Novel haloarchaeal viruses from Lake Retba infecting Haloferax and Halorubrum species
Carolina M. Mizuno
Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Institut Pasteur, 25 rue du Docteur Roux, 75015, Paris, France
Search for more papers by this authorBina Prajapati
Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Finland
Present address: Cell and Molecular Biology Program, Institute of Biotechnology, University of Helsinki, FinlandSearch for more papers by this authorSoizick Lucas-Staat
Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Institut Pasteur, 25 rue du Docteur Roux, 75015, Paris, France
Search for more papers by this authorTelesphore Sime-Ngando
CNRS UMR 6023, Université Clermont-Auvergne, Laboratoire "Microorganismes: Génome et Environnement" (LMGE), F-63000, Clermont-Ferrand, France
Search for more papers by this authorPatrick Forterre
Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Institut Pasteur, 25 rue du Docteur Roux, 75015, Paris, France
Search for more papers by this authorDennis H. Bamford
Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Finland
Search for more papers by this authorDavid Prangishvili
Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Institut Pasteur, 25 rue du Docteur Roux, 75015, Paris, France
Search for more papers by this authorCorresponding Author
Mart Krupovic
Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Institut Pasteur, 25 rue du Docteur Roux, 75015, Paris, France
For correspondence. *E-mail [email protected]; Tel. 33 (0)1 40 61 37 22; Fax 33 (0)1 45 68 88 34. **E-mail [email protected]; Tel. +358 (0) 2941 59104.Search for more papers by this authorCorresponding Author
Hanna M. Oksanen
Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Finland
For correspondence. *E-mail [email protected]; Tel. 33 (0)1 40 61 37 22; Fax 33 (0)1 45 68 88 34. **E-mail [email protected]; Tel. +358 (0) 2941 59104.Search for more papers by this authorCarolina M. Mizuno
Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Institut Pasteur, 25 rue du Docteur Roux, 75015, Paris, France
Search for more papers by this authorBina Prajapati
Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Finland
Present address: Cell and Molecular Biology Program, Institute of Biotechnology, University of Helsinki, FinlandSearch for more papers by this authorSoizick Lucas-Staat
Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Institut Pasteur, 25 rue du Docteur Roux, 75015, Paris, France
Search for more papers by this authorTelesphore Sime-Ngando
CNRS UMR 6023, Université Clermont-Auvergne, Laboratoire "Microorganismes: Génome et Environnement" (LMGE), F-63000, Clermont-Ferrand, France
Search for more papers by this authorPatrick Forterre
Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Institut Pasteur, 25 rue du Docteur Roux, 75015, Paris, France
Search for more papers by this authorDennis H. Bamford
Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Finland
Search for more papers by this authorDavid Prangishvili
Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Institut Pasteur, 25 rue du Docteur Roux, 75015, Paris, France
Search for more papers by this authorCorresponding Author
Mart Krupovic
Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Institut Pasteur, 25 rue du Docteur Roux, 75015, Paris, France
For correspondence. *E-mail [email protected]; Tel. 33 (0)1 40 61 37 22; Fax 33 (0)1 45 68 88 34. **E-mail [email protected]; Tel. +358 (0) 2941 59104.Search for more papers by this authorCorresponding Author
Hanna M. Oksanen
Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Finland
For correspondence. *E-mail [email protected]; Tel. 33 (0)1 40 61 37 22; Fax 33 (0)1 45 68 88 34. **E-mail [email protected]; Tel. +358 (0) 2941 59104.Search for more papers by this authorSummary
The diversity of archaeal viruses is severely undersampled compared with that of viruses infecting bacteria and eukaryotes, limiting our understanding on their evolution and environmental impacts. Here, we describe the isolation and characterization of four new viruses infecting halophilic archaea from the saline Lake Retba, located close to Dakar on the coast of Senegal. Three of the viruses, HRPV10, HRPV11 and HRPV12, have enveloped pleomorphic virions and should belong to the family Pleolipoviridae, whereas the forth virus, HFTV1, has an icosahedral capsid and a long non-contractile tail, typical of bacterial and archaeal members of the order Caudovirales. Comparative genomic and phylogenomic analyses place HRPV10, HRPV11 and HRPV12 into the genus Betapleolipovirus, whereas HFTV1 appears to be most closely related to the unclassified Halorubrum virus HRTV-4. Differently from HRTV-4, HFTV1 encodes host-derived minichromosome maintenance helicase and PCNA homologues, which are likely to orchestrate its genome replication. HFTV1, the first archaeal virus isolated on a Haloferax strain, could also infect Halorubrum sp., albeit with an eightfold lower efficiency, whereas pleolipoviruses nearly exclusively infected autochthonous Halorubrum strains. Mapping of the metagenomic sequences from this environment to the genomes of isolated haloarchaeal viruses showed that these known viruses are underrepresented in the available viromes.
