Amazing structural diversity of giant virus-like particles in forest soil

Abstract

Large DNA viruses of the phylumNucleocytoviricotainfect diverse eukaryotic hosts from protists to humans, with profound consequences for aquatic and terrestrial ecosystems. While nucleocytoviruses are known to be highly diverse in metagenomes, knowledge of their capsid structures is restricted to a few characterized representatives. Here, we visualize giant virus-like particles (VLPs, diameter >0.2 μm) directly from the environment using transmission electron microscopy. We found that Harvard Forest soils contain a higher diversity of giant VLP morphotypes than all hitherto isolated giant viruses combined. These included VLPs with icosahedral capsid symmetry, ovoid shapes similar to pandoraviruses, and bacilliform shapes that may represent novel viruses. We discovered giant icosahedral capsids with structural modifications that had not been described before including tubular appendages, modified vertices, tails, and capsids consisting of multiple layers or internal channels. Many giant VLPs were covered with fibers of varying lengths, thicknesses, densities, and terminal structures. These findings imply that giant viruses employ a much wider array of capsid structures and mechanisms to interact with their host cells than is currently known. We also found diverse tailed bacteriophages and filamentous VLPs, as well as ultra-small cells. Our study offers a first glimpse of the vast diversity of unexplored viral structures in soil and reinforces the potential of transmission electron microscopy for fundamental discoveries in environmental microbiology.

Unexpected diversity and ecological significance of uncultivable large virus-like particles in aquatic environments

“…The ubiquitous distribution of Shield VLPs, which developed at different times of the year under contrasting environmental conditions, was reinforced by our observations of numerous Shield morphotypes in marine systems in which they can reach 8.3 x 10 4 VLPs.mL -1 in surface area ( Extended data Fig. 3C ) as well as by their previous observation in soils 26 . Coupled with the pleomorphism of Shield VLPs and its potential host range, we suggest that this could represent a new generalist phylum, not considered until now, which plays a major ecological role in the regulation of microeukaryotes in many environments.…”

“…Here, we discovered four new abundant large viral morphotypes. Whereas VLPs resembling the Shield form were previously detected in soil samples, dubbed as the “Christmas star” 26 , the Ham, Snake and Sword VLPs present completely new shapes never before observed. In addition, we provide the morphological characterization and monitoring of abundant large icosahedral VLPs and highlight the ecological significance of the total community of large VLPs of microeukaryotes.…”

“…Data from cultures 5,6,10–12 , microscopic observations 26 , and genomic analyses 2,14–17 have led to fundamental discoveries in the study of large viruses. However, in the absence of a methodology to detect, characterize, and quantify their non-cultivable representatives, their diversity and ecological importance remains underexplored.…”

“…To tackle the limitations of both culture and omics-based studies, Fischer et al 26 recently used transmission electron microscopy (TEM) to complement metagenomic approaches, thus revealing the surprising structural diversity of giant virus-like particles (VLPs) in forest soils. Although this methodology allows us to identify and categorize giant viruses based on morphological criteria, it is time-consuming and difficult to apply at high throughput.…”

Widespread Horizontal Gene Transfer Among Animal Viruses

“…A more general hypothesis is that virion architecture may be more plastic than has previously been appreciated. One line of support for this idea is the remarkable range of virion morphotypes observed in electron micrographs of forest soil samples (Fischer et al, 2023). At a primary sequence level, some adintovirus species do not have detectable Cah or Penton genes, some species have highly elaborate predicted Cah or Penton genes, and some species have duplicate Cah or Penton ORFs.…”