Global Patterns of Protein Domain Gain and Loss in Superkingdoms

Abstract

Domains are modules within proteins that can fold and function independently and are evolutionarily conserved. Here we compared the usage and distribution of protein domain families in the free-living proteomes of Archaea, Bacteria and Eukarya and reconstructed species phylogenies while tracing the history of domain emergence and loss in proteomes. We show that both gains and losses of domains occurred frequently during proteome evolution. The rate of domain discovery increased approximately linearly in evolutionary time. Remarkably, gains generally outnumbered losses and the gain-to-loss ratios were much higher in akaryotes compared to eukaryotes. Functional annotations of domain families revealed that both Archaea and Bacteria gained and lost metabolic capabilities during the course of evolution while Eukarya acquired a number of diverse molecular functions including those involved in extracellular processes, immunological mechanisms, and cell regulation. Results also highlighted significant contemporary sharing of informational enzymes between Archaea and Eukarya and metabolic enzymes between Bacteria and Eukarya. Finally, the analysis provided useful insights into the evolution of species. The archaeal superkingdom appeared first in evolution by gradual loss of ancestral domains, bacterial lineages were the first to gain superkingdom-specific domains, and eukaryotes (likely) originated when an expanding proto-eukaryotic stem lineage gained organelles through endosymbiosis of already diversified bacterial lineages. The evolutionary dynamics of domain families in proteomes and the increasing number of domain gains is predicted to redefine the persistence strategies of organisms in superkingdoms, influence the make up of molecular functions, and enhance organismal complexity by the generation of new domain architectures. This dynamics highlights ongoing secondary evolutionary adaptations in akaryotic microbes, especially Archaea.

Arguments Reinforcing the Three-Domain View of Diversified Cellular Life

“…It can also be a conceptual challenge to visualize the effects of protein domain gain, loss, inversions, and rearrangements in concatenation of several genes. These are well-known evolutionary processes influencing the history of molecular sequences [89] and could pose serious issues especially when primary sequence identity between proteins is very low, as could be the case when comparing distantly related taxa over long evolutionary timespans. Simulations have also shown that concatenated gene sets can lead to inconsistencies and produce misleading trees with high BS values [35], in addition to known issues of heterotachy [36].…”

Evolutionary analysis of the global landscape of protein domain types and domain architectures associated with family 14 carbohydrate‐binding modules

“…The phylogenetic distribution of the different domain types as well as of the domain pairs formed by them, showed equally large variations among the extant lineages and taxa (Table S7), which could reflect adaptations to the specific organismal biology. Higher eukaryotes are known to exhibit elevated rates of domain rearrangements and duplications, mainly as a result of their larger genomes and more complex biology [30]. In our dataset, the Arthropoda and Cephalochordata clades exhibited the highest numbers in unique domain types (58 and 25, respectively) and consequently unique domain pairs (98 and 44, respectively) in modular CBM14‐containing proteins.…”

Aerobic Lineage of the Oxidative Stress Response Protein Rubrerythrin Emerged in an Ancient Microaerobic, (Hyper)Thermophilic Environment

“…These low levels and perhaps transitory increments of oxygen could have originated from biotic or abiotic reactions, such as enzymatic ROS-detoxifying reactions or water UV photolysis (Martin and Sousa, 2016). It is probable that during those “oxygen whiffs,” many proteins would be the object of selection pressure to survive in oxygen that could force them to lose or gain new features such as protein domains (Nasir et al, 2014) or physiological activities. In addition, the ancient hot environment of the Archaean eon could helped to accelerate the evolutionary rate of change of these proteins, as postulated to be occurring in current extreme environments (Li et al, 2014).…”