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Viruses and Virus-Like Particles of Eukaryotic Algae University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Papers in Plant Pathology Plant Pathology Department 12-1991 Viruses and Virus-like Particles of Eukaryotic Algae James L. Van Etten University of Nebraska-Lincoln, [email protected] Leslie C. Lane University of Nebraska-Lincoln, [email protected] Russel H. Meints Oregon State University Follow this and additional works at: https://digitalcommons.unl.edu/plantpathpapers Part of the Plant Pathology Commons Van Etten, James L.; Lane, Leslie C.; and Meints, Russel H., "Viruses and Virus-like Particles of Eukaryotic Algae" (1991). Papers in Plant Pathology. 115. https://digitalcommons.unl.edu/plantpathpapers/115 This Article is brought to you for free and open access by the Plant Pathology Department at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Papers in Plant Pathology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. MICROBIOLOGICAL REVIEWS, Dec. 1991, p. 586-620 Vol. 55, No. 4 0146-0749/91/040586-35$02.00/0 Copyright C 1991, American Society for Microbiology Viruses and Viruslike Particles of Eukaryotic Algae JAMES L. VAN ETTEN,1* LESLIE C. LANE,' AND RUSSEL H. MEINTS2 Department of Plant Pathology, University of Nebraska, Lincoln, Nebraska 68583-0722,1 and Department ofBotany and Plant Pathology, Center for Gene Research and Biotechnology, Oregon State University, Corvallis, Oregon 97331-2906 INTRODUCTION ................................................................................... 586 CHARACTERISTICS OF CHLORELLA SPECIES ......................................................................587 General Properties of Chlorella Species ...................................................................................587 Symbiotic Chlorella Species ................................................................................... 590 Chlorella Strains NC64A, Nla, Pbi, and SAG-241-80 .................................................................591 DISCOVERY OF CHLORELLA VIRUSES .................................................................................591 Initial Observations ................................................................................... 591 Development of a Culturable System for PBCV-1 ......................................................................592 PROPERTIES OF CHLORELLA VIRUSES ................................................................................592 General Characteristics of PBCV-1 ................................................................................... 592 Composition of PBCV-1 ................................................................................... 594 PBCV-1 Genome ................................................................................... 596 Serology of PBCV-1 ................................................................................... 597 Additional Chlorella Strain NC64A Viruses ..............................................................................598 Viruses Infecting Chlorella Strain Pbi ................................................................................... 598 REPLICATION OF PBCV-1 ................................................................................... 598 Attachment of PBCV-1 to Chlorella Strain NC64A ....................................................................598 Intracellular Site of PBCV-1 Replication .................................................................................600 Effect of PBCV-1 Infection on Host DNA, RNA, and Protein Syntheses .........................................604 TRANSCRIPTION OF PBCV-1 ................................................................................... 604 VIRUSES ENCODE DNA METHYLTRANSFERASES AND DNA SITE-SPECIFIC (RESTRICTION) ENDONUCLEASES ................................................................................... 607 PBCV-1 DNA Methyltransferases and DNA Site-Specific Endonucleases ........................................607 Additional Viral DNA Methyltransferases and DNA Site-Specffic Endonucleases ..............................607 SEQUENCE OF VIRUS-ENCODED DNA METHYLTRANSFERASES ............................................609 FUNCTION OF VIRUS-ENCODED DNA SITE-SPECIFIC ENDONUCLEASES AND DNA METHYLTRANSFERASES ................................................................................... 609 NATURAL HISTORY OF THE CHLORELLA VIRUSES ..............................................................610 COMPARISON OF CHLORELLA VIRUSES WITH OTHER VIRUSES ...........................................611 PROPERTIES OF VIRUSES OR VLPs OF OTHER ALGAE ........................................................612 CONCLUDING COMMENTS ................................................................................... 