Mimivirus Fibrils Are Important for Viral Attachment to the Microbial World by a Diverse Glycoside Interaction Repertoire

Abstract

Acanthamoeba polyphaga mimivirus (APMV) is a giant virus from the Mimiviridae family. It has many unusual features, such as a pseudoicosahedral capsid that presents a starfish shape in one of its vertices, through which the ϳ1.2-Mb double-stranded DNA is released. It also has a dense glycoprotein fibril layer covering the capsid that has not yet been functionally characterized. Here, we verified that although these structures are not essential for viral replication, they are truly necessary for viral adhesion to amoebae, its natural host. In the absence of fibrils, APMV had a significantly lower level of attachment to the Acanthamoeba castellanii surface. This adhesion is mediated by glycans, specifically, mannose and N-acetylglucosamine (a monomer of chitin and peptidoglycan), both of which are largely distributed in nature as structural components of several organisms. Indeed, APMV was able to attach to different organisms, such as Gram-positive bacteria, fungi, and arthropods, but not to Gram-negative bacteria. This prompted us to predict that (i) arthropods, mainly insects, might act as mimivirus dispersers and (ii) by attaching to other microorganisms, APMV could be ingested by amoebae, leading to the successful production of viral progeny. To date, this mechanism has never been described in the virosphere. IMPORTANCEAPMV is a giant virus that is both genetically and structurally complex. Its size is similar to that of small bacteria, and it replicates inside amoebae. The viral capsid is covered by a dense glycoprotein fibril layer, but its function has remained unknown, until now. We found that the fibrils are not essential for mimivirus replication but that they are truly necessary for viral adhesion to the cell surface. This interaction is mediated by glycans, mainly N-acetylglucosamine. We also verified that APMV is able to attach to bacteria, fungi, and arthropods. This indicates that insects might act as mimivirus dispersers and that adhesion to other microorganisms could facilitate viral ingestion by amoebae, a mechanism never before described in the virosphere.

The Large Marseillevirus Explores Different Entry Pathways by Forming Giant Infectious Vesicles

“…Using several different approaches, we have demonstrated that MsV either can interact with the cell surface and enter through endocytosis or can be found inside giant vesicles that stimulate the phagocytosis mechanism. Finally, the discovery of giant viruses not only has brought to light their genomic complexity, with hundreds of new genes/proteins that are able to perform activities never before attributable to a virus, but also allowed us a glimpse into a microcosm of ecological interactions, where viruses are able, for example, to actively seek new hosts and habitats by adsorbing into other, more complex life forms, such as fungi and arthropods (14). Here, we have identified yet another possible ecological strategy for the release of a giant virus from its last host in vesicles that have the potential to boost its entry into another host, as well as to help it endure in the environment during an "interhost" period.…”

“…The pellet containing vesicles was collected and the supernatant containing only naked particles was discarded. After this purification, the samples were prepared for analysis by scanning electron microscopy (SEM), as previously described (14). Furthermore, we also evaluated if these vesicles could be phagocytosed by amoebas.…”

Biochemical analysis of a sugar 4,6‐dehydratase from Acanthamoeba polyphaga Mimivirus

“…Whether the unusual sugar 4‐amino‐4,6‐dideoxy‐ d ‐glucose is important for infection is presently unclear. What is known, however, is that the heavily glycosylated fibril layer of the virus is required for adhesion to the host organism . It is also not known whether giant viruses are capable of widespread human infections.…”

“…In terms of morphology, the APMV capsid displays pseudoicosahedral symmetry and is composed of proteins adopting the “double jelly roll fold.” Surrounding the capsid is a densely packed arrangement of highly glycosylated protein fibers that play a role in viral adhesion to its natural host, the amoeba . With respect to the glycan composition of the viral fibers, it has been shown that the unusual sugar 4‐amino‐4,6‐dideoxy‐ d ‐glucose is associated with these fibers .…”

A Student’s Guide to Giant Viruses Infecting Small Eukaryotes: From Acanthamoeba to Zooxanthellae

“…It has been hypothesized that these fibers work in tandem with the large size of the viruses to facilitate phagocytosis, as they appear to have a similar composition to peptidoglycan and thus help mimic a bacterium (indeed, the name Mimivirus comes from “ Mimicking Microbe ” [29]). Additionally, the fibrous glycoproteins enable viral adsorption to diverse organisms ranging from bacteria and fungi to arthropods [30], implying a potential for both environmental dispersion and an incidental infection strategy in amoeba. Phycodnaviridae may also use unique structures to gain access to their host, though their mode of entry is typically by adsorption/injection, as opposed to phagocytosis.…”