Back to the roots, desiccation and radiation resistances are ancestral characters in bdelloid rotifers

Boris Hespeels; Diego Fontaneto; Valérie Cornet; Sébastien Penninckx; Jérémy Berthe; Lucie Bruneau; James W Larrick; Eloïse Rapport; Jérémie Bailly; Nicolas Debortoli; Nataliia Iakovenko; Karel Janko; Anne-Catherine Heuskin; Stéphane Lucas; Bernard Hallet; Karine Van Doninck

doi:10.1186/s12915-023-01554-w

Back to the roots, desiccation and radiation resistances are ancestral characters in bdelloid rotifers

Boris Hespeels, Diego Fontaneto, Valérie Cornet, Sébastien Penninckx, Jérémy Berthe, Lucie Bruneau, James W Larrick, Eloïse Rapport, Jérémie Bailly, Nicolas Debortoli, Nataliia Iakovenko, Karel Janko, Anne-Catherine Heuskin, Stéphane Lucas, Bernard Hallet, Karine Van Doninck

Résultats de recherche: Contribution à un journal/une revue › Article › Revue par des pairs

Résumé

BACKGROUND: Bdelloid rotifers are micro-invertebrates distributed worldwide, from temperate latitudes to the most extreme areas of the planet like Antarctica or the Atacama Desert. They have colonized any habitat where liquid water is temporarily available, including terrestrial environments such as soils, mosses, and lichens, tolerating desiccation and other types of stress such as high doses of ionizing radiation (IR). It was hypothesized that bdelloid desiccation and radiation resistance may be attributed to their potential ability to repair DNA double-strand breaks (DSBs). Here, these properties are investigated and compared among nine bdelloid species collected from both mild and harsh habitats, addressing the correlation between the ability of bdelloid rotifers to survive desiccation and their capacity to repair massive DNA breakage in a phylogenetically explicit context. Our research includes both specimens isolated from habitats that experience frequent desiccation (at least 1 time per generation), and individuals sampled from habitats that rarely or never experienced desiccation.

RESULTS: Our analysis reveals that DNA repair prevails in somatic cells of both desiccation-tolerant and desiccation-sensitive bdelloid species after exposure to X-ray radiation. Species belonging to both categories are able to withstand high doses of ionizing radiation, up to 1000 Gy, without experiencing any negative effects on their survival. However, the fertility of two desiccation-sensitive species, Rotaria macrura and Rotaria rotatoria, was more severely impacted by low doses of radiation than that of desiccation-resistant species. Surprisingly, the radioresistance of desiccation-resistant species is not related to features of their original habitat. Indeed, bdelloids isolated from Atacama Desert or Antarctica were not characterized by a higher radioresistance than species found in more temperate environments.

CONCLUSIONS: Tolerance to desiccation and radiation are supported as ancestral features of bdelloid rotifers, with a group of species of the genus Rotaria having lost this trait after colonizing permanent water habitats. Together, our results provide a comprehensive overview of the evolution of desiccation and radiation resistance among bdelloid rotifers.

langue originale	Anglais
Numéro d'article	72
Pages (de - à)	72
Nombre de pages	1
journal	BMC biology
Volume	21
Numéro de publication	1
Les DOIs	https://doi.org/10.1186/s12915-023-01554-w
Etat de la publication	Publié - déc. 2023

Financement

The authors thank V. Baumlé, C. Bopp, M. Terwagne, and E. Nicolas for useful discussions and comments. C. Demazy is highly thanked for her help in Antarctic species maintenance. The authors are also grateful to C. Wilson, A. Houtain, and D.M Welch who provided respectively clones of A. ricciae , R. macrura, and P. roseola. We thank C. Ricci for her help concerning geographical origin of species used in this research. We thank Drs. Nathalie A. Cabrol, Director of the Carl Sagan Center, SETI Institute, Mountain View, CA, USA, and Dr. Colin Flinders, University of Southern California for support, Ms. Hong Wang for help with Atacama species cloning and maintenance and LaRuke Development for financial support. The authors thank the European Space Agency (ESA) and the Belgian Federal Science Policy Office (BELSPO) for their support in the framework of the PRODEX Program. Project was supported by the European Space Agency (ESA) and the Belgian Federal Science Policy Office (BELSPO) in the framework of the PRODEX Program. KVD was supported by the European Research Council (ERC) with the grant agreement 725998 (RHEA). S. Penninckx is funded by the Walloon Region (PROTHERWAL, grant n°7289). K. Janko, D. Fontaneto and N.Iakovenko received support from Czech Science Foundation grant No. 22-28778S.

