Intron Conservation in a UV-Specific DNA Repair Gene Encoded by Chlorella Viruses

Sun, Lizhong; Liu, Yu; McCullough, Amanda K.; Wood, Thomas G.; Lloyd, R. Stephen; Adams, Byron J.; Gurnon, James R.; Etten, James L. Van

doi:10.1007/s002399910009

Cited by 18 publications

(24 citation statements)

References 49 publications

(45 reference statements)

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“…To determine whether the cvSOD gene is common in the chloroviruses, viral genomic DNAs were prepared from 44 different chloroviruses that infect C. variabilis. The chloroviruses were isolated from diverse geographical locations worldwide (49) and hybridized with the 32 P-labeled PBCV-1 tcvsod gene probe. The probe hybridized strongly to 37 of the 44 viruses (see Fig.…”

Section: Resultsmentioning

confidence: 99%

Chlorovirus PBCV-1 Encodes an Active Copper-Zinc Superoxide Dismutase

Kang

Duncan

Kuszynski

et al. 2014

J Virol

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Superoxide dismutases (SODs) are metalloproteins that protect organisms from toxic reactive oxygen species by catalyzing the conversion of superoxide anion to hydrogen peroxide and molecular oxygen. Chlorovirus PBCV-1 encodes a 187-amino-acid protein that resembles a Cu-Zn SOD with all of the conserved amino acid residues for binding copper and zinc (named cvSOD). cvSOD has an internal Met that results in a 165-amino-acid protein (named tcvSOD). Both cvSOD and tcvSOD recombinant proteins inhibited nitroblue tetrazolium reduction of superoxide anion generated in a xanthine-xanthine oxidase system in solution. tcvSOD was chosen for further characterization because it was easier to produce. Recombinant tcvSOD also inhibited a riboflavin photochemical reduction system in a polyacrylamide gel assay, which was blocked by the Cu-Zn SOD inhibitor cyanide but not by azide, which inhibits Fe and Mn SODs. A k cat /K m value for cvSOD was determined by stop-flow spectrophotometry as 1.28 ؋ 10 8 M ؊1 s ؊1 , suggesting that cvSOD-catalyzed O 2 ؊ dismutation was not a diffusion controlled encounter. The cvsod gene was expressed as a late gene, and cvSOD activity was detected in purified virions. Superoxide accumulated rapidly during virus infection, and circumstantial evidence indicates that cvSOD aids its decomposition to benefit virus replication. Cu-Zn SOD homologs have been described to occur in 3 other families of large DNA viruses, poxviruses, baculoviruses, and mimiviruses, which group as a clade. Interestingly, cvSOD does not group in the same clade as the other virus SODs but instead groups in an expanded clade that includes Cu-Zn SODs from many cellular organisms. IMPORTANCEVirus infection often leads to an increase in toxic reactive oxygen species in the host, which can be detrimental to virus replication. Viruses have developed various ways to overcome this barrier. As reported in this article, the chloroviruses often encode and package a functional Cu-Zn superoxide dismutase in the virion that presumably lowers the concentration of reactive oxygen induced early during virus infection.

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Section: Resultsmentioning

confidence: 99%

Chlorovirus PBCV-1 Encodes an Active Copper-Zinc Superoxide Dismutase

Kang

Duncan

Kuszynski

et al. 2014

J Virol

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“…However, the abilities of intron-containing and intron-lacking viruses to repair UV-damaged DNA in the dark were indistinguishable (189). These findings contradict the dogma that intron sequences are more variable than exon sequences (103).…”

Section: Diversity Of Chlorella Virus Genomesmentioning

confidence: 85%

“…Some of the tRNA genes contain introns as large as 1 kb (145). (d) Sequence analyses of a gene (pdg) encoding a UV-specific DNA repair enzyme from 42 NC64A viruses revealed that 15 contain a 98-nucleotide, spliceosomal-processed intron that is 100% conserved; four other viruses contain an identically positioned 81-nucleotide intron that is nearly 100% identical (189). In contrast, the nucleotides in the pdg coding regions (exons) from the intron-containing viruses are 84% to 100% identical.…”

