Abstract

The persistent inertia in the ability to culture environmentally abundant microbes from aquatic ecosystems represents an obstacle in disentangling the complex web of ecological interactions spun by a diverse assortment of participants (pro- and eukaryotes and their viruses). In aquatic microbial communities, the numerically most abundant actors, the viruses, remain the most elusive, and especially in freshwaters their identities and ecology remain unknown. Here, using ultra-deep metagenomic sequencing from pelagic freshwater habitats, we recovered complete genomes of > 2000 phages, including small “miniphages” and large “megaphages” infecting iconic freshwater prokaryotic lineages. For instance, abundant freshwater Actinobacteria support infection by a very broad size range of phages (13–200 Kb). We describe many phages encoding genes that likely afford protection to their host from reactive oxygen species (ROS) in the aquatic environment and in the oxidative burst in protist phagolysosomes (phage-mediated ROS defense). Spatiotemporal abundance analyses of phage genomes revealed evanescence as the primary dynamic in upper water layers, where they displayed short-lived existences. In contrast, persistence was characteristic for the deeper layers where many identical phage genomes were recovered repeatedly. Phage and host abundances corresponded closely, with distinct populations displaying preferential distributions in different seasons and depths, closely mimicking overall stratification and mixis.

Highlights

  • Freshwater planktonic communities are complex and dynamic, exhibiting distinct, recurrent patterns driven by both biotic and abiotic environmental factors [1]

  • Using the abundant freshwater Actinobacteria and their phages as models, we show that do phage genome abundances in deep water bodies mirror the abundance of their hosts, but they reflect the classical patterns in thermal cycles of the water column, i.e., stratification and mixis

  • Metagenomic sequencing, assembly, and complete phage genome recovery We chose for our study two sites that serve as models for two distinct freshwater habitat types: meso-eutrophic Římov reservoir, a typical man-made, canyon-shaped reservoir, common to north temperate regions [20], and Jiřická pond, a shallow, humic mountain pond habitat found across the world [21]

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Summary

Introduction

Freshwater planktonic communities are complex and dynamic, exhibiting distinct, recurrent patterns driven by both biotic and abiotic environmental factors [1]. We reconstructed 2034 complete genomes of phages infecting freshwater prokaryotes. Using the abundant freshwater Actinobacteria and their phages as models, we show that do phage genome abundances in deep water bodies mirror the abundance of their hosts, but they reflect the classical patterns in thermal cycles of the water column, i.e., stratification and mixis. High abundances for both phages and hosts in the epilimnion are transitory, and persistence at lower abundances in the hypolimnion, the far larger niche, is the rule

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