Microscopic Analysis of the Tupanvirus Cycle in Vermamoeba vermiformis

Lorena C F Silva,Bernard La Scola,Fabio Pio Dornas,Graziele Pereira Oliveira,Rodrigo Araújo Lima Rodrigues,Jônatas S Abrahão,Erna G Kroon

doi:10.3389/fmicb.2019.00671

Abstract

Since Acanthamoeba polyphaga mimivirus (APMV) was identified in 2003, several other giant viruses of amoebae have been isolated, highlighting the uniqueness of this group. In this context, the tupanviruses were recently isolated from extreme environments in Brazil, presenting virions with an outstanding tailed structure and genomes containing the most complete set of translation genes of the virosphere. Unlike other giant viruses of amoebae, tupanviruses present a broad host range, being able to replicate not only in Acanthamoeba sp. but also in other amoebae, such as Vermamoeba vermiformis, a widespread, free-living organism. Although the Tupanvirus cycle in A. castellanii has been analyzed, there are no studies concerning the replication of tupanviruses in other host cells. Here, we present an in-depth microscopic study of the replication cycle of Tupanvirus in V. vermiformis. Our results reveal that Tupanvirus can enter V. vermiformis and generate new particles with similar morphology to when infecting A. castellanii cells. Tupanvirus establishes a well-delimited electron-dense viral factory in V. vermiformis, surrounded by lamellar structures, which appears different when compared with different A. castellanii cells. Moreover, viral morphogenesis occurs entirely in the host cytoplasm within the viral factory, from where complete particles, including the capsid and tail, are sprouted. Some of these particles have larger tails, which we named “supertupans.” Finally, we observed the formation of defective particles, presenting abnormalities of the tail and/or capsid. Taken together, the data presented here contribute to a better understanding of the biology of tupanviruses in previously unexplored host cells.

Highlights

Since the isolation of Acanthamoeba polyphaga mimivirus (APMV) in the early 2000s, giant viruses have been arousing interest due to their structural, biological, and genomic complexity (La Scola et al, 2003; Colson et al, 2017)
Mimiviruses attracted attention due to the presence of a large, icosahedral capsid associated with fibrils; pandoraviruses, cedratviruses, and pithoviruses show an ovoid morphology, are very large viruses, and have apical pores; in none of these viruses was there any structure resembling that of a tail, which is only found in tupanviruses (La Scola et al, 2003; Philippe et al, 2013; Legendre et al, 2014; Abrahão et al, 2018)
Tupanviruses were isolated from extreme environments in Brazil and showed unprecedented characteristics, including the ability to replicate in different genera of protozoa (Abrahão et al, 2018)

Summary

Introduction

Since the isolation of Acanthamoeba polyphaga mimivirus (APMV) in the early 2000s, giant viruses have been arousing interest due to their structural, biological, and genomic complexity (La Scola et al, 2003; Colson et al, 2017). In 2015, the prospection of giant viruses from 17 samples from soda lakes and oceanic soil sediments collected in Brazil was performed, resulting in the isolation of two new viral isolates, named Tupanvirus soda lake (TPVsl) and Tupanvirus deep ocean, which are able to replicate in amoebae of different genera, such as Acanthamoeba and Vermamoeba, among others (Abrahão et al, 2018). Mimiviruses attracted attention due to the presence of a large, icosahedral capsid associated with fibrils; pandoraviruses, cedratviruses, and pithoviruses show an ovoid morphology, are very large viruses, and have apical pores; in none of these viruses was there any structure resembling that of a tail, which is only found in tupanviruses (La Scola et al, 2003; Philippe et al, 2013; Legendre et al, 2014; Abrahão et al, 2018)

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