Differential regulation of degradation and immune pathways underlies adaptation of the ectosymbiotic nematode Laxus oneistus to oxic-anoxic interfaces.
Differential regulation of degradation and immune pathways underlies adaptation of the ectosymbiotic nematode Laxus oneistus to oxic-anoxic interfaces.
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DOI：
10.1038/s41598-022-13235-9
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发表时间：
2022-06-13
影响因子：
4.6
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中科院分区：
文献类型：
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真核生物在生理和病理条件下都会经历缺氧。由于缺氧导致细胞能量产生减少，到目前为止研究的所有真核生物都通过抑制新陈代谢来保存能量。然而，自然和反复经历缺氧的动物的分子生理学还没有得到充分的研究。其中一种动物是海洋线虫Laxus oneistus。它在缺氧的硫酸盐或缺氧的沙子中，总是被其硫氧化共生菌Candidatus Thiosymbion oneisti包裹着，茁壮成长。在这里，转录组学和蛋白质组学表明，无论是在缺氧还是非缺氧条件下，东方乳杆菌都主要表达与泛素化、能量生成、氧化应激反应、免疫反应、发育和翻译有关的基因。重要的是，当线虫处于缺氧的硫化条件下时，泛素化基因以及参与自噬、解毒和核糖体生物发生的基因也高度表达。我们假设，这些降解途径是被诱导回收受损的细胞成分(线粒体)和错误折叠的蛋白质成为营养物质。值得注意的是，当欧洲乳杆菌处于低氧硫化条件下时，凝集素和粘蛋白基因也上调，潜在地促进了其硫营养共生体的附着。此外，线虫似乎通过使用另一种电子载体(罗多酚)和受体(富马酸)来重新连接电子转移链，从而在缺氧条件下存活下来。另一方面，在低氧条件下，参与昂贵过程(如氨基酸生物合成、发育、取食、交配)的基因以及蠕虫的Toll样天然免疫途径和几种免疫效应因子(如杀菌/通透性增加蛋白、杀菌剂)上调。综上所述，我们假设，在缺氧的硫酸盐沙子中，Oneistus上调了降解过程，重新连接了氧化磷酸化，并加强了其细菌硫氧化剂的外壳。相反，在上层沙层，它似乎产生了广泛的抗菌剂，并利用氧气进行生物合成和发育。
Eukaryotes may experience oxygen deprivation under both physiological and pathological conditions. Because oxygen shortage leads to a reduction in cellular energy production, all eukaryotes studied so far conserve energy by suppressing their metabolism. However, the molecular physiology of animals that naturally and repeatedly experience anoxia is underexplored. One such animal is the marine nematode Laxus oneistus. It thrives, invariably coated by its sulfur-oxidizing symbiont Candidatus Thiosymbion oneisti, in anoxic sulfidic or hypoxic sand. Here, transcriptomics and proteomics showed that, whether in anoxia or not, L. oneistus mostly expressed genes involved in ubiquitination, energy generation, oxidative stress response, immune response, development, and translation. Importantly, ubiquitination genes were also highly expressed when the nematode was subjected to anoxic sulfidic conditions, together with genes involved in autophagy, detoxification and ribosome biogenesis. We hypothesize that these degradation pathways were induced to recycle damaged cellular components (mitochondria) and misfolded proteins into nutrients. Remarkably, when L. oneistus was subjected to anoxic sulfidic conditions, lectin and mucin genes were also upregulated, potentially to promote the attachment of its thiotrophic symbiont. Furthermore, the nematode appeared to survive oxygen deprivation by using an alternative electron carrier (rhodoquinone) and acceptor (fumarate), to rewire the electron transfer chain. On the other hand, under hypoxia, genes involved in costly processes (e.g., amino acid biosynthesis, development, feeding, mating) were upregulated, together with the worm’s Toll-like innate immunity pathway and several immune effectors (e.g., bactericidal/permeability-increasing proteins, fungicides). In conclusion, we hypothesize that, in anoxic sulfidic sand, L. oneistus upregulates degradation processes, rewires the oxidative phosphorylation and reinforces its coat of bacterial sulfur-oxidizers. In upper sand layers, instead, it appears to produce broad-range antimicrobials and to exploit oxygen for biosynthesis and development.
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