Viral information

Abstract

Viruses are major drivers of global biogeochemistry and the etiological agents of many diseases. They are also the winners in the game of life: there are more viruses on the planet than cellular organisms and they encode most of the genetic diversity on the planet. In fact, it is reasonable to view life as a viral incubator. Nevertheless, most ecological and evolutionary theories were developed, and continue to be developed, without considering the virosphere. This means these theories need to be to reinterpreted in light of viral knowledge or we need to develop new theory from the viral point-of-view. Here we briefly introduce our viral planet and then address a major outstanding question in biology: why is most of life viral? A key insight is that during an infection cycle the original virus is completely broken down and only the associated information is passed on to the next generation. This is different for cellular organisms, which must pass on some physical part of themselves from generation to generation. Based on this premise, it is proposed that the thermodynamic consequences of physical information (e.g., Landauer's principle) are observed in natural viral populations. This link between physical and genetic information is then used to develop the Viral Information Hypothesis, which states that genetic information replicates itself to the detriment of system energy efficiency (i.e., is viral in nature). Finally, we show how viral information can be tested, and illustrate how this novel view can explain existing ecological and evolutionary theories from more fundamental principles.

Keywords: Ecology; Evolution; Information; Phage; Virus.

Fig. 1

Examples of the main types of viruses: tailed phage that infect bacteria, filamentous viruses that infect all domains of life, and enveloped viruses that infect animal and plant cells. There are actually hundreds of variants on these basic themes and interested readers should look at the International Committee on Viral Taxonomy (ICTV) website and/or Viral Taxonomy books. Of particular interest are the numerous novel virions associated with Archaea viruses

Fig. 2

Illustration of Maxwell’s Demon and Landauer’s principle. The Demon/enzyme selectively picks “A” molecules with sufficient energy to react with reactant “B”, which leads to product “AB”. This process slightly cools the “A” population. This loss of heat is put back into the system by the surrounding Universe. During degradation/erasure of “AB”, “A” goes back into its population and this heat can be measured using methods like isothermal calorimetry

Fig. 3

From gravity to viral information: dust to phage. a Schematic of how gravity leads to viral information. b Schematic of how viruses shape ecology (1-3) and evolution (3), leading to diversification and an increase of viral information (4)

Fig. 4

Searching for viral information. The line indicates where the amount of physical information and genetic information contained within cells are equal. Communities above the line contain more physical than genetic information due to low genetic diversity (few species but many individuals), with each individual requiring a certain amount of energy regardless of its genetic composition. Communities below the line contain more genetic information. It is here that the energetic cost of information becomes apparent, and where we expect to find viral information

Fig. 5

The Landauer limit and mutations. A mutation in a DNA population creates at least 2 bits of Physical Information. It costs an extra 3–6 × 10⁻²¹ J to erase the “B” population