Bailleurs de fonds	Numéro du bailleur de fonds
European Space Agency
SETI Institute
Waalse Gewest
Carl Sagan Center
Belgian Science Policy Office
LaRuke Development
European Research Council
RHEA
Horizon 2020 Framework Programme	725998
Grantová Agentura České Republiky	22-28778S
PROTHERWAL	7289

SDG des Nations Unies

Ce résultat contribue à ou aux Objectifs de développement durable suivants

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10.1186/s12915-023-01554-w

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19 Citations
4 Article

Rotifers in space: transcriptomic response of the bdelloid rotifer Adineta vaga aboard the International Space Station
Moris, V. C., Bruneau, L., Berthe, J., Coos, R., Baselet, B., Heuskin, A.-C., Caplin, N., Demets, R., Krause, J., Zuijderduijn, L., Tortora, A., Herova, M., Penninckx, S., Parmitano, L., Tabury, K., Baatout, S., Van Doninck, K. & Hespeels, B., 1 juil. 2025, Dans: BMC biology. 23, 1, p. 182 182.
Résultats de recherche: Contribution à un journal/une revue › Article › Revue par des pairs

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2 Téléchargements (Pure)
DNA repair during nonreductional meiosis in the asexual rotifer Adineta vaga
Terwagne, M., Nicolas, E., Hespeels, B., Herter, L., Virgo, J., Demazy, C., Heuskin, A.-C., Hallet, B. & Van Doninck, K., déc. 2022, Dans: Science Advances. 8, 48
Résultats de recherche: Contribution à un journal/une revue › Article › Revue par des pairs

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Iron Ladies: How Desiccated Asexual Rotifer Adineta vaga Deal With X-Rays and Heavy Ions?
Hespeels, B., Penninckx, S., Cornet, V., Bruneau, L., Bopp, C., Baumlé, V., Redivo, B., Heuskin, A.-C., Moeller, R., Fujimori, A., Lucas, S. & Van Doninck, K., 2020, Dans: Frontiers in Microbiology. 11, p. 1792 1792.
Résultats de recherche: Contribution à un journal/une revue › Article › Revue par des pairs

Accès ouvert

1 Terminé

RISE 2016-2018: Breaking bad? Genomic evolution and protective mechanisms in asexual bdelloid rotifers exposed to charged particle beams.
Hespeels, B. (Responsable du Projet), Van Doninck, K. (Co-investigateur), Lucas, S. (Co-investigateur), Heuskin, A.-C. (Rôle de support), BOPP, C. (Chercheur), BAUMLE, V. (Chercheur), Baatout, S. (Co-investigateur), Baselet, B. (Chercheur), Moreels, M. (Chercheur), Terwagne, M. (Rôle de support), Bruneau, L. (Technicien), RIGAUX, C. (Chercheur) & BRUNETTI, E. (Chercheur)
1/01/16 → 31/12/18
Projet: Recherche

Synthèse, Irradiation et Analyse de Matériaux (SIAM) (2016 - ...)
Louette, P. (!!Manager), Colaux, J. (!!Manager), Felten, A. (!!Manager), Tabarrant, T. (!!Operator), COME, F. (!!Operator) & Debarsy, P.-L. (!!Manager)
Plateforme technologique Synthese, irradiation et analyse des materiaux
Equipement/installations: Plateforme technolgique

New Biology Findings from University of Namur Published (Back to the roots, desiccation and radiation resistances are ancestral characters in bdelloid rotifers)
Hespeels, B., Heuskin, A.-C., Lucas, S., Cornet, V. & Penninckx, S.
21/04/23
1 élément de Couverture média
Presse/Médias: Commentaire d'expert

Additional file 4 of Back to the roots, desiccation and radiation resistances are ancestral characters in bdelloid rotifers
Hespeels, B. (Contributeur), Fontaneto, D. (Contributeur), Cornet, V. (Contributeur), Penninckx, S. (Contributeur), Berthe, J. (Contributeur), Bruneau, L. (Contributeur), Larrick, J. W. (Contributeur), Rapport, E. (Contributeur), Bailly, J. (Contributeur), Debortoli, N. (Contributeur), Iakovenko, N. (Contributeur), Janko, K. (Contributeur), Heuskin, A.-C. (Contributeur), Lucas, S. (Contributeur), Hallet, B. (Contributeur) & Van Doninck, K. (Contributeur), Figshare, 2023
DOI: 10.6084/m9.figshare.22625101
Ensemble de données

