Protein and DNA Modifications: Evolutionary Imprints of Bacterial Biochemical Diversification and Geochemistry on the Provenance of Eukaryotic Epigenetics

Abstract

Epigenetic information, which plays a major role in eukaryotic biology, is transmitted by covalent modifications of nuclear proteins (e.g., histones) and DNA, along with poorly understood processes involving cytoplasmic/secreted proteins and RNAs. The origin of eukaryotes was accompanied by emergence of a highly developed biochemical apparatus for encoding, resetting, and reading covalent epigenetic marks in proteins such as histones and tubulins. The provenance of this apparatus remained unclear until recently. Developments in comparative genomics show that key components of eukaryotic epigenetics emerged as part of the extensive biochemical innovation of secondary metabolism and intergenomic/interorganismal conflict systems in prokaryotes, particularly bacteria. These supplied not only enzymatic components for encoding and removing epigenetic modifications, but also readers of some of these marks. Diversification of these prokaryotic systems and subsequently eukaryotic epigenetics appear to have been considerably influenced by the great oxygenation event in the Earth's history.

Evolution of theD. melanogasterchromatin landscape and its associated proteins

“…In summary, many CAPs appear to have been established early in eukaryotic evolution, as was also reported in (Aravind et al 2014). And the evolution of regulatory proteins may have been especially important during the evolution toward more complex multicellular organisms.…”

“…The chromatin landscape consists of DNA, histones, and other associated proteins and RNAs, and plays a fundamental role in development, cellular memory, and integration of external signals. As a unique feature of the eukaryotic cell, it is closely tied to the evolution of eukaryotes, both regarding their origin and the major transition(s) to multicellularity (Newman 2005;Aravind et al 2014;Gombar et al 2014;Penny et al 2014;Miyamoto et al 2015;Sebé-Pedrós et al 2017). At a basic level, chromatin is responsible for maintenance, organization, and correct use of the genome.…”

“…From an evolutionary point of view, although prokaryotes have specialized proteins associated with their DNA, they do not share homology with eukaryotic CAPs (Luijsterburg et al 2008). In general, evolution of chromatin and diversification of epigenetic mechanisms are suggested to be tightly linked with eukaryotic evolution, from its origin to the transition to multicellularity (Newman 2005;Aravind et al 2014;Gombar et al 2014;Penny et al 2014;Miyamoto et al 2015;Sebé-Pedrós et al 2017). Indeed, the Last Eukaryotic Common Ancestor (LECA) is considered to possess the key components of eukaryotic epigenetics, including most histone modification enzymes and some histone mark readers (Aravind et al 2014).…”

“…In general, evolution of chromatin and diversification of epigenetic mechanisms are suggested to be tightly linked with eukaryotic evolution, from its origin to the transition to multicellularity (Newman 2005;Aravind et al 2014;Gombar et al 2014;Penny et al 2014;Miyamoto et al 2015;Sebé-Pedrós et al 2017). Indeed, the Last Eukaryotic Common Ancestor (LECA) is considered to possess the key components of eukaryotic epigenetics, including most histone modification enzymes and some histone mark readers (Aravind et al 2014). In addition, a current hypothesis on the transition to multicellularity is that complexification of the regulatory genome, via the emergence of repressive chromatin contexts and distal regulatory elements, permitted to generate the cell-type-specific transcriptional programs required for multicellularity (Larroux et al 2006;Mendoza et al 2013;Sebé-Pedrós et al 2016Arenas-Mena 2017;Hinman & Cary 2017).…”

Adenine methylation in eukaryotes: Apprehending the complex evolutionary history and functional potential of an epigenetic modification

“…2). Since eukaryotes typically lack R‐M systems, the acquired N 6 A‐MTases are reused in different functional capacities 88. This is often accompanied by fusions to domains, which on the one hand enable specific interactions with methylated histones/other chromatin proteins 83, 84, DNA 73, or both, and on the other hand facilitate interactions with RNA 59.…”