Mutual Exclusion Occurs in a Chlorella-like Green Alga Inoculated with Two Viruses

Chase, Thomas E.; Nelson, Jennifer; Burbank, Dwight E.; Etten, James L. Van

doi:10.1099/0022-1317-70-7-1829

Cited by 31 publications

(26 citation statements)

References 15 publications

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“…Xia et al, 1986Xia et al, , 1987Xia et al, , 1988Chan et al, 2004) and it was originally suggested that one function of the DNA restriction endonucleases might be to exclude infection by other viruses. However, experimental results did not support this suggestion (Chase et al, 1989). …”

Section: Introductionmentioning

confidence: 95%

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Chlorella viruses prevent multiple infections by depolarizing the host membrane

Greiner

Frohns

Kang

et al. 2009

Journal of General Virology

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Previous experiments established that when the unicellular green alga Chlorella NC64A is inoculated with two viruses, usually only one virus replicates in a single cell. That is, the viruses mutually exclude one another. In the current study, we explore the possibility that virus-induced host membrane depolarization, at least partially caused by a virus-encoded K+ channel (Kcv), is involved in this mutual exclusion. Two chlorella viruses, PBCV-1 and NY-2A, were chosen for the study because (i) they can be distinguished by real-time PCR and (ii) they exhibit differential sensitivity to Cs+, a well-known K+ channel blocker. PBCV-1-induced host membrane depolarization, Kcv channel activity and plaque formation are only slightly affected by Cs+, whereas all three NY-2A-induced events are strongly inhibited by Cs+. The addition of one virus 5–15 min before the other results primarily in replication of the first virus. However, if virus NY-2A-induced membrane depolarization of the host is blocked by Cs+, PBCV-1 is not excluded. We conclude that virus-induced membrane depolarization is at least partially responsible for the exclusion phenomenon.

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Section: Introductionmentioning

confidence: 95%

“…That is, plaques arising from single cells simultaneously inoculated with two different chlorella viruses usually only contain one of the two viruses (Chase et al, 1989). Among the various chlorella viruses used in these competition experiments, some effectively out-compete others in the infection process, i.e.…”

Section: Introductionmentioning

confidence: 99%

Chlorella viruses prevent multiple infections by depolarizing the host membrane

Greiner

Frohns

Kang

et al. 2009

Journal of General Virology

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“…To determine whether the endonuclease(s) excludes infection of a cell by a second virus, chlorella cells were dually inoculated with different viruses and plaques arising from infective centers were distinguished by immunoblotting (20). These experiments revealed that the chlorella viruses, like certain bacteriophages (see 36) exclude one another.…”

Section: Dna Methyltransferases and Site-specific Endonucleasesmentioning

confidence: 99%

“…(b) Multiple virus particles can attach to and degrade the host cell wall without releasing their DNA (J. L. Van Etten, unpublished results). (c) The host exhibits an exclusion phenomenon (see section on DNA MTases and site-specific endonucleases) (20).…”

Section: Ion Channel Proteinsmentioning

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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“…To test the other hypothesis, i.e., that REases exclude infection of a host cell by a second virus, chlorella cells were dually inoculated with different viruses, and plaques arising from infective centers were distinguished by immunoblotting (5). These experiments established that the chloroviruses, like certain bacteriophages, exclude one another; however, this exclusion is independent of the REase activities of the viruses.…”

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confidence: 99%

Virion-Associated Restriction Endonucleases of Chloroviruses

Agarkova

Dunigan

Etten

2006

J Virol

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Chloroviruses are large, double-stranded-DNA, plaque-forming viruses that infect certain eukaryotic chlorella-like green algae. The prototype of the genus is Paramecium bursaria chlorella virus 1 (PBCV-1). Chlorovirus genomes contain various amounts of methylated nucleotides due to virus-encoded DNA methyltransferases (MTases); about 25% of the MTases are associated with companion DNA site-specific (restriction) endonucleases (REases). These enzymes constitute virally encoded restriction-modification (R/M) systems. Although several of the chlorovirus R/M systems are characterized, their biological functions are unknown. The PBCV-1 proteome reveals that two virus-encoded REases, but not their companion MTases, are virion associated, suggesting that viral REases might help degrade the host DNA early in infection. To test this hypothesis, host chromosomal DNA from PBCV-1-infected cells was examined by pulsed-field gel electrophoresis. Initiation of host chromosomal DNA degradation occurred within 5 min postinfection (p.i.). The DNA degradation was insensitive to protein synthesis inhibitors or UV inactivation of virus particles, consistent with the agent being a small protein associated with the virion. Nuclease activities, including those of the two predicted REases and an uncharacterized general nuclease(s), were detected in disrupted PBCV-1 particles. The general nuclease(s) degraded both host and viral DNAs in vitro, although the viral DNA was not degraded in vivo, suggesting differential intracellular trafficking of the virion-associated nucleases. Infection with chloroviruses lacking an R/M system(s) resulted in either delayed host chromosomal DNA degradation or no detectable host chromatin changes. These immediate-early events associated with chlorovirus infections may facilitate rapid switching of the host transcriptional apparatus to viral transcription, which begins within 5 to 10 min p.i.Chloroviruses are large, icosahedral, plaque-forming, genetically diverse but morphologically similar, linear, doublestranded-DNA (dsDNA) viruses (315 to 380 kb) that belong to the family Phycodnaviridae and the genus Chlorovirus (8, 22). The prototype chlorovirus, Paramecium bursaria chlorella virus 1 (PBCV-1), has a 331-kb genome that contains 366 proteinencoding genes and a polycistronic tRNA gene encoding 11 tRNAs. The chloroviruses infect certain freshwater, unicellular, chlorella-like green algae (e.g., Chlorella strain NC64A or Chlorella strain Pbi), which normally exist as endosymbionts in the protozoan Paramecium bursaria. Viruses that infect Chlorella NC64A (NC64A viruses) are serologically different from viruses that infect Chlorella Pbi (Pbi viruses). NC64A viruses neither infect nor attach to Chlorella Pbi, and vice versa (16).One distinctive feature of the chloroviruses is that their genomes contain methylated nucleotides: 5-methylcytosine (m5C) levels range from 0.1% to 47% of the total cytosines, and N 6 -methyladenine (m6A) levels vary from 0% to 37% of the total adenines (25, 26). The discovery that m5C...

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Mutual Exclusion Occurs in a Chlorella-like Green Alga Inoculated with Two Viruses

Cited by 31 publications

References 15 publications

Chlorella viruses prevent multiple infections by depolarizing the host membrane

Chlorella viruses prevent multiple infections by depolarizing the host membrane

Unusual Life Style of Giant Chlorella Viruses

Virion-Associated Restriction Endonucleases of Chloroviruses

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