Nuclear dualism without extensive DNA elimination in the ciliate Loxodes magnus

• 成果类型: Article
• 署名作者: Seah, Brandon K. B.; Singh, Aditi; Vetter, David E.; Emmerich, Christiane; Peters, Moritz; Soltys, Volker; Huettel, Bruno; Swart, Estienne C.
• 署名单位: Max Planck Society; Johann Heinrich von Thunen Institute; Eberhard Karls University of Tubingen; Eberhard Karls University of Tubingen; Max Planck Society
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-11340
• DOI: 10.1073/pnas.2400503121
• 发表日期: 2024-09-24
• 关键词: de-novo identification; paramecium-tetraurelia; macronuclear genome; small rnas; methylation; sequence; rearrangements; reveals; gene; differentiation

摘要

Most eukaryotes have one nucleus and nuclear genome per cell. Ciliates have instead evolved distinct nuclei that coexist in each cell: a silent germline vs. transcriptionally active somatic nuclei. In the best- studied model species, both nuclei can divide asexually, but only germline nuclei undergo meiosis and karyogamy during sex. Thereafter, thousands of DNA segments, called internally eliminated sequences (IESs), are excised from copies of the germline genomes to produce the streamlined somatic genome. In Loxodes, however, somatic nuclei cannot divide but instead develop from germline copies even during asexual cell division, which would incur a huge overhead cost if genome editing was required. Here, we purified and sequenced both genomes in Loxodes magnus to see whether their nondividing somatic nuclei are associated with differences in genome architecture. Unlike in other ciliates studied to date, we did not find canonical germline- limited IESs, implying Loxodes does not extensively edit its genomes. Instead, both genomes appear large and equivalent, replete with retrotransposons and repetitive sequences, unlike the compact, gene- rich somatic genomes of other ciliates. Two other hallmarks of nuclear development in ciliates-domesticated DDE- family transposases and editing- associated small RNAs-were also not found. Thus, among the ciliates, Loxodes genomes most resemble those of conventional eukaryotes. Nonetheless, base modifications, histone marks, and nucleosome positioning of vegetative Loxodes nuclei are consistent with functional differentiation between actively transcribed somatic vs. inactive germline nuclei. Given their phylogenetic position, it is likely that editing was present in the ancestral ciliate but secondarily lost in the Loxodes lineage.