Viral and parasitic cell ratios per free-living microbe across ecosystems

Abstract

ABSTRACTIt is generally assumed that viruses outnumber cells on Earth by at least tenfold1–4. Virus-to-microbe ratios (VMR) are largely based on fluorescently-labelled viral-like particles (VLPs) counts. However, these exclude cell-infecting lytic and lysogenic viruses and potentially include many false positives, e.g. DNA-containing membrane vesicles, genetransfer agents or inert particles. Here, we develop a metagenome-based VMR estimate (mVRM) accounting for all viral stages (virion-lytic-lysogenic) using normalised counts of viral DNA-polymerases and cellular universal single-copy genes as proxies for individuals. To properly estimate mVMR in aquatic ecosystems, we generated metagenomes from co-occurring cellular and viral fractions (>50 kDa-200 μm size range) in freshwater, seawater and 6-14-32% salt solar-saltern ponds. Viruses outnumbered cells in non-blooming freshwater and marine plankton by around twofold. However, mVMR in 133 uniformly-analysed metagenomes from diverse ecosystems showed that free-living cells largely exceeded viruses and epibiont DPANN archaea and/or CPR bacteria in compact environments (sediments, soils, microbial mats, host-associated microbiomes). Along the Piggyback-the-winner model5 lines, lysogenic genes significantly correlated with cell, but not necessarily biotope, density. While viruses likely are the most diverse biological entities on Earth6,7, our results suggest that cells are the most abundant and that cellular parasites may exert population-size control in some high-density ecosystems.