Phylogenetic Analyses of Sites in Different Protein Structural Environments Result in Distinct Placements of the Metazoan Root

Abstract

Phylogenomics, the use of large datasets to examine phylogeny, has revolutionized the study of evolutionary relationships. However, genome-scale data have not been able to resolve all relationships in the tree of life; this could reflect, at least in part, the poor-fit of the models used to analyze heterogeneous datasets. Some of the heterogeneity may reflect the different patterns of selection on proteins based on their structures. To test that hypothesis, we developed a pipeline to divide phylogenomic protein datasets into subsets based on secondary structure and relative solvent accessibility. We then tested whether amino acids in different structural environments had distinct signals for the topology of the deepest branches in the metazoan tree. We focused on a dataset that appeared to have a mixture of signals and we found that the most striking difference in phylogenetic signal reflected relative solvent accessibility. Analyses of exposed sites (residues located on the surface of proteins) yielded a tree that placed ctenophores sister to all other animals whereas sites buried inside proteins yielded a tree with a sponge+ctenophore clade. These differences in phylogenetic signal were not ameliorated when we conducted analyses using a set of maximum-likelihood profile mixture models. These models are very similar to the Bayesian CAT model, which has been used in many analyses of deep metazoan phylogeny. In contrast, analyses conducted after recoding amino acids to limit the impact of deviations from compositional stationarity increased the congruence in the estimates of phylogeny for exposed and buried sites; after recoding amino acid trees estimated using the exposed and buried site both supported placement of ctenophores sister to all other animals. Although the central conclusion of our analyses is that sites in different structural environments yield distinct trees when analyzed using models of protein evolution, our amino acid recoding analyses also have implications for metazoan evolution. Specifically, our results add to the evidence that ctenophores are the sister group of all other animals and they further suggest that the placozoa+cnidaria clade found in some other studies deserves more attention. Taken as a whole, these results provide striking evidence that it is necessary to achieve a better understanding of the constraints due to protein structure to improve phylogenetic estimation.

TheThermosynechococcusgenus: wide environmental distribution, but a highly conserved genomic core

“…Furthermore our analysis is not sensitive to differences in gene regulation or gene copy number. Access to solvents, solubility, active side peptides and differential folding can influence a protein's functionality and therefor may have implications for adaptability or infer evolutionary history (Lesk and Chothia, 1986;Pandey and Braun, 2020). If the orthology approach employed here is correct, the geochemical parameters that are often thought to be important in microbial selection might simply be not as important as we assume them to be in the environment.…”

Protein evolution is structure dependent and non-homogeneous across the tree of life

“…After subdividing the data into exposed and buried residues the data for all proteins were concatenated, resulting in 14 data matrices (one exposed dataset and one buried dataset for the seven datasets in Table 1). There many aspects of protein structure that can be considered in of models of sequence evolution, ranging from the straightforward use of RSA that we considered in the study, to secondary structure [17], [21], [42]- [44], residue-residue interactions [43], to details like amino acid torsion angles [45]. We focused on RSA because that aspect of protein structure has a substantial impact on the rate matrix (see Fig.…”

“…However, selection to maintain protein structure, which has a fundamental role in maintaining protein function, is likely to play a major role in the overall structure of amino acid substitution matrices [19]. The relative solvent accessibility (RSA) of individual amino acids is one of the most important determinants of the patterns of sequence evolution for globular proteins [20], [21]. This suggests it should be possible to subdivide proteins into solvent exposed (high RSA) and buried (low RSA) sites before estimating substitution matrix parameters for various clades.…”

Rho Family of Ras-Like GTPases in Early-Branching Animals

“…One of the most disputed issues concerning the phylogeny of animals is the phylogenetic relationships among non-bilaterian phyla (Porifera, Cnidaria, Ctenophora, and Placozoa) and their relationship with Bilateria [ 65 , 66 ]. Understanding the relationships among phyla and the true topology of the metazoan tree of life is crucial for answering questions concerning the emergence of metazoan characteristics and their evolution during the last 700 million years [ 66 , 67 ]. The traditional view is that sponges are the earliest-branching lineage, while placozoans are a sister group of Eumetazoa ( Figure 3 A) [ 68 ].…”