Non-host class II ribonucleotide reductase in Thermus viruses: sequence adaptation and host interaction
Ribonucleotide reductases (RNR) are essential enzymes for all known life forms. Their current taxonomic distribution suggests extensive horizontal gene transfer e.g., by processes involving viruses. To improve our understanding of the underlying processes, we characterized a monomeric class II RNR (...
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PeerJ Inc.
2019-04-01
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| Online Access: | https://peerj.com/articles/6700.pdf |
| _version_ | 1797420517559369728 |
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| author | Christoph Loderer Karin Holmfeldt Daniel Lundin |
| author_facet | Christoph Loderer Karin Holmfeldt Daniel Lundin |
| author_sort | Christoph Loderer |
| collection | DOAJ |
| description | Ribonucleotide reductases (RNR) are essential enzymes for all known life forms. Their current taxonomic distribution suggests extensive horizontal gene transfer e.g., by processes involving viruses. To improve our understanding of the underlying processes, we characterized a monomeric class II RNR (NrdJm) enzyme from a Thermus virus, a subclass not present in any sequenced Thermus spp. genome. Phylogenetic analysis revealed a distant origin of the nrdJm gene with the most closely related sequences found in mesophiles or moderate thermophiles from the Firmicutes phylum. GC-content, codon usage and the ratio of coding to non-coding substitutions (dN/dS) suggest extensive adaptation of the gene in the virus in terms of nucleotide composition and amino acid sequence. The NrdJm enzyme is a monomeric B12-dependent RNR with nucleoside triphosphate specificity. It exhibits a temperature optimum at 60–70 °C, which is in the range of the growth optimum of Thermus spp. Experiments in combination with the Thermus thermophilus thioredoxin system show that the enzyme is able to retrieve electrons from the host NADPH pool via host thioredoxin and thioredoxin reductases. This is different from other characterized viral RNRs such as T4 phage RNR, where a viral thioredoxin is present. We hence show that the monomeric class II RNR, present in Thermus viruses, was likely transferred from an organism phylogenetically distant from the one they were isolated from, and adapted to the new host in genetic signature and amino acids sequence. |
| first_indexed | 2024-03-09T07:02:38Z |
| format | Article |
| id | doaj.art-dd9ff42cb87a483f9fc300a97638111e |
| institution | Directory Open Access Journal |
| issn | 2167-8359 |
| language | English |
| last_indexed | 2024-03-09T07:02:38Z |
| publishDate | 2019-04-01 |
| publisher | PeerJ Inc. |
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| spelling | doaj.art-dd9ff42cb87a483f9fc300a97638111e2023-12-03T09:49:02ZengPeerJ Inc.PeerJ2167-83592019-04-017e670010.7717/peerj.6700Non-host class II ribonucleotide reductase in Thermus viruses: sequence adaptation and host interactionChristoph Loderer0Karin Holmfeldt1Daniel Lundin2Institute for Microbiology, Technische Universität Dresden, Dresden, Saxony, GermanyCentre for Ecology and Evolution in Microbial model Systems—EEMiS, Linnaeus University, Kalmar, SwedenCentre for Ecology and Evolution in Microbial model Systems—EEMiS, Linnaeus University, Kalmar, SwedenRibonucleotide reductases (RNR) are essential enzymes for all known life forms. Their current taxonomic distribution suggests extensive horizontal gene transfer e.g., by processes involving viruses. To improve our understanding of the underlying processes, we characterized a monomeric class II RNR (NrdJm) enzyme from a Thermus virus, a subclass not present in any sequenced Thermus spp. genome. Phylogenetic analysis revealed a distant origin of the nrdJm gene with the most closely related sequences found in mesophiles or moderate thermophiles from the Firmicutes phylum. GC-content, codon usage and the ratio of coding to non-coding substitutions (dN/dS) suggest extensive adaptation of the gene in the virus in terms of nucleotide composition and amino acid sequence. The NrdJm enzyme is a monomeric B12-dependent RNR with nucleoside triphosphate specificity. It exhibits a temperature optimum at 60–70 °C, which is in the range of the growth optimum of Thermus spp. Experiments in combination with the Thermus thermophilus thioredoxin system show that the enzyme is able to retrieve electrons from the host NADPH pool via host thioredoxin and thioredoxin reductases. This is different from other characterized viral RNRs such as T4 phage RNR, where a viral thioredoxin is present. We hence show that the monomeric class II RNR, present in Thermus viruses, was likely transferred from an organism phylogenetically distant from the one they were isolated from, and adapted to the new host in genetic signature and amino acids sequence.https://peerj.com/articles/6700.pdfRibonucleotide reductaseHorizontal gene transferBacteriophage-derived enzymesThioredoxinTransductionHost-adaptation |
| spellingShingle | Christoph Loderer Karin Holmfeldt Daniel Lundin Non-host class II ribonucleotide reductase in Thermus viruses: sequence adaptation and host interaction PeerJ Ribonucleotide reductase Horizontal gene transfer Bacteriophage-derived enzymes Thioredoxin Transduction Host-adaptation |
| title | Non-host class II ribonucleotide reductase in Thermus viruses: sequence adaptation and host interaction |
| title_full | Non-host class II ribonucleotide reductase in Thermus viruses: sequence adaptation and host interaction |
| title_fullStr | Non-host class II ribonucleotide reductase in Thermus viruses: sequence adaptation and host interaction |
| title_full_unstemmed | Non-host class II ribonucleotide reductase in Thermus viruses: sequence adaptation and host interaction |
| title_short | Non-host class II ribonucleotide reductase in Thermus viruses: sequence adaptation and host interaction |
| title_sort | non host class ii ribonucleotide reductase in thermus viruses sequence adaptation and host interaction |
| topic | Ribonucleotide reductase Horizontal gene transfer Bacteriophage-derived enzymes Thioredoxin Transduction Host-adaptation |
| url | https://peerj.com/articles/6700.pdf |
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