On the origin of mitochondria: a multilayer network approach.

Backgound: The endosymbiotic theory is widely accepted to explain the origin of mitochondria from a bacterial ancestor. While ample evidence supports the intimate connection of Alphaproteobacteria to the mitochondrial ancestor, pinpointing its closest relative within sampled Alphaproteobacteria is still an open evolutionary debate. Many different phylogenetic methods and approaches have been used to answer this challenging question, further compounded by the heterogeneity of sampled taxa, varying evolutionary rates of mitochondrial proteins, and the inherent biases in each method, all factors that can produce phylogenetic artifacts. By harnessing the simplicity and interpretability of protein similarity networks, herein we re-evaluated the origin of mitochondria within an enhanced multilayer framework, which is an extension and improvement of a previously developed method. Methods: We used a dataset of eight proteins found in mitochondria (N = 6 organisms) and bacteria (N = 80 organisms). The sequences were aligned and resulting identity matrices were combined to generate an eight-layer multiplex network. Each layer corresponded to a protein network, where nodes represented organisms and edges were placed following mutual sequence identity. The Multi-Newman-Girvan algorithm was applied to evaluate community structure, and bifurcation events linked to network partition allowed to trace patterns of divergence between studied taxa. Results: In our network-based analysis, we first examined the topology of the 8-layer multiplex when mitochondrial sequences disconnected from the main alphaproteobacterial cluster. The resulting topology lent firm support toward an Alphaproteobacteria-sister placement for mitochondria, reinforcing the hypothesis that mitochondria diverged from the common ancestor of all Alphaproteobacteria. Additionally, we observed that the divergence of Rickettsiales was an early event in the evolutionary history of alphaproteobacterial clades. Conclusion: By leveraging complex networks methods to the challenging question of circumscribing mitochondrial origin, we suggest that the entire Alphaproteobacteria clade is the closest relative to mitochondria (Alphaproteobacterial-sister hypothesis), echoing recent findings based on different datasets and methodologies.

Comparison of complex networks and tree-based methods of phylogenetic analysis and proposal of a bootstrap method.

Complex networks have been successfully applied to the characterization and modeling of complex systems in several distinct areas of Biological Sciences. Nevertheless, their utilization in phylogenetic analysis still needs to be widely tested, using different molecular data sets and taxonomic groups, and, also, by comparing complex networks approach to current methods in phylogenetic analysis. In this work, we compare all the four main methods of phylogenetic analysis (distance, maximum parsimony, maximum likelihood, and Bayesian) with a complex networks method that has been used to provide a phylogenetic classification based on a large number of protein sequences as those related to the chitin metabolic pathway and ATP-synthase subunits. In order to perform a close comparison to these methods, we selected Basidiomycota fungi as the taxonomic group and used a high-quality, manually curated and characterized database of chitin synthase sequences. This enzymatic protein plays a key role in the synthesis of one of the exclusive features of the fungal cell wall: the presence of chitin. The communities (modules) detected by the complex network method corresponded exactly to the groups retrieved by the phylogenetic inference methods. Additionally, we propose a bootstrap method for the complex network approach. The statistical results we have obtained with this method were also close to those obtained using traditional bootstrap methods.

What are the Evolutionary Origins of Mitochondria? A Complex Network Approach.

Mitochondria originated endosymbiotically from an Alphaproteobacteria-like ancestor. However, it is still uncertain which extant group of Alphaproteobacteria is phylogenetically closer to the mitochondrial ancestor. The proposed groups comprise the order Rickettsiales, the family Rhodospirillaceae, and the genus Rickettsia. In this study, we apply a new complex network approach to investigate the evolutionary origins of mitochondria, analyzing protein sequences modules in a critical network obtained through a critical similarity threshold between the studied sequences. The dataset included three ATP synthase subunits (4, 6, and 9) and its alphaproteobacterial homologs (b, a, and c). In all the subunits, the results gave no support to the hypothesis that Rickettsiales are closely related to the mitochondrial ancestor. Our findings support the hypothesis that mitochondria share a common ancestor with a clade containing all Alphaproteobacteria orders, except Rickettsiales.