Chasing the Origin of Viruses: Capsid-Forming Genes as a Life-Saving Preadaptation within a Community of Early Replicators

Abstract

Virus capsids mediate the transfer of viral genetic information from one cell to another, thus the origin of the first viruses arguably coincides with the origin of the viral capsid. Capsid genes are evolutionarily ancient and their emergence potentially predated even the origin of first free-living cells. But does the origin of the capsid coincide with the origin of viruses, or is it possible that capsid-like functionalities emerged before the appearance of true viral entities? We set to investigate this question by using a computational simulator comprising primitive replicators and replication parasites within a compartment matrix. We observe that systems with no horizontal gene transfer between compartments collapse due to the rapidly emerging replication parasites. However, introduction of capsid-like genes that induce the movement of randomly selected genes from one compartment to another rescues life by providing the non-parasitic replicators a mean to escape their current compartments before the emergence of replication parasites. Capsid-forming genes can mediate the establishment of a stable meta-population where parasites cause only local tragedies but cannot overtake the whole community. The long-term survival of replicators is dependent on the frequency of horizontal transfer events, as systems with either too much or too little genetic exchange are doomed to succumb to replication-parasites. This study provides a possible scenario for explaining the origin of viral capsids before the emergence of genuine viruses: in the absence of other means of horizontal gene transfer between compartments, evolution of capsid-like functionalities may have been necessary for early life to prevail.

Fig 1. Both, too infrequent and too frequent horizontal gene transfer events lead to the collapse of the replication processes within the system.

Intermediate transfer frequency, however, can cope with the presence of replication parasites.

Fig 2. (A) In the developed model, replication of genes can induce mutations.

These genetic changes can: change the type of the gene, render the gene useless (loss-of-function) or turn it into a replication parasite. (B) The model comprises a three dimensional matrix of static compartments in which all the simulated events take place. Horizontal movement within compartment is mediated via spontaneously and/or genetically induced (depending on the setup) forming of vesicles.

Fig 3. In the absence of horizontal gene transfer, the inevitable emergence of replication parasites leads to the tragedy of the commons: selfish replicators utilize all the resources without contributing anything to the system.

Fig 4. (A) Spontaneous horizontal gene transfer events allow replicators to spread within the system before the emergence of replication parasites.

Size of the system was 5x5x5 (125) compartments and the spontaneous horizontal transfer rate was 8.0E-4 for each cell. (B) Simultaneous existence of induced and spontaneous horizontal gene transfer. The cells depict the number of simulations (out of 10) surviving over 100 000 iterations. Blue-cell indicates the conditions depicted in panel A. Other parameter-values are listed in Table 2.

Fig 5. Survival of life over 100 000 simulation cycles depending on (A) the frequency of horizontal transfer events and the probability for the emergence of replication parasites, or (B) the size of the compartments matrix and the size of each compartment within the matrix.

All simulations were run ten times and the average number of simulations surviving over 100 000 cycles is presented. The cell with white borders in (A) has the attribute values used in (B), and vice versa.