Contient cette citation

Hespeels, B., Fontaneto, D., Cornet, V., Penninckx, S., Berthe, J., Bruneau, L., Larrick, J. W., Rapport, E., Bailly, J., Debortoli, N., Iakovenko, N., Janko, K., Heuskin, A.-C., Lucas, S., Hallet, B., & Van Doninck, K. (2023). Back to the roots, desiccation and radiation resistances are ancestral characters in bdelloid rotifers. BMC biology, 21(1), 72. Article 72. https://doi.org/10.1186/s12915-023-01554-w

@article{079e28811413469ea2d511b8d770d1ac,

title = "Back to the roots, desiccation and radiation resistances are ancestral characters in bdelloid rotifers",

abstract = "BACKGROUND: Bdelloid rotifers are micro-invertebrates distributed worldwide, from temperate latitudes to the most extreme areas of the planet like Antarctica or the Atacama Desert. They have colonized any habitat where liquid water is temporarily available, including terrestrial environments such as soils, mosses, and lichens, tolerating desiccation and other types of stress such as high doses of ionizing radiation (IR). It was hypothesized that bdelloid desiccation and radiation resistance may be attributed to their potential ability to repair DNA double-strand breaks (DSBs). Here, these properties are investigated and compared among nine bdelloid species collected from both mild and harsh habitats, addressing the correlation between the ability of bdelloid rotifers to survive desiccation and their capacity to repair massive DNA breakage in a phylogenetically explicit context. Our research includes both specimens isolated from habitats that experience frequent desiccation (at least 1 time per generation), and individuals sampled from habitats that rarely or never experienced desiccation.RESULTS: Our analysis reveals that DNA repair prevails in somatic cells of both desiccation-tolerant and desiccation-sensitive bdelloid species after exposure to X-ray radiation. Species belonging to both categories are able to withstand high doses of ionizing radiation, up to 1000 Gy, without experiencing any negative effects on their survival. However, the fertility of two desiccation-sensitive species, Rotaria macrura and Rotaria rotatoria, was more severely impacted by low doses of radiation than that of desiccation-resistant species. Surprisingly, the radioresistance of desiccation-resistant species is not related to features of their original habitat. Indeed, bdelloids isolated from Atacama Desert or Antarctica were not characterized by a higher radioresistance than species found in more temperate environments.CONCLUSIONS: Tolerance to desiccation and radiation are supported as ancestral features of bdelloid rotifers, with a group of species of the genus Rotaria having lost this trait after colonizing permanent water habitats. Together, our results provide a comprehensive overview of the evolution of desiccation and radiation resistance among bdelloid rotifers.",

keywords = "Ancestral character reconstructions, Antarctica, Atacama Desert, Bdelloid rotifers, DNA repair, Desiccation, Extreme tolerance",

author = "Boris Hespeels and Diego Fontaneto and Val{\'e}rie Cornet and S{\'e}bastien Penninckx and J{\'e}r{\'e}my Berthe and Lucie Bruneau and Larrick, \{James W\} and Elo{\"i}se Rapport and J{\'e}r{\'e}mie Bailly and Nicolas Debortoli and Nataliia Iakovenko and Karel Janko and Anne-Catherine Heuskin and St{\'e}phane Lucas and Bernard Hallet and \{Van Doninck\}, Karine",

note = "Funding Information: Project was supported by the European Space Agency (ESA) and the Belgian Federal Science Policy Office (BELSPO) in the framework of the PRODEX Program. KVD was supported by the European Research Council (ERC) with the grant agreement 725998 (RHEA). S. Penninckx is funded by the Walloon Region (PROTHERWAL, grant n°7289). K. Janko, D. Fontaneto and N.Iakovenko received support from Czech Science Foundation grant No. 22-28778S. Funding Information: The authors thank V. Bauml{\'e}, C. Bopp, M. Terwagne, and E. Nicolas for useful discussions and comments. C. Demazy is highly thanked for her help in Antarctic species maintenance. The authors are also grateful to C. Wilson, A. Houtain, and D.M Welch who provided respectively clones of A. ricciae, R. macrura, and P. roseola. We thank C. Ricci for her help concerning geographical origin of species used in this research. We thank Drs. Nathalie A. Cabrol, Director of the Carl Sagan Center, SETI Institute, Mountain View, CA, USA, and Dr. Colin Flinders, University of Southern California for support, Ms. Hong Wang for help with Atacama species cloning and maintenance and LaRuke Development for financial support. The authors thank the European Space Agency (ESA) and the Belgian Federal Science Policy Office (BELSPO) for their support in the framework of the PRODEX Program. Publisher Copyright: {\textcopyright} 2023, The Author(s).",

