroides can grow via a periplasmic DMSO reductase (DMSOR), which serves as the terminal electron acceptor in a cascade in which electrons are transferred from quinol to DMSO or TMAO (24). This process does not require the cytochrome bc 1 complex, and electrons are transferred from quinol to DMSOR via a membranebound b-type cytochrome and a periplasmic c-type cytochrome (25). DMSOR from both R. sphaeroides and the closely related bacterium R. capsulatus have been crystallized and shown to contain the molybdopterin cofactor (Moco) as the sole prosthetic group (for a review, see reference 21).Studies on the genetics of DMSO reduction in both R. sphaeroides and R. capsulatus have been limited mainly to several reports which describe the sequence of the gene encoding DMSOR (2, 22, 37, 51). The dmsA or dorA gene product has extensive homology to other molybdoenzymes such as biotin sulfoxide reductase and TMAO reductase (50). Recently, the sequences of two genes upstream of the dmsA gene of R. sphaeroides f. sp. denitrificans were reported (45). The dmsC and dmsB gene products were shown to be homologous to the torC and torD gene products, which encode a c-type cytochrome and a membrane protein, respectively, and it was suggested that the dmsCBA genes form a transcriptional unit, similar to the torCDA genes in E. coli (27). Studies from our laboratory revealed that R. sphaeroides 2.4.1 T possesses two different circular chromosomes, of ϳ3.0 Mbp (CI) and ϳ0.9 Mbp (CII) (42,43). A number of genes have been shown to be duplicated between CI and CII (5). In contrast, we have previously shown by Tn5 mutagenesis that some pathways, e.g., p-aminobenzoic acid, uracil, histidine, and thymine biosynthesis, are partitioned rather than duplicated between CI and CII (4). These results suggested that CII is an essential genomic element, having unique as well as shared and duplicated functions.Recently, we used a low-redundancy sequencing strategy for analysis of the genetic content of CII (5). We analyzed ϳ300 kb of unique DNA which identified approximately 200 putative open reading frames (ORFs) representing a wide variety of functions, e.g., amino acid biosynthesis, nutrient transporters, redox-active systems, ...

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“…CI and CII are 3,188,631 and 943,022 bp long, respectively, and contain approximately 3,106 and 874 open reading frames, respectively. Preliminary genome analyses (5,6,25,26) have revealed that a wide variety of essential and housekeeping genes are present on both CI and CII.…”

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confidence: 99%

DNA Sequence Duplication in Rhodobacter sphaeroides 2.4.1: Evidence of an Ancient Partnership between Chromosomes I and II

Choudhary

MacKenzie³

et al. 2004

J Bacteriol

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The complex genome of Rhodobacter sphaeroides 2.4.1, composed of chromosomes I (CI) and II (CII), has been sequenced and assembled. We present data demonstrating that the R. sphaeroides genome possesses an extensive amount of exact DNA sequence duplication, 111 kb or ϳ2.7% of the total chromosomal DNA. The chromosomal DNA sequence duplications were aligned to each other by using MUMmer. Frequency and size distribution analyses of the exact DNA duplications revealed that the interchromosomal duplications occurred prior to the intrachromosomal duplications. Most of the DNA sequence duplications in the R. sphaeroides genome occurred early in species history, whereas more recent sequence duplications are rarely found. To uncover the history of gene duplications in the R. sphaeroides genome, 44 gene duplications were sampled and then analyzed for DNA sequence similarity against orthologous DNA sequences. Phylogenetic analysis revealed that ϳ80% of the total gene duplications examined displayed type A phylogenetic relationships; i.e., one copy of each member of a duplicate pair was more similar to its orthologue, found in a species closely related to R. sphaeroides, than to its duplicate, counterpart allele. The data reported here demonstrate that a massive level of gene duplications occurred prior to the origin of the R. sphaeroides 2.4.1 lineage. These findings lead to the conclusion that there is an ancient partnership between CI and CII of R. sphaeroides 2.4.1.Rhodobacter sphaeroides 2.4.1, a purple nonsulfur photosynthetic eubacterium, belongs to the ␣-3 subgroup of the Proteobacteria (40,41). This species, along with other members of the class Proteobacteria, represents one of the largest divisions within the prokaryotes (41) and comprises a large number of gram-negative bacteria. R. sphaeroides is also one of the most metabolically versatile and diverse subgroups of the ␣-3 subgroup of the Proteobacteria, which includes Rhizobium, Agrobacterium, Caulobacter, Brucella, and Rickettsia (40,41). A few examples of the metabolic diversity are the diversity in assembly and regulation of the light-harvesting apparatus, in nitrogen fixation, in carbon dioxide fixation, in hydrogen metabolism, in electron transport, in oxyanion reduction, and in tetrapyrrole biosynthesis (9,19).R. sphaeroides 2.4.1 contains one of the most complex genomes found in members of the Proteobacteria (4,18,21). This species was the first bacterial species shown to possess a complex genome consisting of two circular chromosomes, one ϳ3.0 Mbp long (chromosome I [CI]) and one ϳ0.9 Mbp long (chromosome II [CII]), and five additional endogenous replicons (36, 37). The existence of multiple chromosomes in bacteria is now no longer an exception and has been instrumental in setting aside the long-held dogma that all bacterial species have a single circular chromosome.Currently there is an extensive list of prokaryotic genomes that have been sequenced, including that of R. sphaeroides 2.4.1. As a result, R. sphaeroides is an ideal system for the study o...

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Low-resolution sequencing of Rhodobacter sphaeroides 2.A.1T: chromosome II is a true chromosome

Cited by 36 publications

References 55 publications

Snapshot of a Large Dynamic Replicon in a Halophilic Archaeon: Megaplasmid or Minichromosome?

Snapshot of a Large Dynamic Replicon in a Halophilic Archaeon: Megaplasmid or Minichromosome?

Characterization of genes encoding dimethyl sulfoxide reductase of Rhodobacter sphaeroides 2.4.1T: an essential metabolic gene function encoded on chromosome II

DNA Sequence Duplication in Rhodobacter sphaeroides 2.4.1: Evidence of an Ancient Partnership between Chromosomes I and II

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