Kelly Joseph B, Carlson David E, Reuter Manuela, Sommershof Annette, Adamec Lubomír, Becks Lutz
Aquatic Ecology and Evolution, Department of Biology, University of Konstanz, Konstanz 78464, Germany.
Institute for Advanced Computational Science, Stony Brook University, Stony Brook, NY 11794, USA.
Mol Biol Evol. 2025 Feb 3;42(2). doi: 10.1093/molbev/msaf030.
The evolution of intracellular endosymbiosis marks a major transition in the biology of the host and endosymbiont. Yet, how adaptation manifests in the genomes of the participants remains relatively understudied. We investigated this question by sequencing the genomes of Tetrahymena utriculariae, a commensal of the aquatic carnivorous bladderwort Utricularia reflexa, and its intracellular algae, Micractinium tetrahymenae. We discovered an expansion in copy number and negative selection in a TLD domain-bearing gene family in the genome of T. utriculariae, identifying it as a candidate for being an adaptive response to oxidative stress resulting from the physiology of its endosymbionts. We found that the M. tetrahymenae genome is larger than those of other Micractinium and Chlorella and contains a greater number of rapidly expanding orthogroups. These were enriched for Gene Ontology terms relevant to the regulation of intracellular signal transduction and cellular responses to stress and stimulus. Single-exon tandem repeats were overrepresented in paralogs belonging to these rapidly expanding orthogroups, which implicates long terminal repeat retrotransposons (LTRs) as potential agents of adaptation. We additionally performed a comparative transcriptomic analysis of M. tetrahymenae in a free-living state and in endosymbiosis with T. utriculariae and discovered that the genes that are differentially expressed were enriched for pathways that evidence shifts in energy generation and storage and in cellular protection strategies. Together, our results elucidate the axes along which the participants must adapt in this young endosymbiosis and highlight evolutionary responses to stress as a shared trend.
细胞内共生的演化标志着宿主和共生体生物学的一个重大转变。然而，适应如何在参与方的基因组中体现仍相对缺乏研究。我们通过对水生食肉狸藻类植物反折狸藻的共生体——梨形四膜虫及其细胞内藻类四膜虫微芒藻的基因组进行测序来研究这个问题。我们发现梨形四膜虫基因组中一个带有TLD结构域的基因家族的拷贝数增加且受到负选择，将其确定为对其共生体生理产生的氧化应激的适应性反应的候选基因。我们发现四膜虫微芒藻的基因组比其他微芒藻属和小球藻属的基因组更大，并且包含更多快速扩张的直系同源群。这些直系同源群在与细胞内信号转导调控以及细胞对压力和刺激的反应相关的基因本体术语中富集。单外显子串联重复在属于这些快速扩张的直系同源群的旁系同源物中过度存在，这表明长末端重复逆转座子（LTRs）是潜在的适应性因子。我们还对处于自由生活状态以及与梨形四膜虫共生状态的四膜虫微芒藻进行了比较转录组分析，发现差异表达的基因在能量产生和储存以及细胞保护策略发生转变的途径中富集。总之，我们的结果阐明了在这种年轻的共生关系中参与方必须适应的轴，并突出了对压力的进化反应作为一个共同趋势。
