Archaic chaos: intrinsically disordered proteins in Archaea

Abstract

BackgroundMany proteins or their regions known as intrinsically disordered proteins (IDPs) and intrinsically disordered regions (IDRs) lack unique 3D structure in their native states under physiological conditions yet fulfill key biological functions. Earlier bioinformatics studies showed that IDPs and IDRs are highly abundant in different proteomes and carry out mostly regulatory functions related to molecular recognition and signal transduction. Archaea belong to an intriguing domain of life whose members, being microbes, are characterized by a unique mosaic-like combination of bacterial and eukaryotic properties and include inhabitants of some of the most extreme environments on the planet. With the expansion of the archaea genome data (more than fifty archaea species from five different phyla are known now), and with recent improvements in the accuracy of intrinsic disorder prediction, it is time to re-examine the abundance of IDPs and IDRs in the archaea domain.ResultsThe abundance of IDPs and IDRs in 53 archaea species is analyzed. The amino acid composition profiles of these species are generally quite different from each other. The disordered content is highly species-dependent. Thermoproteales proteomes have 14% of disordered residues, while in Halobacteria, this value increases to 34%. In proteomes of these two phyla, proteins containing long disordered regions account for 12% and 46%, whereas 4% and 26% their proteins are wholly disordered. These three measures of disorder content are linearly correlated with each other at the genome level. There is a weak correlation between the environmental factors (such as salinity, pH and temperature of the habitats) and the abundance of intrinsic disorder in Archaea, with various environmental factors possessing different disorder-promoting strengths. Harsh environmental conditions, especially those combining several hostile factors, clearly favor increased disorder content. Intrinsic disorder is highly abundant in functional Pfam domains of the archaea origin. The analysis based on the disordered content and phylogenetic tree indicated diverse evolution of intrinsic disorder among various classes and species of Archaea.ConclusionsArchaea proteins are rich in intrinsic disorder. Some of these IDPs and IDRs likely evolve to help archaea to accommodate to their hostile habitats. Other archaean IDPs and IDRs possess crucial biological functions similar to those of the bacterial and eukaryotic IDPs/IDRs.

Exceptionally abundant exceptions: comprehensive characterization of intrinsic disorder in all domains of life

“…This is motivated by the fact that consensusbased approaches provide improved predictive quality [42]. Our approach is a marked improvement over the previous studies, where only one [24,30,32] or two [28,29] predictors were used to characterize disorder. The putative disorder was used to calculate the disorder content (fraction of disordered residues in a given chain), the number and size of disordered segments and long disordered segments that consist of at least 30 consecutive disordered amino acids, Table 1 Summary of the biological processes, molecular functions, and cellular components, which were annotated based on Gene Ontology (GO), across the four domains of life…”

“…Consistent with previous works [44], we count the disordered segments with at least four consecutive disordered residues. We include such short segments, since they can be predicted with relatively high predictive performance [44] and they were included in some of the similar studies [28,30]. However, we note that our results may include some artifacts, since these short regions were speculated as being less likely to be functionally relevant compared to long disordered regions [24].…”

“…The number of species analyzed in the studies discussed above ranged from a few to a few hundreds. For example, the abundance of IDPs and IDRs in 53 archaean species was recently evaluated [28]. In another recent study, Burra et al analyzed 332 prokaryotic proteomes [29], and in still another recent work (which, to the best of our knowledge, is the largest scale intrinsic disorder analysis undertaken so far), the proteomes of 3,484 species were analyzed [30].…”

“…This (revolutionary) change in the understanding of the molecular bases of protein functions was fueled by growing appreciation of the idea that IDPs and IDRs are not rare and obscure exceptions, but are exceptionally common and fascinating entities. In fact, several efforts were devoted to estimating the abundance of intrinsically disordered proteins in nature [23][24][25][26][27][28][29][30][31]. In these studies, predictive algorithms were used to estimate the content of intrinsic disorder in various proteomes or specific protein.…”

Paradoxes and wonders of intrinsic disorder: Stability of instability

“…42,[44][45][46] On the other hand, the role of disorder in adaptation to the environment can be illustrated by the fact that the salt, pH, and/or temperature-tolerant bacteria and Achaea typically contain more IDPs than their mesophilic and salt/pH-sensitive counterparts. 31,47 Many aspects related to the structure, conformational behavior and functionality of IDPs look rather strange from the viewpoint of "traditional" ordered proteins. 48,49 To give a brief outlook of various paradoxes and wonders of intrinsic disorder, a series of short comments on different unusual features of IDPs was started in the Intrinsically Disordered Proteins journal.…”