Deciphering the virus-to-prokaryote ratio (VPR): insights into virus–host relationships in a variety of ecosystems

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Abstract

The discovery of the numerical importance of viruses in a variety of (aquatic) ecosystems has changed our perception of their importance in microbial processes. Bacteria and Archaea undoubtedly represent the most abundant cellular life forms on Earth and past estimates of viral numbers (represented mainly by viruses infecting prokaryotes) have indicated abundances at least one order of magnitude higher than that of their cellular hosts. Such dominance has been reflected most often by the virus-to-prokaryote ratio (VPR), proposed as a proxy for the relationship between viral and prokaryotic communities. VPR values have been discussed in the literature to express viral numerical dominance (or absence of it) over their cellular hosts, but the ecological meaning and interpretation of this ratio has remained somewhat nebulous or contradictory. We gathered data from 210 publications (and additional unpublished data) on viral ecology with the aim of exploring VPR. The results are presented in three parts: the first consists of an overview of the minimal, maximal and calculated average VPR values in an extensive variety of different environments. Results indicate that VPR values fluctuate over six orders of magnitude, with variations observed within each ecosystem. The second part investigates the relationship between VPR and other indices, in order to assess whether VPR can provide insights into virus–host relationships. A positive relationship was found between VPR and viral abundance (VA), frequency of visibly infected cells (FVIC), burst size (BS), frequency of lysogenic cells (FLC) and chlorophyll a (Chl a) concentration. An inverse relationship was detected between VPR and prokaryotic abundance (PA) (in sediments), prokaryotic production (PP) and virus–host contact rates (VCR) as well as salinity and temperature. No significant relationship was found between VPR and viral production (VP), fraction of mortality from viral lysis (FMVL), viral decay rate (VDR), viral turnover (VT) or depth. Finally, we summarize our results by proposing two scenarios in two contrasting environments, based on current theories on viral ecology as well as the present results. We conclude that since VPR fluctuates in every habitat for different reasons, as it is linked to a multitude of factors related to virus–host dynamics, extreme caution should be used when inferring relationships between viruses and their hosts. Furthermore, we posit that the VPR is only useful in specific, controlled conditions, e.g. for the monitoring of fluctuations in viral and host abundance over time.

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