Prevalent structural disorder carries signature of prokaryotic adaptation to oxic atmosphere

Abstract

Microbes have adopted efficient mechanisms to contend with environmental changes. The emergence of oxygen was a major event that led to an abrupt change in Earth's atmosphere. To adjust with this shift in environmental condition ancient microbes must have undergone several modifications. Although some proteomic and genomic attributes were proposed to facilitate survival of microorganisms in the presence of oxygen, the process of adaptation still remains elusive. Recent studies have focused that intrinsically disordered proteins play crucial roles in adaptation to a wide range of ecological conditions. Therefore, it is likely that disordered proteins could also play indispensable roles in microbial adaptation to the aerobic environment. To test this hypothesis we measured the disorder content of 679 prokaryotes from four oxygen requirement groups. Our result revealed that aerobic proteomes are endowed with the highest protein disorder followed by facultative microbes. Minimal disorder was observed in anaerobic and microaerophilic microbes with no significant difference in their disorder content. Considering all the potential confounding factors that can modulate protein disorder, here we established that the high protein disorder in aerobic microbe is not a by-product of adaptation to any other selective pressure. On the functional level, we found that the high disorder in aerobic proteomes has been utilized for processes that are important for their aerobic lifestyle. Moreover, aerobic proteomes were found to be enriched with disordered binding sites and to contain transcription factors with high disorder propensity. Based on our results, here we proposed that the high protein disorder is an adaptive opportunity for aerobic microbes to fit with the genomic and functional complexities of the aerobic lifestyle.

Keywords: Environmental adaptation; GC content; Optimal temperature; Oxygen; Phylogenetic inertia; Protein intrinsic disorder.