Section: Diversity Of Chlorella Virus Genomesmentioning

confidence: 99%

Unusual Life Style of Giant Chlorella Viruses

2003

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Paramecium bursaria chlorella virus (PBCV-1) is the prototype of a family of large, icosahedral, plaque-forming, dsDNA viruses that replicate in certain unicellular, eukaryotic chlorella-like green algae. Its 330-kb genome contains ~373 protein-encoding genes and 11 tRNA genes. The predicted gene products of ~50% of these genes resemble proteins of known function, including many that are unexpected for a virus, e.g., ornithine decarboxylase, hyaluronan synthase, GDP-D-mannose 4,6 dehydratase, and a potassium ion channel protein. In addition to their large genome size, the chlorella viruses have other features that distinguish them from most viruses. These features include: (a) The viruses encode multiple DNA methyltransferases and DNA site-specific endonucleases. (b) The viruses encode at least some, if not all, of the enzymes required to glycosylate their proteins. (c) PBCV-1 has at least three types of introns, a self-splicing intron in a transcription factorlike gene, a spliceosomal processed intron in its DNA polymerase gene, and a small intron in one of its tRNA genes. (d) Many chlorella virus-encoded proteins are either the smallest or among the smallest proteins of their class. (e) Accumulating evidence indicates that the chlorella viruses have a very long evolutionary history.

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“…These include spliceosomally processed (17,44,61), tRNA (31), and self-splicing group I (25,32,60) introns. This last type of introns are related to inteins: both remove themselves from the precursor product (group I introns do so at the RNA level and inteins do so at the protein level), both are inserted in conserved motifs of essential genes, both frequently include an EN domain that mediates their homing, and both are considered mobile selfish genetic elements (11).…”

Section: Resultsmentioning

confidence: 99%

Algal Viruses with Distinct Intraspecies Host Specificities Include Identical Intein Elements

Nagasaki

Shirai

Tomaru

et al. 2005

Appl Environ Microbiol

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Heterosigma akashiwo virus (HaV) is a large double-stranded DNA virus infecting the single-cell bloomforming raphidophyte (golden brown alga) H. akashiwo. A molecular phylogenetic sequence analysis of HaV DNA polymerase showed that it forms a sister group with Phycodnaviridae algal viruses. All 10 examined HaV strains, which had distinct intraspecies host specificities, included an intein (protein intron) in their DNA polymerase genes. The 232-amino-acid inteins differed from each other by no more than a single nucleotide change. All inteins were present at the same conserved position, coding for an active-site motif, which also includes inteins in mimivirus (a very large double-stranded DNA virus of amoebae) and in several archaeal DNA polymerase genes. The HaV intein is closely related to the mimivirus intein, and both are apparently monophyletic to the archaeal inteins. These observations suggest the occurrence of horizontal transfers of inteins between viruses of different families and between archaea and viruses and reveal that viruses might be reservoirs and intermediates in horizontal transmissions of inteins. The homing endonuclease domain of the HaV intein alleles is mostly deleted. The mechanism keeping their sequences basically identical in HaV strains specific for different hosts is yet unknown. One possibility is that rapid and local changes in the HaV genome change its host specificity. This is the first report of inteins found in viruses infecting eukaryotic algae.

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Intron Conservation in a UV-Specific DNA Repair Gene Encoded by Chlorella Viruses

Cited by 18 publications

References 49 publications

Chlorovirus PBCV-1 Encodes an Active Copper-Zinc Superoxide Dismutase

Chlorovirus PBCV-1 Encodes an Active Copper-Zinc Superoxide Dismutase

Unusual Life Style of Giant Chlorella Viruses

Algal Viruses with Distinct Intraspecies Host Specificities Include Identical Intein Elements

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