ABSTRACT: Eukaryotes may experience oxygen deprivation under several physiological and pathological conditions. Because oxygen shortage leads to a reduction in cellular energy production, all the eukaryotes studied so far evolved ways to conserve energy via suppression of metabolism. However, the molecular physiology of animals that naturally and repeatedly experience anoxia is poorly studied. One such animal is the symbiotic marine nematode Laxus oneistus. This thrives, invariably coated by its sulfur-oxidizing bacterium Candidatus Thiosymbion oneisti, in anoxic sulfidic or hypoxic sand. Here, by applying transcriptomics and proteomics, we discovered that, irrespective of the oxygen concentration it is subjected to, this nematode is mostly and constitutively engaging in ubiquitination-mediated proteolysis, energy generation, oxidative stress response and immune response. Furthermore, by incubating L. oneistus under sulfidic anoxic or hypoxic conditions, we found that, under the first condition, the worm upregulated genes involved in ribosome biogenesis, proteolytic systems (autophagy and the ubiquitin-proteasome system), chaperones, detoxification and lectins. Degradation pathways were likely induced to recycle damaged cellular components (mitochondria) and misfolded proteins into nutrients, whereas lectins were likely expressed to promote the attachment of its anaerobic, thiotrophic symbiont. Besides, L. oneistus appeared to survive oxygen deprivation by using alternative electron carriers (rhodoquinone) and acceptors (fumarate) to rewire the electron transfer chain. On the other hand, under hypoxia, genes involved in costly processes (e.g., development, amino acid biosynthesis, feeding behaviour, mating) were upregulated. Intriguingly, the worm’s Toll-like innate immunity pathway and a number of immune effectors (e.g., Bacterial Permeability Increasing proteins, fungicides) were upregulated in the presence of oxygen. In conclusion, we hypothesize that L. oneistus survives in anoxic sulfidic sand by overexpressing degradation processes, rewiring oxidative phosphorylation and by reinforcing its coat of bacterial sulfur-oxidizers. In the presence of oxygen, instead, it appears to exploit glycolysis to eat, mate and grow. Moreover, oxygen appears to affect L. oneistus immune system in such way, as to favor specific attachment of its anaerobic partner in anoxia and to produce broad-range antimicrobials when oxygen is present.
