Whether mammal–microbiome interactions are persistent and specific over evolutionary time is controversial. Here we show that host phylogeny and major dietary shifts have affected the distribution of different gut bacterial lineages and did so on vastly different bacterial phylogenetic resolutions. Diet mostly influences the acquisition of ancient and large microbial lineages. Conversely, correlation with host phylogeny is mostly seen among more recently diverged bacterial lineages, consistent with processes operating at similar timescales to host evolution. Considering microbiomes at appropriate phylogenetic scales allows us to model their evolution along the mammalian tree and to infer ancient diets from the predicted microbiomes of mammalian ancestors. Phylogenetic analyses support co-speciation as having a significant role in the evolution of mammalian gut microbiome compositions. Highly co-speciating bacterial genera are also associated with immune diseases in humans, laying a path for future studies that probe these co-speciating bacteria for signs of co-evolution.
Phylosymbiosis is a pattern defined as the tendency of closely related species to host microbiota whose compositions resemble each other more than host species drawn at random from the same tree. Understanding the mechanisms behind phylosymbiosis is important because it can shed light on rules governing the assembly of host-associated microbiotas and, potentially, their coevolutionary dynamics with hosts. For example, is phylosymbiosis a result of coevolution, or can it be generated by simple ecological filtering processes? Beyond qualitative theoretical models, quantitative theoretical expectations can provide new insights. For example, deviations from a simple baseline of ecological filtering may be used to test more-complex hypotheses (e.g., coevolution). Here, we use simulations to provide evidence that simple host-related ecological filtering can readily generate phylosymbiosis, and we contrast these predictions with real-world data. We find that while phylosymbiosis is widespread in nature, phylosymbiosis patterns are compatible with a simple ecological model in the majority of taxa. Internal compartments of hosts, such as the animal gut, often display stronger phylosymbiosis than expected from a purely ecological filtering process, suggesting that other mechanisms are also involved.
Efficient algorithms and programs for the analysis of the ever-growing amount of biological sequence data are strongly needed in the genomics era. The pace at which new data and methodologies are generated calls for the use of pre-existing, optimized-yet extensible-code, typically distributed as libraries or packages. This motivated the Bio++ project, aiming at developing a set of C++ libraries for sequence analysis, phylogenetics, population genetics, and molecular evolution. The main attractiveness of Bio++ is the extensibility and reusability of its components through its object-oriented design, without compromising the computer-efficiency of the underlying methods. We present here the second major release of the libraries, which provides an extended set of classes and methods. These extensions notably provide built-in access to sequence databases and new data structures for handling and manipulating sequences from the omics era, such as multiple genome alignments and sequencing reads libraries. More complex models of sequence evolution, such as mixture models and generic n-tuples alphabets, are also included.
Highlights d Thousands of gut bacterial genomes from worldwide human populations were sequenced d HGT occurs at high frequency in the gut microbiome of individual persons d HGT occurs more frequently in the microbiome of industrialized and urban populations d Transferred gene functions in the microbiome reflect the lifestyle of the host
During the last decades, describing, analysing and understanding the phylogenetic structure of species assemblages has been a central theme in both community ecology and macro-ecology. Among the wide variety of phylogenetic structure metrics, three have been predominant in the literature: Faith's phylogenetic diversity (PD), which represents the sum of the branch lengths of the phylogenetic tree linking all species of a particular assemblage, the mean pairwise distance between all species in an assemblage (MPD) and the pairwise distance between the closest relatives in an assemblage (MNTD). Comparisons between studies using one or several of these metrics are difficult because there has been no comprehensive evaluation of the phylogenetic properties each metric captures. In particular it is unknown how PD relates to MDP and MNTD. Consequently, it is possible that apparently opposing patterns in different studies might simply reflect differences in metric properties. Here, we aim to fill this gap by comparing these metrics using simulations and empirical data. We first used simulation experiments to test the influence of community structure and size on the mismatch between metrics whilst varying the shape and size of the phylogenetic tree of the species pool. Second we investigated the mismatch between metrics for two empirical datasets (gut microbes and global carnivoran assemblages). We show that MNTD and PD provide similar information on phylogenetic structure, and respond similarly to variation in species richness and assemblage structure. However, MPD demonstrate a very different behaviour, and is highly sensitive to deep branching structure. We suggest that by combining complementary metrics that are sensitive to processes operating at different phylogenetic depths (i.e. MPD and MNTD or PD) we can obtain a better understanding of assemblage structure.
