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The repertoire of protein architectures in proteomes is evolutionarily conserved and capable of preserving an accurate record of genomic history. Here we use a census of protein architecture in genomes that have been fully sequenced to generate genome-based phylogenies that what do the tips of the branches in a phylogenetic tree represent the evolution of the protein world at fold F and fold superfamily FSF levels.
The patterns of representation of F and FSF architectures over evolutionary history suggest three epochs in the evolution of the protein world: 1 architectural diversification, where members of an architecturally rich ancestral community diversified their protein repertoire; 2 superkingdom specification, where superkingdoms Archaea, Bacteria, and Eukarya were specified; and 3 organismal diversification, where F and FSF specific to relatively small sets of organisms appeared as the result of diversification of organismal lineages.
Functional annotation of FSF along these architectural chronologies revealed patterns of discovery of biological function. Most importantly, the analysis identified an early and extensive differential loss of architectures occurring primarily in Archaea that segregates the archaeal lineage from the ancient community of organisms and establishes the first organismal divide.
Reconstruction of phylogenomic trees of proteomes reflects the timeline of architectural diversification in the emerging lineages. Thus, Archaea undertook a minimalist strategy using only a small subset of the full architectural repertoire and then crystallized into a diversified superkingdom late in evolution. Our analysis also suggests a communal ancestor to all life that was molecularly complex and adopted genomic strategies currently present in Eukarya. The repertoire of protein structures encoded in a genome delimits the cellular functions and interactions that sustain cellular life.
It also serves as an imprint of genomic history. While nucleic acid and protein sequence can be highly dynamic, domain structure in proteins is generally maintained for long periods of evolutionary time Gerstein and Hegyi ; Chothia et al. For this reason, domains are considered not only units of structure but also units of evolution Murzin et al. In fact, there have been very few of these finds in the history of life on earth. F and FSF architectures are highly conserved in nature.
FSF are composed of protein molecules with low sequence identity but with structures and functions indicative of a probable common evolutionary origin they group one or more sequence-related FF. F group FSF with secondary structures that are similarly arranged in 3D space but that may not necessarily be evolutionarily related.
The vast majority of F and FSF represent highly successful architectural discoveries that have accumulated and dispersed throughout the 10 7 —10 8 species that inhabit our planet. Indeed, the occurrence and abundance of F and FSF, and their combination in proteins, has been used successfully to build reasonable universal trees of life capable of describing the history of major organismal lineages satisfactorily Caetano-Anollés and Caetano-Anollés ; Yang et al.
Furthermore, the phylogenetic analysis of the architectural repertoire can dissect deep evolutionary phenomena related to the origins of life Caetano-Anollés and Caetano-Anollés; Dupont et al. In this study, we take advantage of this potential. The ancestor of all organisms alive today is at the root of the universal phylogenetic tree, and its cellular and molecular organization illuminates our understanding on how life originated and evolved Woese ; Penny and Poole However, its nature has been controversial.
This stems from limitations and conflict in the evolutionary signals that are embedded in the limited number of molecular or cellular features that have been analyzed. In contrast, a tracing of the origins of the tripartite world from an ancient RNA world based on DNA sequence, RNA relics, and other marketing pillars examples suggests that the ancestor was eukaryotic-like and complex Poole et al.
Moreover, analysis of entire genomic complements indicated that massive HGT was not warranted e. It also revealed the complexities of phylogenetic reconstruction Delsuc et al. Despite the promises of evolutionary genomics, the nature of the universal ancestor and the universal tree has yet to be resolved Delsuc et al. However, phylogenetic analyses of combined or concatenated genomic sequences e. We recently used a genomic census of protein architecture to generate genome-based phylogenies phylogenomic trees that describe the evolution of the protein world at different hierarchical levels of protein structural organization Caetano-Anollés and Caetano-Anollés; Wang et al.
These trees love hope strength quotes used to classify proteins mostly globulardefine structural transformations, and uncover evolutionary patterns in structure. We also traced patterns of organismal distribution in these trees and found that architectures at the base were omnipresent or common to all superkingdoms and that a timeline of organismal diversification could be inferred Caetano-Anollés and Caetano-Anollés ; Wang et al.
The diversity of ancient architectures common to superkingdoms suggested that the universal ancestor had a complex and relatively modern eukaryotic-like organization and hinted at a prokaryotic world stemming fundamentally from reductive evolutionary processes. In this study, we embark on a systematic and global study of genomes that have been fully sequenced and represent organisms from all three superkingdoms of life that exhibit free-living FLparasitic Pand obligate parasitic OP lifestyles.
We first reconstructed phylogenomic trees of F and FSF using standard phylogenetic methods. The trees uncovered congruent patterns of architectural diversification and reductive evolutionary processes. Finally, we used this information to reconstruct global trees of proteomes and to propose a scenario for the birth and diversification of the tripartite world. The trees were well resolved, but branches were generally poorly supported by bootstrap analysis, an expected outcome with trees of this size.
F and FSF trees grouped architectures into similar clades. This explains the qualitative similarity of results for F and FSF described below. To unfold the data embedded in the trees, we quantified the distribution of F and FSF among proteomes by a distribution index fdefined as the relative number of species using each F or FSF. Figure 1B displays this index f plotted against the relative age of architectures ndmeasured on the trees as a relative distance in nodes from the hypothetical ancestor.
At this point, a large number of architectures were clustered, each specific to a small number of organisms. Further in evolutionary time 0. Architectural chronologies of F folds left and FSF fold superfamilies right suggest three evolutionary epochs in the timeline of the protein world. Venn diagrams show occurrence of architectures in the three superkingdoms of life, Archaea ABacteria Band Eukarya E.
