Ribonucleotide reductase genes influence the biology and ecology of marine viruses
Date
2019
Authors
Journal Title
Journal ISSN
Volume Title
Publisher
University of Delaware
Abstract
In marine systems, virioplankton are critical to biogeochemical cycling, microbial mortality, and horizontal gene transfer. However, relatively little is known about the ecology and biology of environmental phage populations, largely due to the lack of a universal marker. Viral marker genes such as ribonucleotide reductase (RNR) can provide insight into both phage diversity and phenotype. RNRs are ancient enzymes that reduce ribonucleotides to deoxyribonucleotides. This is the only known de novo pathway for dNTP synthesis and is the rate-limiting step of DNA synthesis. Thus, RNRs are common in the genomes of lytic dsDNA phage. RNRs are divided into three classes based on their reactivity with oxygen: Class I RNRs are O2-dependent; Class II RNRs are O2-independent, B12-dependent; and Class III RNRs are O2-sensitive. Class I is further divided into subclasses (Ia-If) based on metal requirements. These biochemical differences tie RNRs and their cellular carriers closely to their environments. We hypothesized that this connection would hold true for viruses as well as cells, making RNRs informative at both the individual virus and community levels. At the individual level, we corrected a misannotation of the RNR in a cyanophage, revealing an RNR with highly specific adaptations to the intracellular environment of its host. This cyanophage RNR also showed adaptations that may have a role in driving its observed highly lytic phenotype. At the community level, the RNR-containing virus community was reflective of the total viral community and that viruses with different RNR types had different ecological distributions in the oceans. RNR type distributions mirrored those of the trace metals required for RNR activity, except for subclass If. Subclass If is exclusive to cyanophage, so this subclass mirrored the distributions of marine Synechococcus and Prochlorococcus. Together, these two stories show RNRs as drivers of marine viral ecology and influencers of viral phenotype and life history strategies.