615 ACKNOWLEDGMENTS ................................................................................... 616 REFERENCES ................................................................................... 616 INTRODUCTION photosynthesis, cell cycle regulation, cell motility, and non- Mendelian (chloroplast) inheritance. Given the importance Eukaryotic algae range in size and complexity from small of eukaryotic algae, there is surprisingly little information unicellular organisms (microalgae) to large multicellular or- about viruses or viruslike particles (VLP) in these organ- ganisms (macroalgae), such as seaweeds. Most eukaryotic isms. algae are free living, and members can grow and survive in It is difficult to credit the first person who described a virus many terrestrial and aquatic environments. A few, however, or VLP in a eukaryotic alga. The problem is complicated are found only in symbiotic association with other organisms because early reports consisted solely of microscopic obser- such as molluscs, flatworms, coelenterates, protozoa, and vations and, in some cases, cultures were not axenic. A few fungi (lichens). Algae significantly influence aquatic environ- in the Russian literature as as 30 both as in the food chain papers long years ago ments, primary producers and, described a lytic activity in cultures of the green alga conversely, as pollutants when growth becomes uncon- trolled. Because most algae require only light, simple salts, Chlorella pyrenoidosa (174, 224-226). This lytic activity was and a nitrogen source for rapid growth, they are potential given the name "chlorellophage." However, these investi- producers of proteins, carbohydrates, and fats for feeding gators acknowledged that their cultures were contaminated humans and animals. In addition, algae are a source of useful with bacteria. Furthermore, the chlorellophage had typical compounds such as 13-carotene, alginic acid, carrageenans, bacteriophage morphology (174, 224). Therefore, despite the and agar (12, 137, 148). Algae such as Chlamydomonas and name chlorellophage, the host for these particles is unclear. Chlorella spp. have also served as models for studying Several investigators, almost simultaneously, reported the presence of VLPs in eukaryotic algae in the early 1970s. Lee (73) described 50- to 60-nm polyhedral particles in vegetative * Corresponding author. cells of the red alga Sirodotia tenuissima, Pickett-Heaps 586 VOL. 55, 1991 VIRUSES OF EUKARYOTIC ALGAE 587 (123) described polyhedral particles (240 nm in diameter) in digestion of the parental walls. The autospores develop germlings of the green alga Oedogonium sp., and Toth and rapidly into vegetative cells. The number of progeny formed Wilce (176) described 170-nm polyhedral particles in spores from a single vegetative cell varies with species and envi- of the marine brown alga Chorda tomentosa. Since these ronmental conditions (200). initial reports, VLPs or viruses have been reported in at least Chlorella species typically grow on a simple salts solution 44 taxa of eukaryotic algae (Table 1). These are distributed in and utilize ammonium, or as a 10 of the 14 recognized classes of eukaryotic algae nitrate, amino nitrogen (141). nitrogen source (116). However, they often grow best on Particles have not been found in any member of the families casein Euglenophyceae, Bacillariophyceae, Raphidophyceae, and hydrolysate (91, 151). Simple sugars such as sucrose Tribophyceae. VLPs and viruses of eukaryotic algae have or glucose increase the growth rate of some species but been reviewed previously by Lemke (74), Sherman and inhibit the growth of others. The doubling time varies with Brown (149), Dodds (27, 28), Martin and Benson (84), and the strain or species, but many of them double in about 24 h. Van Etten et al. (190, 192). The review by Sherman and Algae assigned to the genus Chlorella are more heteroge- Brown contains several electron micrographs of these parti- neous than their simple morphology suggests (25, 58, 65, cles, including some not published elsewhere. One other 151). Huss et al. are examining the relationships among report is noteworthy. In 1970 Schnepf et al. (143) described Chlorella species by using DNA base ratios, DNA hybrid- large (200 nm in diameter) polyhedral particles in an Aph- ization, and DNA reassociation kinetics (see reference 58 elidium sp. (which, although described as a fungus, may and references cited therein). The guanosine-plus-cytosine actually be a protozoan) that parasitized the green alga content of nuclear DNA, which ranges from 43 to 79% (49), Scenedesmus armatus. These particles were much larger reflects the heterogeneity of algae assigned to the genus than most fungal viruses
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