Terminal leaves were not labeled, as they would not be legible. Based on these patterns, we propose three evolutionary epochs of the protein world: light green structural diversification; salmon superkingdom specification; yellow organismal diversification epochs. When these architectural chronologies were dissected for the three superkingdoms Fig. We hypothesize that the probability to lose an existing architecture later in evolution because of lifestyle adaptation is higher than the probability of the other lineages simultaneously discovering the same architecture at the time of its origin.
In general, what do the tips of the branches in a phylogenetic tree represent higher the value of fthe higher is the probability that a few organisms lost an architecture, and the lower the probability that many organisms independently discovered the same architecture at the same time. Six phases in the evolutionary timeline of the protein world based on distribution of F left and FSF right within the three superkingdoms of life.
Trees describe global most-parsimonious scenarios for organismal diversification of proteomes based on architectural distribution patterns. Numbers indicate the size of architectural repertoires in A, B, and E lineages at the corresponding nd values. The horizontal scale is as in B. B Distribution index f of What do the tips of the branches in a phylogenetic tree represent and FSF within the three superkingdoms for gray all organisms or black free living only against the age of the individual architectures.
Light green Structural diversification; salmon superkingdom specification; yellow organismal diversification epochs. Roman numerals indicate the evolutionary phases of the protein world described in the text. Red lines Cumulative loss of BE architectures number what do the tips of the branches in a phylogenetic tree represent architectures absent in each organism, summated over organisms, and integrated over nd ; the ordinate what is a core service agency in logarithmic scale with units not displayed; the abscissa matches nd values.
Further evidence, presented below through the analysis of architectural distribution Fig. Venn diagrams of architectural use show that architectures that are common to all superkingdoms are the most abundant Fig. Loss of ancient architectures was mostly confined to Archaea Fig. Very few F or FSF of ancient origin e. This process becomes very extensive in the region of 0. The sigma 2 domain of RNA polymerase sigma factors a.
A similar trend can be seen in the representation of FSF Fig. The LysM domain d. This significant early differential loss of architectures occurring primarily in Archaea segregates them from the world of ancient organisms, establishing the first organismal divide. Decreases in architectural representation f -value occurred also in Eukarya and Bacteria, but involved fewer and younger architectures.
This process signals the beginning of difference between taxonomy and taxon superkingdom what is fast reading speed epoch, which culminates in the appearance of the first architectures unique to a superkingdom, specifically Bacteria B bar in Fig. Those were the TilS substrate-binding domain F d.
This early start did not alter the general patterns of F and FSF representation but allowed Bacteria to acquire significant structural diversity in the 0. Here the differences between prokaryotes and eukaryotes seem to be defined, both through AB-specific and E-specific architectures Fig. Immediately following appearance of the last AB-specific architecture, the representation strategy in Eukarya undergoes a major revision.
Concurrently, both Bacteria and Archaea maintain the specialization trend of small representation for almost all new F and FSF. To explain the above trends from a functional perspective, we tallied the FSF participating in various cellular functions in every phase of the architectural chronology. Functions were defined using a hierarchical coarse-grained classification encompassing seven functional categories and 50 subcategories Vogel et al. For each phase and category, the fraction f o of FSF used in each superkingdom was calculated Fig.
This index f o indicates what functions drop out of use in each phase and superkingdom: f o what is a dominant allele to 1 indicates that the superkingdom in question completely lost only a few FSF of that function in that phase, whereas f o close to 0 indicates what do the tips of the branches in a phylogenetic tree represent most FSF were lost or not gained. To aid interpretation of this index, we also calculated average f -values f that describe organismal FSF usage for every function, phase, and superkingdom Fig.
When f is close to 1, all organisms in a superkingdom use FSF for that function. When f is close to 0, most organisms fail to use them. Evolution of biological function along the six phases of the architectural chronology. A Bar diagrams describe the fraction of FSF corresponding to each of seven coarse-grained functional categories in each superkingdom what do the tips of the branches in a phylogenetic tree represent to their use in all life within a particular evolutionary phase f oand circles describe how widely distributed these FSF are among organisms within each superkingdom, as average distribution indices f.
When bars and circles are both high or low, the relative importance of that function is either high or low, respectively—the function present in most FSF is important to most organisms in a superkingdom, or the function present in few FSF is only important to a small organismal subset. When bars are high and circles are low or when bars are low and circles are high, function in most FSF is important to small organismal subsets or function in few FSF is important to most organisms, respectively.
B Pie charts describe FSF distribution in functional categories for every phase. The size of each pie chart is proportional to the number of FSF in each phase. Therefore, most functions were discovered during the architectural diversification epoch. What do the tips of the branches in a phylogenetic tree represent, Eukarya seem to be specified earlier than suggested by the architectural chronologies Fig.
In phase VI, Eukarya retain f o bars and f close to 1 and Bacteria diversify all functions tall f o bars with very low f. Based is life a waste of time previous results, we reconstructed trees of proteomes to follow the rise of three organismal superkingdoms in evolution. We excluded organisms leading parasitic lifestyles P and OP from further phylogenomic analysis to increase the reliability of deep branches.
This decision was based does linkedin tell you when you remove a connection the massive loss of architectures in parasitic lifestyles Fig. S1possibly causing homoplastic events frequently observed in phylogenetic trees. We built global trees using three subsets of FSF architectures Fig.
S3 originating what is the definition of impact study different phases of the evolutionary timeline defined above, so as to follow separation of major branches through evolutionary time. The topology of rooted and unrooted trees reconstructed using polarized directed or nonpolarized undirected characters was almost identical in these studies data not shown.
The tree had poor resolution, likely because most architectures used were shared by all superkingdoms, but revealed clearly a monophyletic clade grouping of Eukarya. The younger architectures that appeared before the first bacterial FSF 0.
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