Conflict of Interest
The authors have no conflict of interest to declare.
Supporting Information
| Filename | Description |
|---|---|
| emi14604-sup-0001-supinfo.docxWord 2007 document , 12.6 KB | Appendix S1: Supporting Information |
| emi14604-sup-0002-TableS1.xlsxExcel 2007 spreadsheet , 27.3 KB | Supplementary Table 1. Annotation of pleolipoviral genomes |
| emi14604-sup-0003-TableS2.xlsxExcel 2007 spreadsheet , 20.5 KB | Supplementary Table 2. Blastp of pleolipoviruses |
| emi14604-sup-0004-TableS3.xlsxExcel 2007 spreadsheet , 39.3 KB | Supplementary Table 3. Annotation of HFTV1 genome |
| emi14604-sup-0005-TableS4.docxWord 2007 document , 25 KB | Supplementary Table 4. Haloferax and Halorubrum culture collection strains used in this study |
| emi14604-sup-0006-Figures.pdfPDF document, 1.1 MB |
Supplementary Figure 1. Plaque morphologies of the Lake Retba viruses. Four plaques for each virus have been circled. A. HRPV10 hazy plaques of 3-5 mm in diameter. B. HRPV11 hazy plaques of 5-10 in diameter (very difficult to document, but visible in optimal lighting conditions). C. HRPV12 hazy plaques of 5-8 mm in diameter. D. HFTV1 clear plaques of 2-4 mm in diameter. Supplementary Figure 2. Comparison of genomic contigs obtained for HRPV11 using two different assembly algorithms (de novo assembly algorithm implemented in CLC Genomics Workbench v7 and SPAdes, respectively). Supplementary Figure 3. A and B. Maximum likelihood phylogeny of ORF4 (spike protein) and ORF7 (NTPase) from pleolipoviruses. Members of the genera Alphapleolipovirus, Betapleolipovirus, and Gammapleolipovirus are colored blue, orange, and green, respectively, whereas HRPV10-12 are highlighted in grey. C. Maximum likelihood phylogenetic tree of the large subunit of the terminases from cultivated and uncultivated tailed haloviruses. Uncultivated and cultivated haloviruses are highlighted with blue and orange backgrounds, respectively, whereas HFTV1 is shown on a grey background. Sequences were aligned using MUSCLE (Edgar, 2004) and maximum likelihood trees were constructed using the program FastTree2 (Price et al., 2010). The numbers above the branches represent bootstrap support values from 100 replicates. The scale bars represent the number of substitutions per site. Supplementary Figure 4. Analysis of the HFTV1 genome by nuclease treatments. Lane 1, non-treated genome; Lane 2, genome treated with RQ1 DNase; Lane 3, genome treated with Exonuclease III; Lane 4, genome treated with mung bean nuclease (5 U / mg DNA). The positions of the molecular mass markers (bp) are indicated on left. The arrow indicates the position of the agarose gel wells. Supplementary Figure 5. Classification of the HFTV1 open reading frames based on the best-blast hit analysis. Sequence similarity searches were performed using blastp algorithm against the NCBI non-redundant proteins database (for details, see Supplementary Table 3). Supplementary Figure 6. In silico analysis of the HFTV1 genome using PhageTerm, a tool specifically designed for determination of genomic termini and packaging mechanism using next-generation sequencing data. A. Sequence coverage at the predicted genomic terminus of HFTV1. Exact terminal position is represented by a dotted red line. B. Evaluation of alternative start positions in the HFTV1 genome. The position 92 is determined as the most likely start site with the best p-value. C. Summary of the PhageTerm results indicating terminal redundancy of the HFTV1 genome; the likely start position; the lack of defined right end of the genome (i.e., distributed); the circular permutation; orientation; the class of packaging mechanism; and the typical representative (bacteriophage P1) with a similar genome packaging mechanism. Supplementary Figure 7. A. Phylogenomic tree of cultivated and uncultivated tailed haloviruses was constructed using the Genome BLAST Distance Phylogeny (GBDP) strategy implemented in VICTOR (Meier-Kolthoff and Goker, 2017). The numbers above branches are GBDP pseudo-bootstrap support values from 100 replications. B. Recruitment plot for haloviruses against saltern viromes sequenced from the Lake Retba (Roux et al., 2016) and South Bay Salt Works (Rodriguez-Brito et al., 2010) was performed by BLASTN algorithm and expressed as Reads recruited Per Kb of genome per Gb of metagenome (RPKG) (see Experimental Procedures for details). |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
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