Precious giants from extreme environments, Brazil
Jônatas Abrahão, on behalf of the co-authors Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere
The paper in Nature Communications is here: http://go.nature.com/2BZlgQW
Brazil is well-known for its remarkable biodiversity and biological richness. A number of biomes remains to be explored under the lens of science, and this exploration must be done as quickly as possible due the degradation of our natural landscapes by anthropogenic activities. Certainly, this is the main motivation of our group to persist in our exploration of giant viruses in Brazilian environments. In this study, we have investigated the presence of giant viruses in two very special locations. The first one is the Pantanal of Nhecolandia, a region that contains the largest and most diversified field of tropical lakes in the world, comprising approximately 12,000 lakes including soda lakes. Soda lakes are environments that conserve and/or mimic ancient life conditions (e.g., an extremely high salinity and pH) and are considered some of the most extreme aquatic environments on Earth. A collection of soda lake samples was taken by my good colleague Ivan Bergier (Embrapa Pantanal) and kindly sent to our laboratory in Belo Horizonte. The second set of samples selected for this study was also special: ocean sediments collected at a depth of 3,000 m, at Campos dos Goytacazes, in the Brazilian Atlantic Ocean. The collection was done by a submarine robot during petroleum prospecting studies by the Petrobras Company, and kindly provided to our group. As the reader can see, this beautiful and exciting adventure began during the selection and collection of the samples.
In the laboratory, the story of tupanvirus discovery started when our PhD candidate Thalita Arantes was seeking giant viruses from the soda lake samples. She noticed that some of the samples were causing the aggregation and lysis of amoebas. At that time, our group had isolated only mimiviruses, and that type of cytopathic effect induced by the soda lake samples intrigued us. I asked Thalita to prepare amoebas infected with that agent for scanning electron microscopy (SEM). Because the virus had not been purified, I was aware that performing SEM could be a stupid idea, but I had no choice, because our transmission electron microscope was not available at that time. Luckily, the first area we observed in the SEM grid revealed tupanvirus soda lake particles, with that long and beautiful tail. The rest of the grid was dirt that contained pieces of amoebas, which reinforced how lucky we were to see the virus particles clearly during our first observation. We named it Tupanvirus as a tribute to the South American Guarani Indigenous tribes, for whom Tupan—or Tupã—(the God of Thunder) is one of the main mythological figures. On the following day, I emailed my dear collaborator Prof. Bernard La Scola (Aix Marseille University). Bernard agreed that tupanvirus could be a new giant virus, and our teams started to work together on this project.
In 2016, Profs. Bernard La Scola and Didier Raoult kindly invited me to stay for one year in Marseille and work on tupanviruses and other projects as an Invited Researcher. On that occasion, Bernard had already welcomed my former PhD, Lorena Silva, into his laboratory as part of a Capes-Cofecub project, a Brazilian-French collaboration programme that Bernard and I had joined in 2015. When I arrived in Marseille, Bernard and Lorena had advanced the tupanvirus research. After re-isolate tupanvirus, they discovered that tupan has an unprecedentedly broad host-range. They also realized that tupanvirus can induce the shutdown of host 18S rRNA. While in Brazil, our team had advanced the characterization of the viral cycle in Acanthamoeba and the virion features by electron microscopy; in Marseille we were working on the genome and proteomics. When we noticed that the tupanvirus genome contained genes encoding 20 putative types of aminoacyl tRNA-synthetases (aaRS), we realized that we had something special on our hands. Later, we found a new tupanvirus strain in deep ocean samples. At the beginning we were suspicious and worried about possible contamination, but genome sequencing revealed that the deep ocean tupanvirus genome is quite different from the soda lake tupanvirus. The laboratory meetings coordinated by Bernard were always exciting and we used to receive many suggestions for new experiments and analyses every week. In this scenario, my family plans to travel and enjoy Europe during the weekends were replaced by full-time hard-work. However, the final result of this journey in the laboratory was great.
A few months later, another PhD candidate from my lab, Ludmila Silva, arrived in Marseille and started work on the intriguing presence, distribution, evolution and expression of the 18S intronic regions found in tupanviruses and other giant viruses. Ludmila also investigated the mechanisms behind the ribosomal shutdown caused by tupanvirus in hosts and non-hosts. The phylogenetic and pangenomic analyses were performed mainly by Prof. Anthony Levasseur and Prof. Philippe Colson, respectively. Due to the dimensions of the work, which encompassed many fields, more experts and students were involved (see the long list of co-authors). A tupanvirus manuscript was born after seven meetings involving senior-researchers coordinated by Didier and Bernard and 26 drafts!
However, just few months after the submission, we received a surprise. A journalist expert on scientific topics emailed us asking our opinion about a paper to be published in Science at that time, describing the discovery of klosneuvirus. This remarkable work described the discovery (by metagenomics) of giant virus genomes harbouring an almost complete set of aaRS. Before reading the paper, I confess that I got concerned about the loss of novelty of the tupanvirus manuscript. However, even compared to klosneuviruses, tupanviruses have a more complete set of translation related-genes, the most resourceful in the known virosphere. Perhaps most importantly, tupanviruses have been isolated, and because of this, we could observe all the remarkable biological features associated with them, including their broad host-range, the expression of the intronic 18S-like regions, the induction of host ribosomal shut-down and particle toxicity. We hope that in the near future klosneuviruses will be isolated and give us more clues about their biological features.
As the reader can see, the discovery and characterization of tupanviruses has been a long, complex and pleasant journey. I am sure that tupanviruses will fuel new debates about the origins and evolution of giant viruses. The structure of the tupanvirus particles is puzzling, especially the tail. The question of which factors could be related to the broad host-range of tupanvirus is also intriguing. Finally, is there any connection between the soda lake and deep ocean environments where the tupanviruses were isolated? In summary, as is usual in the giant virus field, tupanviruses bring more questions than answers.
Thanks for reading our paper.