year = "2023",

month = dec,

doi = "10.1186/s12915-023-01554-w",

language = "English",

volume = "21",

pages = "72",

journal = "BMC biology",

issn = "1741-7007",

publisher = "BioMed Central Ltd",

number = "1",

}

Hespeels, B, Fontaneto, D, Cornet, V , Penninckx, S, Berthe, J, Bruneau, L, Larrick, JW, Rapport, E, Bailly, J, Debortoli, N, Iakovenko, N, Janko, K, Heuskin, A-C , Lucas, S, Hallet, B & Van Doninck, K 2023, 'Back to the roots, desiccation and radiation resistances are ancestral characters in bdelloid rotifers', BMC biology, VOL. 21, Numéro 1, 72, p. 72. https://doi.org/10.1186/s12915-023-01554-w

TY - JOUR

T1 - Back to the roots, desiccation and radiation resistances are ancestral characters in bdelloid rotifers

AU - Hespeels, Boris

AU - Fontaneto, Diego

AU - Cornet, Valérie

AU - Penninckx, Sébastien

AU - Berthe, Jérémy

AU - Bruneau, Lucie

AU - Larrick, James W

AU - Rapport, Eloïse

AU - Bailly, Jérémie

AU - Debortoli, Nicolas

AU - Iakovenko, Nataliia

AU - Janko, Karel

AU - Heuskin, Anne-Catherine

AU - Lucas, Stéphane

AU - Hallet, Bernard

AU - Van Doninck, Karine

N1 - Funding Information: Project was supported by the European Space Agency (ESA) and the Belgian Federal Science Policy Office (BELSPO) in the framework of the PRODEX Program. KVD was supported by the European Research Council (ERC) with the grant agreement 725998 (RHEA). S. Penninckx is funded by the Walloon Region (PROTHERWAL, grant n°7289). K. Janko, D. Fontaneto and N.Iakovenko received support from Czech Science Foundation grant No. 22-28778S. Funding Information: The authors thank V. Baumlé, C. Bopp, M. Terwagne, and E. Nicolas for useful discussions and comments. C. Demazy is highly thanked for her help in Antarctic species maintenance. The authors are also grateful to C. Wilson, A. Houtain, and D.M Welch who provided respectively clones of A. ricciae, R. macrura, and P. roseola. We thank C. Ricci for her help concerning geographical origin of species used in this research. We thank Drs. Nathalie A. Cabrol, Director of the Carl Sagan Center, SETI Institute, Mountain View, CA, USA, and Dr. Colin Flinders, University of Southern California for support, Ms. Hong Wang for help with Atacama species cloning and maintenance and LaRuke Development for financial support. The authors thank the European Space Agency (ESA) and the Belgian Federal Science Policy Office (BELSPO) for their support in the framework of the PRODEX Program. Publisher Copyright: © 2023, The Author(s).

PY - 2023/12

Y1 - 2023/12

N2 - BACKGROUND: Bdelloid rotifers are micro-invertebrates distributed worldwide, from temperate latitudes to the most extreme areas of the planet like Antarctica or the Atacama Desert. They have colonized any habitat where liquid water is temporarily available, including terrestrial environments such as soils, mosses, and lichens, tolerating desiccation and other types of stress such as high doses of ionizing radiation (IR). It was hypothesized that bdelloid desiccation and radiation resistance may be attributed to their potential ability to repair DNA double-strand breaks (DSBs). Here, these properties are investigated and compared among nine bdelloid species collected from both mild and harsh habitats, addressing the correlation between the ability of bdelloid rotifers to survive desiccation and their capacity to repair massive DNA breakage in a phylogenetically explicit context. Our research includes both specimens isolated from habitats that experience frequent desiccation (at least 1 time per generation), and individuals sampled from habitats that rarely or never experienced desiccation.RESULTS: Our analysis reveals that DNA repair prevails in somatic cells of both desiccation-tolerant and desiccation-sensitive bdelloid species after exposure to X-ray radiation. Species belonging to both categories are able to withstand high doses of ionizing radiation, up to 1000 Gy, without experiencing any negative effects on their survival. However, the fertility of two desiccation-sensitive species, Rotaria macrura and Rotaria rotatoria, was more severely impacted by low doses of radiation than that of desiccation-resistant species. Surprisingly, the radioresistance of desiccation-resistant species is not related to features of their original habitat. Indeed, bdelloids isolated from Atacama Desert or Antarctica were not characterized by a higher radioresistance than species found in more temperate environments.CONCLUSIONS: Tolerance to desiccation and radiation are supported as ancestral features of bdelloid rotifers, with a group of species of the genus Rotaria having lost this trait after colonizing permanent water habitats. Together, our results provide a comprehensive overview of the evolution of desiccation and radiation resistance among bdelloid rotifers.

