Unveiling Crucivirus Diversity by Mining Metagenomic Data
Ignacio de la Higuera,
George W. Kasun,
Ellis L. Torrance,
Alyssa A. Pratt,
Amberlee Maluenda,
Jonathan Colombet,
Maxime Bisseux,
Viviane Ravet,
Anisha Dayaram,
Daisy Stainton,
Simona Kraberger,
Peyman Zawar-Reza,
Sharyn Goldstien,
James V. Briskie,
Robyn White,
Helen Taylor,
Christopher Gomez,
David G. Ainley,
Jon S. Harding,
Rafaela S. Fontenele,
Joshua Schreck,
Simone G. Ribeiro,
Stephen A. Oswald,
Jennifer M. Arnold,
François Enault,
Arvind Varsani,
Kenneth M. Stedman
Affiliations
Ignacio de la Higuera
Department of Biology, Center for Life in Extreme Environments, Portland State University, Portland, Oregon, USA
George W. Kasun
Department of Biology, Center for Life in Extreme Environments, Portland State University, Portland, Oregon, USA
Ellis L. Torrance
Department of Biology, Center for Life in Extreme Environments, Portland State University, Portland, Oregon, USA
Alyssa A. Pratt
Department of Biology, Center for Life in Extreme Environments, Portland State University, Portland, Oregon, USA
Amberlee Maluenda
Department of Biology, Center for Life in Extreme Environments, Portland State University, Portland, Oregon, USA
Jonathan Colombet
Université Clermont Auvergne, CNRS, Laboratoire Microorganismes: Génome et Environnement, UMR 6023, Clermont–Ferrand, France
Maxime Bisseux
Université Clermont Auvergne, CNRS, Laboratoire Microorganismes: Génome et Environnement, UMR 6023, Clermont–Ferrand, France
Viviane Ravet
Université Clermont Auvergne, CNRS, Laboratoire Microorganismes: Génome et Environnement, UMR 6023, Clermont–Ferrand, France
Anisha Dayaram
Institut für Neurophysiology, Charité-Universitätsmedizin, Berlin, Germany
Daisy Stainton
Department of Entomology and Plant Pathology, Division of Agriculture, University of Arkansas System, Fayetteville, Arkansas, USA
Simona Kraberger
The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life Sciences, Arizona State University, Tempe, Arizona, USA
Peyman Zawar-Reza
School of Earth and Environment, University of Canterbury, Christchurch, New Zealand
Sharyn Goldstien
School of Biological Sciences, University of Canterbury, Christchurch, New Zealand
James V. Briskie
School of Biological Sciences, University of Canterbury, Christchurch, New Zealand
Robyn White
School of Biological Sciences, University of Canterbury, Christchurch, New Zealand
Helen Taylor
Department of Anatomy, University of Otago, Dunedin, New Zealand
Christopher Gomez
Graduate School of Maritime Sciences, Laboratory of Sediment Hazards and Disaster Risk, Kobe University, Kobe City, Japan
David G. Ainley
HT Harvey and Associates, Los Gatos, California, USA
Jon S. Harding
School of Biological Sciences, University of Canterbury, Christchurch, New Zealand
Rafaela S. Fontenele
The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life Sciences, Arizona State University, Tempe, Arizona, USA
Joshua Schreck
The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life Sciences, Arizona State University, Tempe, Arizona, USA
Simone G. Ribeiro
Embrapa Recursos Genéticos e Biotecnologia, Brasília, DF, Brazil
Stephen A. Oswald
Division of Science, Pennsylvania State University, Reading, Pennsylvania, USA
Jennifer M. Arnold
Division of Science, Pennsylvania State University, Reading, Pennsylvania, USA
François Enault
Université Clermont Auvergne, CNRS, Laboratoire Microorganismes: Génome et Environnement, UMR 6023, Clermont–Ferrand, France
Arvind Varsani
The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life Sciences, Arizona State University, Tempe, Arizona, USA
Kenneth M. Stedman
Department of Biology, Center for Life in Extreme Environments, Portland State University, Portland, Oregon, USA
ABSTRACT The discovery of cruciviruses revealed the most explicit example of a common protein homologue between DNA and RNA viruses to date. Cruciviruses are a novel group of circular Rep-encoding single-stranded DNA (ssDNA) (CRESS-DNA) viruses that encode capsid proteins that are most closely related to those encoded by RNA viruses in the family Tombusviridae. The apparent chimeric nature of the two core proteins encoded by crucivirus genomes suggests horizontal gene transfer of capsid genes between DNA and RNA viruses. Here, we identified and characterized 451 new crucivirus genomes and 10 capsid-encoding circular genetic elements through de novo assembly and mining of metagenomic data. These genomes are highly diverse, as demonstrated by sequence comparisons and phylogenetic analysis of subsets of the protein sequences they encode. Most of the variation is reflected in the replication-associated protein (Rep) sequences, and much of the sequence diversity appears to be due to recombination. Our results suggest that recombination tends to occur more frequently among groups of cruciviruses with relatively similar capsid proteins and that the exchange of Rep protein domains between cruciviruses is rarer than intergenic recombination. Additionally, we suggest members of the stramenopiles/alveolates/Rhizaria supergroup as possible crucivirus hosts. Altogether, we provide a comprehensive and descriptive characterization of cruciviruses. IMPORTANCE Viruses are the most abundant biological entities on Earth. In addition to their impact on animal and plant health, viruses have important roles in ecosystem dynamics as well as in the evolution of the biosphere. Circular Rep-encoding single-stranded (CRESS) DNA viruses are ubiquitous in nature, many are agriculturally important, and they appear to have multiple origins from prokaryotic plasmids. A subset of CRESS-DNA viruses, the cruciviruses, have homologues of capsid proteins encoded by RNA viruses. The genetic structure of cruciviruses attests to the transfer of capsid genes between disparate groups of viruses. However, the evolutionary history of cruciviruses is still unclear. By collecting and analyzing cruciviral sequence data, we provide a deeper insight into the evolutionary intricacies of cruciviruses. Our results reveal an unexpected diversity of this virus group, with frequent recombination as an important determinant of variability.