Mammalian gut microbiomes profoundly influence host fitness, but the processes that drive the evolution of host-microbiome systems are poorly understood. Recent studies suggest that mammals and their individual gut symbionts can have parallel evolutionary histories, as represented by their congruent phylogenies. These ''co-phylogenetic'' patterns are signatures of ancient co-speciation events and illustrate the cohesiveness of the mammalian host-gut microbiome entity over evolutionary times. Theory predicts that co-speciation between mammals and their gut symbionts could result from their co-evolution. However, there is only limited evidence of such co-evolution. Here, we propose a model that explains cophylogenetic patterns without relying on co-evolution. Specifically, we suggest that individual gut bacteria are likely to diverge in patterns recapitulating host phylogeny when hosts undergo allopatric speciation, limiting inter-host bacterial dispersal and genomic recombination. We provide evidence that the model is empirically grounded and propose a series of observational and experimental approaches to test its validity. ll
Methods to infer the ancestral conditions of life are commonly based on geological and paleontological analyses. Recently, several studies used genome sequences to gain information about past ecological conditions taking advantage of the property that the G+C and amino acid contents of bacterial and archaeal ribosomal DNA genes and proteins, respectively, are strongly influenced by the environmental temperature. The adaptation to optimal growth temperature (OGT) since the Last Universal Common Ancestor (LUCA) over the universal tree of life was examined, and it was concluded that LUCA was likely to have been a mesophilic organism and that a parallel adaptation to high temperature occurred independently along the two lineages leading to the ancestors of Bacteria on one side and of Archaea and Eukarya on the other side. Here, we focus on Archaea to gain a precise view of the adaptation to OGT over time in this domain. It has been often proposed on the basis of indirect evidence that the last archaeal common ancestor was a hyperthermophilic organism. Moreover, many results showed the influence of environmental temperature on the evolutionary dynamics of archaeal genomes: Thermophilic organisms generally display lower evolutionary rates than mesophiles. However, to our knowledge, no study tried to explain the differences of evolutionary rates for the entire archaeal domain and to investigate the evolution of substitution rates over time. A comprehensive archaeal phylogeny and a non homogeneous model of the molecular evolutionary process allowed us to estimate ancestral base and amino acid compositions and OGTs at each internal node of the archaeal phylogenetic tree. The last archaeal common ancestor is predicted to have been hyperthermophilic and adaptations to cooler environments can be observed for extant mesophilic species. Furthermore, mesophilic species present both long branches and high variation of nucleotide and amino acid compositions since the last archaeal common ancestor. The increase of substitution rates observed in mesophilic lineages along all their branches can be interpreted as an ongoing adaptation to colder temperatures and to new metabolisms. We conclude that environmental temperature is a major factor that governs evolutionary rates in Archaea.
The resurrection of ancestral proteins provides direct insight into how natural selection has shaped proteins found in nature. By tracing substitutions along a gene phylogeny, ancestral proteins can be reconstructed in silico and subsequently synthesized in vitro. This elegant strategy reveals the complex mechanisms responsible for the evolution of protein functions and structures. However, to date, all protein resurrection studies have used simplistic approaches for ancestral sequence reconstruction (ASR), including the assumption that a single sequence alignment alone is sufficient to accurately reconstruct the history of the gene family. The impact of such shortcuts on conclusions about ancestral functions has not been investigated. Here, we show with simulations that utilizing information on species history using a model that accounts for the duplication, horizontal transfer, and loss (DTL) of genes statistically increases ASR accuracy. This underscores the importance of the tree topology in the inference of putative ancestors. We validate our in silico predictions using in vitro resurrection of the LeuB enzyme for the ancestor of the Firmicutes, a major and ancient bacterial phylum. With this particular protein, our experimental results demonstrate that information on the species phylogeny results in a biochemically more realistic and kinetically more stable ancestral protein. Additional resurrection experiments with different proteins are necessary to statistically quantify the impact of using species tree-aware gene trees on ancestral protein phenotypes. Nonetheless, our results suggest the need for incorporating both sequence and DTL information in future studies of protein resurrections to accurately define the genotype–phenotype space in which proteins diversify.
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