Data from: Adaptation to environmental temperature is a major determinant of molecular evolutionary rates in Archaea

Methods to infer the ancestral conditions of life are commonly based on geological and palaeontological analyses. Recently, several studies focused on the use of genomes to gain information about past ecological conditions. Several used the property that the G+C and amino-acid contents of bacterial and archaeal rDNA 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+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 optimal growth temperatures 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.

推断生命祖先状态的研究方法通常依托于地质学与古生物学分析手段。近年来，诸多研究转而依托基因组数据获取古生态环境的相关信息。其中多项研究利用了如下特性：细菌与古菌的核糖体DNA（ribosomal DNA, rDNA）基因的G+C碱基含量，以及其编码蛋白质的氨基酸组成，分别显著受环境温度调控。此前针对生命之树（universal tree of life）上自最后共同祖先（Last Universal Common Ancestor, LUCA）以来各类群对最适生长温度（optimal growth temperature, OGT）的适应性演化展开的研究最终得出结论：LUCA大概率为嗜温生物，且在分别通向细菌祖先与古菌+真核生物祖先的两条演化支系中，均独立发生了对高温环境的平行适应性演化事件。本研究聚焦古菌域（Archaea），以期精准解析该类群随演化时间推移对最适生长温度的适应性演化轨迹。此前已有多项基于间接证据的研究提出，最后古菌共同祖先为超嗜热生物。此外，诸多研究结果证实环境温度对古菌基因组的演化动态具有显著调控作用：嗜热古菌的演化速率通常低于嗜温古菌。然而据我们所知，目前尚无研究尝试阐释整个古菌域内演化速率的差异机制，也未探究核苷酸替换速率（substitution rate）随演化时间的动态变化。我们依托一套完备的古菌系统发育树与分子演化过程的非均质模型，估算了古菌系统发育树各内部节点处的祖先碱基组成、氨基酸组成以及最适生长温度。研究预测，最后古菌共同祖先为超嗜热生物，而现存嗜温物种均展现出向低温环境的适应性演化特征。进一步分析显示，自最后古菌共同祖先以来，嗜温物种不仅具有更长的系统发育分支长度，其核苷酸与氨基酸组成的变异程度也显著更高。在所有分支中，嗜温支系所观测到的替换速率提升现象，可被解读为对低温环境与全新代谢方式的持续性适应性演化过程。综上，环境温度是调控古菌域内演化速率的核心驱动因素。