Viruses in astrobiology

Abstract

Viruses are the most abundant biological entities on Earth, and yet, they have not received enough consideration in astrobiology. Viruses are also extraordinarily diverse, which is evident in the types of relationships they establish with their host, their strategies to store and replicate their genetic information and the enormous diversity of genes they contain. A viral population, especially if it corresponds to a virus with an RNA genome, can contain an array of sequence variants that greatly exceeds what is present in most cell populations. The fact that viruses always need cellular resources to multiply means that they establish very close interactions with cells. Although in the short term these relationships may appear to be negative for life, it is evident that they can be beneficial in the long term. Viruses are one of the most powerful selective pressures that exist, accelerating the evolution of defense mechanisms in the cellular world. They can also exchange genetic material with the host during the infection process, providing organisms with capacities that favor the colonization of new ecological niches or confer an advantage over competitors, just to cite a few examples. In addition, viruses have a relevant participation in the biogeochemical cycles of our planet, contributing to the recycling of the matter necessary for the maintenance of life. Therefore, although viruses have traditionally been excluded from the tree of life, the structure of this tree is largely the result of the interactions that have been established throughout the intertwined history of the cellular and the viral worlds. We do not know how other possible biospheres outside our planet could be, but it is clear that viruses play an essential role in the terrestrial one. Therefore, they must be taken into account both to improve our understanding of life that we know, and to understand other possible lives that might exist in the cosmos.

Keywords: astrobiology; experimental evolution; horizontal gene transfer; origin of life; quasispecies; virosphere; virus biosignatures.

FIGURE 1

Spigelman’s Monster. In this experiment published in 1967, the RNA from phage Qβ (red lines) and the enzyme responsible for its copy (blue pentagons) were incubated in the presence of nucleotides, and subjected to in vitro replication. The products of each polymerization reaction were serially transferred to new tubes. After 75 of these transfers, 83% of the RNA genome was eliminated, which in turn increased the multiplication rate of the RNA population. This seminal paper by Mills et al. (1967) demonstrated that darwinian evolution can occur in a test tube. Similar serial transfers experiments are used in the study of virus evolution.

FIGURE 2

Organization and Diversity of the Virosphere. The vast genetic diversification of viruses is reflected in a variety of viral genome lengths (1.8 Kb–2.5 Mb) and organizations (e.g., circular vs. linear, segmented or not), virion sizes (17 nm–1 μm) and morphologies, host ranges, and in the types of interactions between viruses and their hosts. Here, we represent the six virus realms in the middle circle, as they emerge from an ancestral RNA-recognition motif (RRM) in the center. The roman numbers indicate the nature of the packaged nucleic acid according to the Baltimore classification scheme, where blue numbers represent DNA and red numbers RNA. Non-viral mobile genetic elements (perivirosphere) and the unknown viral sequences (viral dark matter) are included in the background. Some representative virus morphologies from viruses infecting all three domains are depicted with approximate relative sizes and colored according to their host. The available molecular structures were downloaded from RCSB Protein Data Bank and visualized with UCSF ChimeraX. ss, single-stranded; ds, double-stranded; RT, retro-transcriptase.

FIGURE 3

Icosahedral Symmetry Formation and Detection. (A) Left: Cartoon representing the assembly of identical capsid protein subunits (orange) around a nucleic acid (blue). Right: The resulting virion has icosahedral symmetry, as indicated by the overlapping icosahedron (green). The different colors represent the three different positions that the subunits can occupy in this T = 3 structure that corresponds to the plant-infecting RNA virus TBSV (pdb: 2TBV). In this case, a capsid is assembled from 180 copies of the capsid protein. The structural data were downloaded from RCSB Protein Data Bank and visualized with UCSF ChimeraX. (B) Left: Image of an adenovirus particle detected by atomic force microscopy (AFM) [adapted from de Pablo and San Martín (2022)]. Right: X-ray diffraction pattern caused by a mimivirus particle using X-ray free-electron laser (XFEL) [adapted from Ekeberg et al. (2015)].