Archaeal protein kinases and protein phosphatases: insights from genomics and biochemistry

Abstract

Protein phosphorylation/dephosphorylation has long been considered a recent addition to Nature's regulatory arsenal. Early studies indicated that this molecular regulatory mechanism existed only in higher eukaryotes, suggesting that protein phosphorylation/dephosphorylation had emerged to meet the particular signal-transduction requirements of multicellular organisms. Although it has since become apparent that simple eukaryotes and even bacteria are sites of protein phosphorylation/dephosphorylation, the perception widely persists that this molecular regulatory mechanism emerged late in evolution, i.e. after the divergence of the contemporary phylogenetic domains. Only highly developed cells, it was reasoned, could afford the high 'overhead' costs inherent in the acquisition of dedicated protein kinases and protein phosphatases. The advent of genome sequencing has provided an opportunity to exploit Nature's phylogenetic diversity as a vehicle for critically examining this hypothesis. In tracing the origins and evolution of protein phosphorylation/dephosphorylation, the members of the Archaea, the so-called 'third domain of life', will play a critical role. Whereas several studies have demonstrated that archaeal proteins are subject to modification by covalent phosphorylation, relatively little is known concerning the identities of the proteins affected, the impact on their functional properties, or the enzymes that catalyse these events. However, examination of several archaeal genomes has revealed the widespread presence of several ostensibly 'eukaryotic' and 'bacterial' protein kinase and protein phosphatase paradigms. Similar findings of 'phylogenetic trespass' in members of the Eucarya (eukaryotes) and the Bacteria suggest that this versatile molecular regulatory mechanism emerged at an unexpectedly early point in development of 'life as we know it'.

Posttranslational Protein Modification inArchaea

“…Shortly thereafter, in 1980, the presence of phosphorylated proteins in Halobacterium salinarum was reported (413), confirming that Archaea too are ca- (214,215,253).…”

“…However, in contrast to N-glycosylation and, in most cases, lipid modification, covalent modification of proteins by phosphorylation is a reversible event. This property, combined with the major perturbation in protein structure that results from phosphorylation (189), has made this versatile form of posttranslational modification widely used when rapid and profound changes in protein behavior are called for (214,215). As such, protein phosphorylation and dephosphorylation are most commonly exploited by the cell in adaptive pathways designed to present appropriate responses to various cues associated with a multitude of external and internal stimuli (173).…”

Carbohydrate Metabolism in Archaea: Current Insights into Unusual Enzymes and Pathways and Their Regulation

“…There is increasing evidence that posttranscriptional regulation as well as posttranslational modifications (PTMs), e.g., lipid modification, protein glycosylation, methylation, phosphorylation, acetylation, and ubiquitination, also play a significant role within the Archaea (for a recent review, see reference 424). Among this great variety of PTMs, reversible protein phosphorylation/dephosphorylation has an important function in signal transduction and allows a rapid cellular response to diverse external and internal signals (425). Protein phosphorylation is well established in Archaea.…”

Innovation in gene regulation: The case of chromatin computation

“…Nevertheless, genomes contain fewer phosphatases than kinases (in Eukarya by a factor of 10, Fig. 1) [85,86]. This suggests that a highly specific phosphorylation machinery might be counteracted by a fairly general dephosphorylation machinery.…”