AB - BACKGROUND: Bdelloid rotifers are micro-invertebrates distributed worldwide, from temperate latitudes to the most extreme areas of the planet like Antarctica or the Atacama Desert. They have colonized any habitat where liquid water is temporarily available, including terrestrial environments such as soils, mosses, and lichens, tolerating desiccation and other types of stress such as high doses of ionizing radiation (IR). It was hypothesized that bdelloid desiccation and radiation resistance may be attributed to their potential ability to repair DNA double-strand breaks (DSBs). Here, these properties are investigated and compared among nine bdelloid species collected from both mild and harsh habitats, addressing the correlation between the ability of bdelloid rotifers to survive desiccation and their capacity to repair massive DNA breakage in a phylogenetically explicit context. Our research includes both specimens isolated from habitats that experience frequent desiccation (at least 1 time per generation), and individuals sampled from habitats that rarely or never experienced desiccation.RESULTS: Our analysis reveals that DNA repair prevails in somatic cells of both desiccation-tolerant and desiccation-sensitive bdelloid species after exposure to X-ray radiation. Species belonging to both categories are able to withstand high doses of ionizing radiation, up to 1000 Gy, without experiencing any negative effects on their survival. However, the fertility of two desiccation-sensitive species, Rotaria macrura and Rotaria rotatoria, was more severely impacted by low doses of radiation than that of desiccation-resistant species. Surprisingly, the radioresistance of desiccation-resistant species is not related to features of their original habitat. Indeed, bdelloids isolated from Atacama Desert or Antarctica were not characterized by a higher radioresistance than species found in more temperate environments.CONCLUSIONS: Tolerance to desiccation and radiation are supported as ancestral features of bdelloid rotifers, with a group of species of the genus Rotaria having lost this trait after colonizing permanent water habitats. Together, our results provide a comprehensive overview of the evolution of desiccation and radiation resistance among bdelloid rotifers.

KW - Ancestral character reconstructions

KW - Antarctica

KW - Atacama Desert

KW - Bdelloid rotifers

KW - DNA repair

KW - Desiccation

KW - Extreme tolerance

UR - https://www.scopus.com/pages/publications/85151889788

U2 - 10.1186/s12915-023-01554-w

DO - 10.1186/s12915-023-01554-w

M3 - Article

C2 - 37024917

SN - 1741-7007

VL - 21

SP - 72

JO - BMC biology

JF - BMC biology

IS - 1

M1 - 72

ER -

Back to the roots, desiccation and radiation resistances are ancestral characters in bdelloid rotifers

Résumé

Financement

SDG des Nations Unies

Accès au document

Autres fichiers et liens

Empreinte digitale

Résultat de recherche

Rotifers in space: transcriptomic response of the bdelloid rotifer Adineta vaga aboard the International Space Station

DNA repair during nonreductional meiosis in the asexual rotifer Adineta vaga

Iron Ladies: How Desiccated Asexual Rotifer Adineta vaga Deal With X-Rays and Heavy Ions?

Projets

RISE 2016-2018: Breaking bad? Genomic evolution and protective mechanisms in asexual bdelloid rotifers exposed to charged particle beams.

Équipement

Synthèse, Irradiation et Analyse de Matériaux (SIAM) (2016 - ...)

Presse/médias

New Biology Findings from University of Namur Published (Back to the roots, desiccation and radiation resistances are ancestral characters in bdelloid rotifers)

Ensembles de données

Additional file 4 of Back to the roots, desiccation and radiation resistances are ancestral characters in bdelloid rotifers

Contient cette citation