Ionizing radiation responses appear incidental to desiccation responses in the bdelloid rotifer Adineta vaga
Abstract Background The remarkable resistance to ionizing radiation found in anhydrobiotic organisms, such as some bacteria, tardigrades, and bdelloid rotifers has been hypothesized to be incidental to their desiccation resistance. Both stresses produce reactive oxygen species and cause damage to DN...
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| Format: | Article |
| Language: | English |
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BMC
2024-01-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-023-01807-8 |
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| author | Victoria C. Moris Lucie Bruneau Jérémy Berthe Anne-Catherine Heuskin Sébastien Penninckx Sylvia Ritter Uli Weber Marco Durante Etienne G. J. Danchin Boris Hespeels Karine Van Doninck |
| author_facet | Victoria C. Moris Lucie Bruneau Jérémy Berthe Anne-Catherine Heuskin Sébastien Penninckx Sylvia Ritter Uli Weber Marco Durante Etienne G. J. Danchin Boris Hespeels Karine Van Doninck |
| author_sort | Victoria C. Moris |
| collection | DOAJ |
| description | Abstract Background The remarkable resistance to ionizing radiation found in anhydrobiotic organisms, such as some bacteria, tardigrades, and bdelloid rotifers has been hypothesized to be incidental to their desiccation resistance. Both stresses produce reactive oxygen species and cause damage to DNA and other macromolecules. However, this hypothesis has only been investigated in a few species. Results In this study, we analyzed the transcriptomic response of the bdelloid rotifer Adineta vaga to desiccation and to low- (X-rays) and high- (Fe) LET radiation to highlight the molecular and genetic mechanisms triggered by both stresses. We identified numerous genes encoding antioxidants, but also chaperones, that are constitutively highly expressed, which may contribute to the protection of proteins against oxidative stress during desiccation and ionizing radiation. We also detected a transcriptomic response common to desiccation and ionizing radiation with the over-expression of genes mainly involved in DNA repair and protein modifications but also genes with unknown functions that were bdelloid-specific. A distinct transcriptomic response specific to rehydration was also found, with the over-expression of genes mainly encoding Late Embryogenesis Abundant proteins, specific heat shock proteins, and glucose repressive proteins. Conclusions These results suggest that the extreme resistance of bdelloid rotifers to radiation might indeed be a consequence of their capacity to resist complete desiccation. This study paves the way to functional genetic experiments on A. vaga targeting promising candidate proteins playing central roles in radiation and desiccation resistance. |
| first_indexed | 2024-03-07T15:25:45Z |
| format | Article |
| id | doaj.art-71275c24930a467a862909210e0e565e |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-03-07T15:25:45Z |
| publishDate | 2024-01-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-71275c24930a467a862909210e0e565e2024-03-05T16:43:21ZengBMCBMC Biology1741-70072024-01-0122112710.1186/s12915-023-01807-8Ionizing radiation responses appear incidental to desiccation responses in the bdelloid rotifer Adineta vagaVictoria C. Moris0Lucie Bruneau1Jérémy Berthe2Anne-Catherine Heuskin3Sébastien Penninckx4Sylvia Ritter5Uli Weber6Marco Durante7Etienne G. J. Danchin8Boris Hespeels9Karine Van Doninck10Laboratory of Evolutionary Genetics and Ecology (LEGE), Department of Biology – URBE, University of NamurLaboratory of Evolutionary Genetics and Ecology (LEGE), Department of Biology – URBE, University of NamurLaboratory of Evolutionary Genetics and Ecology (LEGE), Department of Biology – URBE, University of NamurNamur Research Institute for Life Sciences (NARILIS), Laboratory of Analysis By Nuclear Reactions (LARN), University of NamurMedical Physics Department, Institut Jules Bordet – Université Libre de BruxellesBiophysics Department, GSI Helmholtzzentrum Für SchwerionenforschungBiophysics Department, GSI Helmholtzzentrum Für SchwerionenforschungBiophysics Department, GSI Helmholtzzentrum Für SchwerionenforschungInstitut Sophia Agrobiotech, INRAE, Université Côte d’Azur, CNRSLaboratory of Evolutionary Genetics and Ecology (LEGE), Department of Biology – URBE, University of NamurLaboratory of Evolutionary Genetics and Ecology (LEGE), Department of Biology – URBE, University of NamurAbstract Background The remarkable resistance to ionizing radiation found in anhydrobiotic organisms, such as some bacteria, tardigrades, and bdelloid rotifers has been hypothesized to be incidental to their desiccation resistance. Both stresses produce reactive oxygen species and cause damage to DNA and other macromolecules. However, this hypothesis has only been investigated in a few species. Results In this study, we analyzed the transcriptomic response of the bdelloid rotifer Adineta vaga to desiccation and to low- (X-rays) and high- (Fe) LET radiation to highlight the molecular and genetic mechanisms triggered by both stresses. We identified numerous genes encoding antioxidants, but also chaperones, that are constitutively highly expressed, which may contribute to the protection of proteins against oxidative stress during desiccation and ionizing radiation. We also detected a transcriptomic response common to desiccation and ionizing radiation with the over-expression of genes mainly involved in DNA repair and protein modifications but also genes with unknown functions that were bdelloid-specific. A distinct transcriptomic response specific to rehydration was also found, with the over-expression of genes mainly encoding Late Embryogenesis Abundant proteins, specific heat shock proteins, and glucose repressive proteins. Conclusions These results suggest that the extreme resistance of bdelloid rotifers to radiation might indeed be a consequence of their capacity to resist complete desiccation. This study paves the way to functional genetic experiments on A. vaga targeting promising candidate proteins playing central roles in radiation and desiccation resistance.https://doi.org/10.1186/s12915-023-01807-8DesiccationRadiationAntioxidantsDNA repairBdelloid rotifers |
| spellingShingle | Victoria C. Moris Lucie Bruneau Jérémy Berthe Anne-Catherine Heuskin Sébastien Penninckx Sylvia Ritter Uli Weber Marco Durante Etienne G. J. Danchin Boris Hespeels Karine Van Doninck Ionizing radiation responses appear incidental to desiccation responses in the bdelloid rotifer Adineta vaga BMC Biology Desiccation Radiation Antioxidants DNA repair Bdelloid rotifers |
| title | Ionizing radiation responses appear incidental to desiccation responses in the bdelloid rotifer Adineta vaga |
| title_full | Ionizing radiation responses appear incidental to desiccation responses in the bdelloid rotifer Adineta vaga |
| title_fullStr | Ionizing radiation responses appear incidental to desiccation responses in the bdelloid rotifer Adineta vaga |
| title_full_unstemmed | Ionizing radiation responses appear incidental to desiccation responses in the bdelloid rotifer Adineta vaga |
| title_short | Ionizing radiation responses appear incidental to desiccation responses in the bdelloid rotifer Adineta vaga |
| title_sort | ionizing radiation responses appear incidental to desiccation responses in the bdelloid rotifer adineta vaga |
| topic | Desiccation Radiation Antioxidants DNA repair Bdelloid rotifers |
| url | https://doi.org/10.1186/s12915-023-01807-8 |
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