Department of Functional and Evolutionary Ecology, Environmental Cell Biology Group, University of Vienna, Vienna, Austria.
Vienna Doctoral School of Ecology and Evolution, Vienna, Austria.
Sci Rep. 2022 Jun 13;12(1):9725. doi: 10.1038/s41598-022-13235-9.
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.
真核生物在生理和病理条件下都可能经历缺氧。由于氧气短缺会导致细胞能量产生减少，迄今为止研究过的所有真核生物都通过抑制新陈代谢来节约能量。然而，自然地和反复经历缺氧的动物的分子生理学仍未得到充分探索。海洋线虫 Laxus oneistus 就是这样一种动物。它在缺氧的硫化物或缺氧的沙中茁壮成长，身上总是覆盖着其硫氧化共生体 Candidatus Thiosymbion oneisti。在这里，转录组学和蛋白质组学表明，无论是否缺氧，L. oneistus 主要表达参与泛素化、能量产生、氧化应激反应、免疫反应、发育和翻译的基因。重要的是，当线虫处于缺氧的硫化物条件下时，也高度表达泛素化基因，以及参与自噬、解毒和核糖体生物发生的基因。我们假设这些降解途径被诱导用于将受损的细胞成分（线粒体）和错误折叠的蛋白质回收为营养物质。值得注意的是，当 L. oneistus 处于缺氧的硫化物条件下时，凝集素和粘蛋白基因也被上调，可能是为了促进其硫营养共生体的附着。此外，线虫似乎通过使用替代电子载体（泛醌）和受体（延胡索酸）来生存缺氧，重新布线电子传递链。另一方面，在低氧条件下，与昂贵过程（例如氨基酸生物合成、发育、进食、交配）相关的基因上调，同时线虫的 Toll 样先天免疫途径和几种免疫效应物（例如杀菌/通透性增加蛋白、杀真菌剂）也被上调。总之，我们假设在缺氧的硫化物沙中，L. oneistus 上调降解过程，重新布线氧化磷酸化并加强其细菌硫氧化体的覆盖。相反，在较上层的沙层中，它似乎产生广谱的抗菌物质，并利用氧气进行生物合成和发育。
