The Virosphere’s Own Trojan Horse

Melissa Walker wrote this post as a part of Dr. Stacy Krueger-Hadfield’s Science Communication course at the University of Alabama at Birmingham. Melissa’s research focuses on the interactions between freshwater biofilms and the viruses that infect them. She is currently developing protocols for harvesting host-phage systems from stream biofilms in order to better understand the role of both lytic and lysogenic phages in the development and persistence of these important communities. Melissa completed a B.S. in Botany at the University of Hawaii at Manoa. Her career goals focus on bridging the gap between translational medicine and basic science research through novel approaches to and innovative applications of phage-host systems.

Were you ever required to read Homer’s The Iliad?

No need to break it out if you did (or didn’t). The Achaeans ended a 10-year long siege against the Trojans by placing a large hollow wooden gift horse at the city gates under the façade of concession. Meanwhile, their entire army hid inside, creeping out after the evening festivities to slaughter the Trojans in their beds.

The viral ecosphere (also known as the virosphere) presents this same Greek tragedy every single day, an ecological Trojan War.

Today’s Achaeans, recently discovered giant viruses, are classified with the nucleocytoplasmic large DNA viruses. These warriors are the largest identified to date, with linear double-stranded genomes ranging in size from 100 kbp to 2.5 Mbp (Gallot-Lavallée & Blanc, 2017). 

These amoebic predators disguise themselves as Trojan Horses, hiding a slew of genes inside which are switched into actions once the virus has been phagocytized (Oliveira, La Scola, & Abrahão, 2019).

Giant viruses even have their own version of Achilles, known as Tupanvirus (Fig. 1, Fig. 2), which is capable of multiple amazing feats.

Fig 1. Acanthamoeba castellanii surrounds and engulfs Tupanviruses. These giant viruses infect the amoeba’s trophozite life stage and can prevent the amoeba from encysting, an antiviral defense strategy which transitions the amoeba into its second life stage, a cyst stage, which is immune to Tupanvirus infection.
© Meletios Verras
Fig 2. Tupanviruses – the blue viruses that under TEM resemble the Starship Enterprise. © Jônatas Abrahão

To start, Tupanvirus has the largest tail in the known virosphere (see inset), an enormous cylindrical structure ~ 550 nm in length and a whopping 450 nm in diameter (Abrahão et al., 2018). The entire virus can be anywhere from 1.2 to 2.3 mm in size (Oliveira, Silva, et al., 2019).

Tupanvirus also infects multiple hosts, a phenomenon uncommon in eukaryotic infectors (Oliveira, La Scola, et al., 2019

In addition, Tupanvirus’s own genome is ~1,5 Mb and codes for than 1250 genes, including up to 70 tRNAs, 20 aminoacyl tRNA synthetases, 11 translation initiation factors as well as additional factors related to tRNA/mRNA maturation and stabilization. This means that Tupanviruses have the most complete translation apparatus of any virus identified to date (Abrahão et al., 2018).

Finally, Tupanvirus is capable of zombie-fying their game! 

Shortly after initial infection, the virus causes a change in amoebal morphology and the cells become rounded (Fig. 3; Oliveira, Silva, et al., 2019). 

Fig 3. An SEM of aggregation and interaction between infected and uninfected A. castellanii cells. The white arrows indicate infected cells while the asterisks indicate uninfected cells. Oliveira et al. 2019

Additionally, there is upregulation of both viral and cellular genes expressing a mannose-binding protein (MBP). The increased presence of MBP correlates with the cellular aggregation of both infected (zombified) and uninfected cells. These bunches are a potential virulence strategy to ensure new host cells are available for the virions being packaged inside the infected cell (Fig. 3; Oliveira, Silva, et al., 2019).

The next time you’re in the mood for deceit and betrayal, with a side of zombies, just grab the closest copy of your Molecular Ecologist. There’s bound to be a good story in there.

References

Abrahão, J., Silva, L., Silva, L. S., Khalil, J. Y. B., Rodrigues, R., Arantes, T., . . . La Scola, B. (2018). Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere. Nature Communications, 9(1), 749. doi:10.1038/s41467-018-03168-1

Gallot-Lavallée, L., & Blanc, G. (2017). A Glimpse of Nucleo-Cytoplasmic Large DNA Virus Biodiversity through the Eukaryotic Genomics Window. Viruses, 9(1), 17. doi:10.3390/v9010017

Oliveira, G., La Scola, B., & Abrahão, J. (2019). Giant virus vs amoeba: fight for supremacy. Virology Journal, 16(1), 126. doi:10.1186/s12985-019-1244-3

Oliveira, G., Silva, L., Leão, T., Mougari, S., Da Fonseca, F. G., Geessien Kroon, E., . . . Abrahão, J. S. (2019). Tupanvirus-infected amoebas are induced to aggregate with uninfected cells promoting viral dissemination. Scientific Reports, 9(1), 1-11. doi:10.1038/s41598-018-36552-4

About Stacy Krueger-Hadfield

I am a marine evolutionary ecologist interested in the impacts of seascapes and complex life cycles on marine population dynamics. I use natural history, manipulative field experiments and population genetic and genomic approaches with algal and invertebrate models in temperate rocky shores,estuaries and the open ocean.
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