Distinct DNA Exit and Packaging Portals in the Virus Acanthamoeba polyphaga mimivirus

University of Wisconsin, Madison, United States of America
PLoS Biology (Impact Factor: 9.34). 06/2008; 6(5):e114. DOI: 10.1371/journal.pbio.0060114
Source: PubMed


Author Summary

Two fundamental events in viral life cycles are the delivery of viral genomes into host cells and the packaging of these genomes into viral protein capsids. In bacteriophages and herpesviruses, these processes occur linearly along the genome, base pair after base pair, through a single portal located at a unique site in the viral capsid. We have addressed the question of whether such a linear translocation through a single portal also takes place for viruses harboring very large genomes, by studying genome delivery and packaging in the amoeba-infecting virus Acanthamoeba polyphaga mimivirus. With 1.2 million base pairs, this double-stranded DNA genome is the largest documented viral genome. By using electron tomography and cryo-scanning electron microscopy, we identified a large tunnel in the Mimivirus capsid that is formed shortly after infection, following a large-scale opening of the capsid. The tunnel allows the whole viral genome to exit in a rapid, one-step process. DNA encapsidation is mediated by a transient aperture in the capsid that, we suggest, may promote concomitant entry of multiple segments of the viral DNA molecule. These unprecedented modes of viral genome translocation imply that Mimivirus—and potentially other large viruses—evolved mechanisms that allow them to cope effectively with the exit and entry of particularly large genomes.

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    • "The membrane biogenesis of APMV is initiated from the host cytoplasmic membrane cisternae at around 7.5 h PI (Zauberman et al., 2008; Mutsafi et al., 2013). Regular budding of ∼70 nm vesicles from the cellular cisternae have been observed around the viral factories at earlier PI times (Mutsafi et al., 2013). "
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    ABSTRACT: Rab GTPases are the key regulators of intracellular membrane trafficking in eukaryotes. Many viruses and intracellular bacterial pathogens have evolved to hijack the host Rab GTPase functions, mainly through activators and effector proteins, for their benefit. Acanthamoeba polyphaga mimivirus (APMV) is one of the largest viruses and belongs to the monophyletic clade of nucleo-cytoplasmic large DNA viruses (NCLDV). The inner membrane lining is integral to the APMV virion structure. APMV assembly involves extensive host membrane modifications, like vesicle budding and fusion, leading to the formation of a membrane sheet that is incorporated into the virion. Intriguingly, APMV and all group I members of the Mimiviridae family code for a putative Rab GTPase protein. APMV is the first reported virus to code for a Rab GTPase (encoded by R214 gene). Our thorough in silico analysis of the subfamily specific (SF) region of Mimiviridae Rab GTPase sequences suggests that they are related to Rab5, a member of the group II Rab GTPases, of lower eukaryotes. Because of their high divergence from the existing three isoforms, A, B, and C of the Rab5-family, we suggest that Mimiviridae Rabs constitute a new isoform, Rab5D. Phylogenetic analysis indicated probable horizontal acquisition from a lower eukaryotic ancestor followed by selection and divergence. Furthermore, interaction network analysis suggests that vps34 (a Class III PI3K homolog, coded by APMV L615), Atg-8 and dynamin (host proteins) are recruited by APMV Rab GTPase during capsid assembly. Based on these observations, we hypothesize that APMV Rab plays a role in the acquisition of inner membrane during virion assembly.
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    • "Electron microscopic studies led to the detailed description of the intracellular development of these extraordinary endocytobionts during the proliferative phase (Scheid et al. 2010). Pore-like structures of the spore-like particles could be demonstrated which were similar to structures (portal, tunnel) found in the Mimiviruses (Zaubermann et al. 2008). Another observation concerned the amoebic nucleus: This nucleus seemed to disappear during the developmental processes of the endocytobionts within the trophozoites (Scheid et al. 2010). "
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    ABSTRACT: In this article, the results of a long effort to derive valuable phylogenetic data about an extraordinary spore-like infectious particle (endocytobiont) within host amoebae (Acanthamoeba sp.) recently isolated from the contact lens and the inflamed eye of a patient with keratitis are presented. The development of these endocytobionts has already been demonstrated with electron microscopic photo sequences, leading to a relevant model of its development presented here. The molecular biological investigation following the discovery of two other Pandoravirus species within aquatic sediments in 2013 led to the taxonomic affiliation of our endocytobiont with the genus Pandoravirus. A range of endocytobionts (intracellular biofilms) have been found in recent years, among which are several viruses which obligatorily proliferate within free-living amoebae. In human medicine, foreign objects which are placed in or on humans cause problems with microorganisms in biofilms. Contact lenses are especially important, because they are known as a source of a rapid formation of biofilm. These were the first Pandoraviruses described, and because this is additionally the first documented association with humans, we have clearly demonstrated how easily such (viral) endocytobionts can be transferred to humans. This case counts as an example of parasites acting as vectors of phylogenetically different microorganisms especially when living sympatric within their biocoenosis of biofilms. As the third part of the "Pandoravirus trilogy", it finally reveals the phylogenetic nature of these "extraordinary endocytobionts" within Acanthamoebae.
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    • "APMV has a pseudo-icosahedral symmetry, with a complex pentagonal face region named stargate [60,63]. This stargate form is a star-shaped projection from which the viral genome is released, and it can be important during early stages of the viral replication cycle [60,61,63,64] (Figure 2). "
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    ABSTRACT: In 2003, Acanthamoeba polyphaga mimivirus (APMV) was first described and began to impact researchers around the world, due to its structural and genetic complexity. This virus founded the family Mimiviridae. In recent years, several new giant viruses have been isolated from different environments and specimens. Giant virus research is in its initial phase and information that may arise in the coming years may change current conceptions of life, diversity and evolution. Thus, this review aims to condense the studies conducted so far about the features and peculiarities of APMV, from its discovery to its clinical relevance.
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