Metagenome-derived virus-microbe ratios across ecosystems

Abstract

It is generally assumed that viruses outnumber cells on Earth by at least tenfold. 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, gene-transfer 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 um 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 model lines, lysogenic genes significantly correlated with cell, but not necessarily biotope, density. While viruses likely are the most diverse biological entities on Earth, our results suggest that cells are the most abundant and that cellular parasites may exert population-size control in some high-density ecosystems.

Viruses Defined by the Position of the Virosphere within the Replicator Space

“…MGEs are ubiquitous in the biosphere. Packaged MGEs, also known as "virus particles (virions)," appear to be among the most common biological entities on earth, with many more virus particles than cells detectable in at least some environments (11)(12)(13)-although the distribution of the virus/cell ratios in different habitats varies substantially and remains a matter of ongoing investigation (14,15). Along similar lines, typical genes of MGEs, such as those encoding transposases, are the most abundant genetic moieties in the oceans (16), and MGEs in different stages of decay account for most of the genetic material in many complex organisms with large genomes, such as animals, plants, and some protists (17,18).…”

Bacterial defenses and their trade-off with growth are not ubiquitous but depend on ecological contexts

“…Bacterial viruses, also known as phages or bacteriophages, represent the most abundant biological entities on Earth. They significantly outnumber bacterial cells across various samples and microbiomes, with ratios reaching up to ~15-25 fold, as observed in freshwater plankton (López-García et al 2023;Roux and Brum 2023). With few exceptions, such as intracellular parasitic and symbiotic bacteria, the majority of bacterial species fall prey to phages (Koonin et al 2017).…”

Viruses contribute to microbial diversification in the rumen ecosystem and are associated with certain animal production traits

“…It is worth noting that the above two methods likely underestimate phage abundance because they primarily account for free lytic virions. In contrast, VHR calculated from metagenomic sequences can quantify not only free virions but also temperate phages and intracellular lytic phages (78). Furthermore, the single-cell polony method can help identify lineage-resolved viral infections across thousands of cells of various microbes simultaneously (which was not certified by peer review) is the author/funder.…”