Phylogenetic Tracings of Proteome Size Support the Gradual Accretion of Protein Structural Domains and the Early Origin of Viruses from Primordial Cells

Abstract

Untangling the origin and evolution of viruses remains a challenging proposition. We recently studied the global distribution of protein domain structures in thousands of completely sequenced viral and cellular proteomes with comparative genomics, phylogenomics, and multidimensional scaling methods. A tree of life describing the evolution of proteomes revealed viruses emerging from the base of the tree as a fourth supergroup of life. A tree of domains indicated an early origin of modern viral lineages from ancient cells that co-existed with the cellular ancestors. However, it was recently argued that the rooting of our trees and the basal placement of viruses was artifactually induced by small genome (proteome) size. Here we show that these claims arise from misunderstanding and misinterpretations of cladistic methodology. Trees are reconstructed unrooted, and thus, their topologies cannot be distorted a posteriori by the rooting methodology. Tracing proteome size in trees and multidimensional views of evolutionary relationships as well as tests of leaf stability and exclusion/inclusion of taxa demonstrated that the smallest proteomes were neither attracted toward the root nor caused any topological distortions of the trees. Simulations confirmed that taxa clustering patterns were independent of proteome size and were determined by the presence of known evolutionary relatives in data matrices, highlighting the need for broader taxon sampling in phylogeny reconstruction. Instead, phylogenetic tracings of proteome size revealed a slowdown in innovation of the structural domain vocabulary and four regimes of allometric scaling that reflected a Heaps law. These regimes explained increasing economies of scale in the evolutionary growth and accretion of kernel proteome repertoires of viruses and cellular organisms that resemble growth of human languages with limited vocabulary sizes. Results reconcile dynamic and static views of domain frequency distributions that are consistent with the axiom of spatiotemporal continuity that is tenet of evolutionary thinking.

Giant viruses: spore‐like missing links between Rickettsia and mitochondria?

“…The most comprehensive analysis giving support to the hypothesis that viruses have a monophyletic cellular origin comes from deep phylogenetic reconstructions based on comparisons among protein fold families, [13][14][15] which are not confounded by artifacts due to phylogenetic reconstruction methods. 16,17 Such parsimony-based analyses reconstruct very ancient phylogeny from shared structures 18 and/or functions. [19][20][21][22][23] Shared synteny to evaluate evolutionary relatedness This method using the presence/absence of shared structures is a viable alternative to the otherwise doi: 10.1111/nyas.14022 powerful alignment−homology methodology most phyletic reconstructions use nowadays.…”

“…The most comprehensive analysis giving support to the hypothesis that viruses have a monophyletic cellular origin comes from deep phylogenetic reconstructions based on comparisons among protein fold families, which are not confounded by artifacts due to phylogenetic reconstruction methods . Such parsimony‐based analyses reconstruct very ancient phylogeny from shared structures and/or functions …”

That is life: communicating RNA networks from viruses and cells in continuous interaction

“…6,63,64 At least with the discovery of mimiviruses (and other giant viruses), it might be plausible that giant viruses have cellular origins. [65][66][67][68][69][70] We must constantly remember that viruses and subviral infectious genetic parasites are the most abundant biological agents on the planet. 71,72 They outnumber cellular life forms by 10 times, invade all cellular organisms, and serve as key agents in the generation of adaptive and innate immune systems, which are essential for the survival of cellular life forms since they are key for the capacity for self/nonself-differentiation.…”

Education for Sustainability: Lessons from Living Systems Governance

“…These power laws are evidenced whatever the kind of metabolism. A power law of exponent 2/3 is representative of the simultaneous governance of nitrogen and phosphorus concentrations which are limiting factors of proteins and DNA metabolism [60] and of matter growth and energy availability in plant cells [51].…”