The evolution of compositionally and functionally distinct actin filaments

Abstract

The actin filament is astonishingly well conserved across a diverse set of eukaryotic species. It has essentially remained unchanged in the billion years that separate yeast, Arabidopsis and man. In contrast, bacterial actin-like proteins have diverged to the extreme, and many of them are not readily identified from sequence-based homology searches. Here, we present phylogenetic analyses that point to an evolutionary drive to diversify actin filament composition across kingdoms. Bacteria use a one-filament-one-function system to create distinct filament systems within a single cell. In contrast, eukaryotic actin is a universal force provider in a wide range of processes. In plants, there has been an expansion of the number of closely related actin genes, whereas in fungi and metazoa diversification in tropomyosins has increased the compositional variety in actin filament systems. Both mechanisms dictate the subset of actin-binding proteins that interact with each filament type, leading to specialization in function. In this Hypothesis, we thus propose that different mechanisms were selected in bacteria, plants and metazoa, which achieved actin filament compositional variation leading to the expansion of their functional diversity.

The ring of life hypothesis for eukaryote origins is supported by multiple kinds of data

“…By contrast, while the Crenarchaeota do not have an FtsZ equivalent, the crenarchaeotal protein crenactin, is related to eukaryotic actin or 'actin-related proteins' and is absent from Euryarchaeota [59]. Actins are structural proteins, often having such diverse functions as providing cell structural support and, in animals, facilitating muscle contraction, for instance [62]. Most recently, it has been shown that a newly discovered group of Archaebacteria-the 'Lokiarchaeota'-possess an actin variant that is the most closely related prokaryotic actin to eukaryotic actins.…”

Plant Actin-Depolymerizing Factors Possess Opposing Biochemical Properties Arising from Key Amino Acid Changes throughout Evolution

“…Eukaryotic cells have a highly ordered and dynamic actin architecture that is accurately and directly regulated by numerous actin binding proteins (ABPs) with different functions (Staiger, 2000;Staiger and Blanchoin, 2006;Fu, 2015). Thus, it has been proposed that the evolution of actin was accompanied by the formation of particular ABPs Gunning et al, 2015).…”

Novel actin filaments from Bacillus thuringiensis form nanotubules for plasmid DNA segregation

“…S11). The ATP binding site, which is preserved between all actin-like proteins, acts as an ATP hydrolysis and phosphate release controlled conformational switch that is activated by polymerization (21). The ATP switch acts as a timing mechanism to coordinate polymerization and depolymerization (Fig.…”