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Differential regulation of degradation and immune pathways underlies adaptation of the ectosymbiotic nematode Laxus oneistus to oxic-anoxic interfaces
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Paredes, Gabriela F., Viehboeck, Tobias, Markert, Stephanie, Mausz, Michaela A., Sato, Yui, Liebeke, Manuel, König, Lena and Bulgheresi, Silvia (2022) Differential regulation of degradation and immune pathways underlies adaptation of the ectosymbiotic nematode Laxus oneistus to oxic-anoxic interfaces. Scientific Reports, 12 (1). 9725. doi:10.1038/s41598-022-13235-9 ISSN 2045-2322.
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WRAP-differential-regulation-degradation-immune-pathways-underlies-adaptation-ectosymbiotic-nematode-Laxus-oneistus-oxic-anoxic-interfaces-Mausz-2022.pdf - Published Version - Requires a PDF viewer. Available under License Creative Commons Attribution 4.0. Download (1516Kb) | Preview |
Official URL: https://doi.org/10.1038/s41598-022-13235-9
Abstract
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.
| Item Type: | Journal Article | |||||||||
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| Subjects: | Q Science > QH Natural history > QH301 Biology | |||||||||
| Divisions: | Faculty of Science, Engineering and Medicine > Science > Life Sciences (2010- ) | |||||||||
| SWORD Depositor: | Library Publications Router | |||||||||
| Library of Congress Subject Headings (LCSH): | Eukaryotic cells -- Research, Developmental biology, Oxygen -- Physiological transport, Anoxemia, Metabolism | |||||||||
| Journal or Publication Title: | Scientific Reports | |||||||||
| Publisher: | Nature Publishing Group | |||||||||
| ISSN: | 2045-2322 | |||||||||
| Official Date: | 13 June 2022 | |||||||||
| Dates: |
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| Volume: | 12 | |||||||||
| Number: | 1 | |||||||||
| Article Number: | 9725 | |||||||||
| DOI: | 10.1038/s41598-022-13235-9 | |||||||||
| Status: | Peer Reviewed | |||||||||
| Publication Status: | Published | |||||||||
| Access rights to Published version: | Open Access (Creative Commons) | |||||||||
| Date of first compliant deposit: | 8 September 2022 | |||||||||
| Date of first compliant Open Access: | 9 September 2022 | |||||||||
| RIOXX Funder/Project Grant: |
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