On the origin of cells and viruses: primordial virus world scenario

Abstract

It is proposed that the precellular stage of biological evolution unraveled within networks of inorganic compartments that harbored a diverse mix of virus-like genetic elements. This stage of evolution might makes up the Last Universal Cellular Ancestor (LUCA) that more appropriately could be denoted Last Universal Cellular Ancestral State (LUCAS). Such a scenario recapitulates the ideas of J. B. S. Haldane sketched in his classic 1928 essay. However, unlike in Haldane's day, considerable support for this scenario exits today: lack of homology between core DNA replication system components in archaea and bacteria, distinct membrane chemistries and enzymes of lipid biosynthesis in archaea and bacteria, spread of several viral hallmark genes among diverse groups of viruses, and the extant archaeal and bacterial chromosomes appear to be shaped by accretion of diverse, smaller replicons. Under the viral model of precellular evolution, the key components of cells originated as components of virus-like entities. The two surviving types of cellular life forms, archaea and bacteria, might have emerged from the LUCAS independently, along with, probably, numerous forms now extinct.

Figure 1

Genetic complexity and “cellularity” of LUCA(S): the space of logical possibilities. “Cellularity” is the degree of similarity to the organization of modern cells. The notion of “cellularity” is qualitative, there are no specific units. The complexity scale also could be considered arbitrary, but the units of complexity can be assumed to (roughly) represent the number of genes. The primordial virus world model delineated in this article implies the complex, noncellular LUCAS.

Figure 2

Distinct possible organizations of LUCA(S). The dashed line schematically denotes an unspecified form of compartmentalization in the precellular LUCAS.

Figure 3

The primordial virus world model of precellular evolution. Some major stages in precellular evolution are denoted to the right. Thin, waved lines indicate RNA elements, and circles and ovals indicate DNA elements. Hexagons denote virus‐like particles, and those enclosed in rounded rectangles denote membrane‐containing virions. DNA segments replicated by an archaeal‐type replication machinery are shown in red, and those replicated by the bacterial‐type replication system are shown in blue; the two types of membranes are similarly color coded. The archaeal‐type replication system might have antedated the bacterial systems during precellular evolution as argued elsewhere. ¹⁰⁶ Arrows between compartments indicate horizontal transfer of the contents.