Ubiquitous, B12-dependent virioplankton utilizing ribonucleotide-triphosphate reductase demonstrate interseasonal dynamics and associate with a diverse range of bacterial hosts in the pelagic ocean

Author:

Wu Ling-Yi1,Piedade Gonçalo J23ORCID,Moore Ryan M4ORCID,Harrison Amelia O4ORCID,Martins Ana M3,Bidle Kay D5,Polson Shawn W4ORCID,Sakowski Eric G6ORCID,Nissimov Jozef I7ORCID,Dums Jacob T48ORCID,Ferrell Barbra D4,Wommack K Eric4ORCID

Affiliation:

1. Theoretical Biology and Bioinformatics, Science4Life, Utrecht University , Padualaan 8, Utrecht 3584 CH, the Netherlands

2. Department of Marine Microbiology and Biogeochemistry, NIOZ Royal Netherlands Institute for Sea Research , 1797 SZ t’Horntje, The Netherlands

3. Department of Oceanography and Fisheries and Ocean Sciences Institute-OKEANOS, University of the Azores , 9901-862 Horta, Faial, Azores, Portugal

4. Delaware Biotechnology Institute, University of Delaware , 590 Avenue 1743, Newark, DE 19713, USA

5. Department of Marine and Coastal Sciences, Rutgers University , 71 Dudley Rd., New Brunswick, NJ 08901, USA

6. Department of Earth Sciences, Johns Hopkins University , Baltimore, MD, USA

7. Department of Biology, University of Waterloo , 200 University Ave. West, Waterloo, ON N2L 3G1, Canada

8. Biotechnology Program, North Carolina State University , 2800 Faucette Dr, Raleigh, NC 27695, USA

Abstract

Abstract Through infection and lysis of their coexisting bacterial hosts, viruses impact the biogeochemical cycles sustaining globally significant pelagic oceanic ecosystems. Currently, little is known of the ecological interactions between lytic viruses and their bacterial hosts underlying these biogeochemical impacts at ecosystem scales. This study focused on populations of lytic viruses carrying the B12-dependent Class II monomeric ribonucleotide reductase (RNR) gene, ribonucleotide-triphosphate reductase (Class II RTPR), documenting seasonal changes in pelagic virioplankton and bacterioplankton using amplicon sequences of Class II RTPR and the 16S rRNA gene, respectively. Amplicon sequence libraries were analyzed using compositional data analysis tools that account for the compositional nature of these data. Both virio- and bacterioplankton communities responded to environmental changes typically seen across seasonal cycles as well as shorter term upwelling–downwelling events. Defining Class II RTPR-carrying viral populations according to major phylogenetic clades proved a more robust means of exploring virioplankton ecology than operational taxonomic units defined by percent sequence homology. Virioplankton Class II RTPR populations showed positive associations with a broad phylogenetic diversity of bacterioplankton including dominant taxa within pelagic oceanic ecosystems such as Prochlorococcus and SAR11. Temporal changes in Class II RTPR virioplankton, occurring as both free viruses and within infected cells, indicated possible viral–host pairs undergoing sustained infection and lysis cycles throughout the seasonal study. Phylogenetic relationships inferred from Class II RTPR sequences mirrored ecological patterns in virio- and bacterioplankton populations demonstrating possible genome to phenome associations for an essential viral replication gene.

Funder

National Science Foundation

CSC | Chinese Government Scholarship

EEA Grants

Delaware IDeA Network of Biomedical Research Excellence

Publisher

Oxford University Press (OUP)

Subject

General Medicine

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