BACKGROUND Symbiotic relationships between microbes and their hosts are widespread and diverse, often providing protection or nutrients, and may be either obligate or facultative. However, the genetic mechanisms allowing organisms to maintain host-symbiont associations at the molecular level are still mostly unknown, and in the case of bacterial-animal associations, most genetic studies have focused on adaptations and mechanisms of the bacterial partner. The gutless tubeworms (Siboglinidae, Annelida) are obligate hosts of chemoautotrophic endosymbionts (except for Osedax which houses heterotrophic Oceanospirillales), which rely on the sulfide-oxidizing symbionts for nutrition and growth. Whereas several siboglinid endosymbiont genomes have been characterized, genomes of hosts and their adaptations to this symbiosis remain unexplored. RESULTS Here, we present and characterize adaptations of the cold seep-dwelling tubeworm Lamellibrachia luymesi, one of the longest-lived solitary invertebrates. We sequenced the worm's ~ 688-Mb haploid genome with an overall completeness of ~ 95% and discovered that L. luymesi lacks many genes essential in amino acid biosynthesis, obligating them to products provided by symbionts. Interestingly, the host is known to carry hydrogen sulfide to thiotrophic endosymbionts using hemoglobin. We also found an expansion of hemoglobin B1 genes, many of which possess a free cysteine residue which is hypothesized to function in sulfide binding. Contrary to previous analyses, the sulfide binding mediated by zinc ions is not conserved across tubeworms. Thus, the sulfide-binding mechanisms in sibgolinids need to be further explored, and B1 globins might play a more important role than previously thought. Our comparative analyses also suggest the Toll-like receptor pathway may be essential for tolerance/sensitivity to symbionts and pathogens. Several genes related to the worm's unique life history which are known to play important roles in apoptosis, cell proliferation, and aging were also identified. Last, molecular clock analyses based on phylogenomic data suggest modern siboglinid diversity originated in 267 mya (± 70 my) support previous hypotheses indicating a Late Mesozoic or Cenozoic origins of approximately 50-126 mya for vestimentiferans. CONCLUSIONS Here, we elucidate several specific adaptations along various molecular pathways that link phenome to genome to improve understanding of holobiont evolution. Our findings of adaptation in genomic mechanisms to reducing environments likely extend to other chemosynthetic symbiotic systems.

中文翻译：

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深海蠕虫 Lamellibrachia luymesi 对化学共生的基因组适应。

背景技术微生物与其宿主之间的共生关系广泛且多样，通常提供保护或营养，并且可以是专性的或兼性的。然而，允许生物体在分子水平上维持宿主-共生体关联的遗传机制仍然大多未知，就细菌-动物关联而言，大多数遗传学研究都集中在细菌伙伴的适应和机制上。无肠管虫（Siboglinidae、Annelida）是化能自养内共生体的专性宿主（Osedax 除外，它拥有异养海洋螺菌目），它们依赖硫化物氧化共生体获取营养和生长。尽管已经对几种西博格列尼内共生体基因组进行了表征，但宿主基因组及其对这种共生关系的适应仍未得到探索。结果在这里，我们展示并描述了冷泉管虫 Lamellibrachia luymesi 的适应特征，Lamellibrachia luymesi 是最长寿的独居无脊椎动物之一。我们对蠕虫约 688 Mb 的单倍体基因组进行了测序，总体完整性约为 95%，发现 L. luymesi 缺乏许多氨基酸生物合成必需的基因，使它们必须依赖共生体提供的产物。有趣的是，已知宿主利用血红蛋白将硫化氢携带至硫营养型内共生体。我们还发现了血红蛋白 B1 基因的扩展，其中许多基因具有游离的半胱氨酸残基，推测其在硫醚结合中发挥作用。与之前的分析相反，锌离子介导的硫化物结合在管虫中并不保守。因此，sibgolinids 中的硫化物结合机制需要进一步探索，B1 球蛋白可能发挥比之前想象的更重要的作用。我们的比较分析还表明，Toll 样受体途径可能对于共生体和病原体的耐受性/敏感性至关重要。还鉴定了与线虫独特生活史相关的几个基因，这些基因在细胞凋亡、细胞增殖和衰老中发挥重要作用。最后，基于系统发育学数据的分子钟分析表明，现代 siboglinid 多样性起源于 267 mya (± 70 my)，支持了先前的假设，表明 Vestimentiferans 起源于中生代晚期或新生代约 50-126 mya。结论在这里，我们阐明了沿着连接表型组和基因组的各种分子途径的几种特定适应，以增进对全生物进化的理解。我们对基因组机制适应减少环境的发现可能会扩展到其他化学合成共生系统。