Rotifers Highlight the Evolution of Asexuals: the mechanisms of genome evolution in the absence of meiosis

Informations projet

RHEA

N° de convention de subvention: 725998

DOI

10.3030/725998

Projet clôturé

Date de signature de la CE 23 Mai 2017

Date de début 1 Octobre 2017

Date de fin 30 Septembre 2024

Financé au titre de

• EXCELLENT SCIENCE - European Research Council (ERC)

Coût total

€ 1 908 375,00

Contribution de l’UE

€ 1 908 375,00

Coordonné par

UNIVERSITE LIBRE DE BRUXELLES
Belgium

Periodic Reporting for period 5 - RHEA (Rotifers Highlight the Evolution of Asexuals: the mechanisms of genome evolution in the absence of meiosis)

Période du rapport: 2023-10-01 au 2024-09-30

Résumé du contexte et des objectifs généraux du projet

While sexual reproduction is common to almost all eukaryotes, its ubiquity and complexity is often reported as the “queen of problem in evolutionary biology”. Very few organisms have renounced to their complete absence for reproduction suggesting strong evolutionary advantages to the maintenance of sexual reproduction in the long term. It has often been stated that recombination during sexual reproduction (meiosis) is critical to improve the response to selection. However, to study this we need a model system that evolves without sexual reproduction.
Bdelloid rotifers are the most notorious asexual animal model system, having diversified into more than 400 species without males or sexual reproduction. Both its longevity as an asexual clade and its diversity contradicts the expectation that asexual lineages are evolutionary dead-ends. Understanding how these asexual lineages evolve can help elucidating the evolutionary forces that maintain recombination and sexual reproduction. The first objective of this ERC project RHEA is to identify in bdelloid rotifers the specific mechanisms that prevents genome deterioration in the absence of sexual reproduction. The answers obtained will be informative for the theories of sex. In addition to their asexual evolution, bdelloid rotifers possess the unusual feature of extreme desiccation resistance at any stage of their life-cycle. This desiccation resistance also confers bdelloid rotifers with an extreme radiation resistance. Both prolonged desiccation and radiation induce oxidative stress and DNA double strand breaks that bdelloid rotifers seem to handle well by protecting their proteins allowing an efficient repair of the broken DNA upon rehydration. The second main objective of this ERC is to explore the molecular mechanisms that make these animals unique in terms of hyper-resistance, providing a new biological model system for understanding fundamental biological processes such as DNA repair and cell survival. This ERC project, by focusing on a unique study organism combining asexual reproductive features with unusual resistance traits, provides a unique opportunity to discover novel mechanisms in eukaryotes. Moreover, deciphering how rotifers handle potential DNA damage is of considerable interest, not only for understanding their evolutionary adaptations, but also for possible applications to medical fields where DNA integrity is of central importance, such as cancer and aging.
KVD’s groundbreaking ERC research has revealed how A. vaga rotifers use different strategies to protect their cells. In regular body cells, which do not divide, the main defense is a strong antioxidant system that protects proteins. This allows for fast but less precise DNA repair. In contrast, reproductive cells, which pass genetic material to the next generation, use a highly accurate repair system. This system is linked to meiosis (the process of forming reproductive cells) and can fix broken chromosomes over multiple generations. These discoveries change how we understand asexual reproduction, genome stability, and survival in extreme conditions, while also opening new possibilities for medical and biotechnological applications.

Travail effectué depuis le début du projet jusqu’à la fin de la période considérée dans le rapport et principaux résultats atteints jusqu’à présent

This ERC project, headed by Karine Van Doninck (KVD), uncovered how bdelloid rotifers reproduce and maintain genome stability. Combining cytogenetic and advanced sequencing analyses, we assembled Adineta vaga’s 12 chromosomes and discovered homologous chromosome pairing between them—a key feature of meiosis—challenging their long-held status as "ancient asexual ameiotic scandals". Our findings revealed that A. vaga reproduces through a modified form of meiosis, preserving diploidy and heterozygosity in their gametes, while allowing some recombination.
We also discovered a novel DNA repair mechanism, Break-induced Homologous Extension Repair (BIHER), which progressively restores damaged chromosomes across generations following exposure to ionizing radiation. This repair process is linked to homologous recombination during their modified meiosis. It represents a breakthrough in cellular resilience and sheds light on how A. vaga gradually restores its 12-chromosomes and can survive and reproduce despite extreme genomic damage. Additionally, we found that while germline DNA repair is slow, transgenerational but precise, somatic cells rely on faster, error-prone DNA repair mechanisms, correlating with the species’ exceptional survival responses to radiation and desiccation.
Our work extended beyond reproduction and DNA repair. We also identified key genes acquired from bacteria that contribute to their stress resistance, including Ligase E, which enhances radiation tolerance in human cells (patented), and a manganese superoxide dismutase, crucial for oxidative stress defense. These findings emphasize the importance of horizontally acquired genes in bdelloid adaptation and opened doors to applied projects.
Results were published in top-tier journals (e.g. Science Advances, Nature Communications). Beyond academic publishing, KVD launched an art & science initiative, culminating in a public exhibition at PILAR Brussels. This project aimed to communicate the ERC research findings through artistic expression, making the scientific discoveries accessible to a wider audience. The scientific articles and the exhibition garnered substantial press coverage, further amplifying the impact of this project’s dissemination.

Progrès au-delà de l’état des connaissances et impact potentiel prévu (y compris l’impact socio-économique et les conséquences sociétales plus larges du projet jusqu’à présent)

In 2016, alongside her ERC CoG, Karine Van Doninck (KVD) secured an ESA project with postdoc Boris Hespeels, in collaboration with the LARN physics group (UNamur) and Dr. S. Baatout (VITO, Mol). This project investigates the extraordinary resilience of bdelloid rotifers to ionizing radiation, vacuum, and extreme temperatures, with four ISS missions planned—three of which have already launched successfully. Findings from the first mission, along with additional ESA project results, have been published in several scientific journals, including BMC Biology.
Building on insights from the ERC and ESA projects, Rohan Arora’s PhD research at the KVD laboratory explored the antioxidant defense (AOD) system of Adineta vaga, focusing on how its proteins—particularly those involved in DNA repair—are protected under stress. Cell survival critically depends on a functional proteome, yet maintaining protein integrity is especially challenging in extreme environments. Extremotolerant organisms like bdelloid rotifers, which can withstand complete desiccation and high radiation doses, face strong evolutionary pressure to develop novel, efficient antioxidant mechanisms. Prolonged desiccation or exposure to high ionizing radiation (IR) indeed generates excessive reactive oxygen species (ROS), causing widespread damage to DNA, proteins, and other biomolecules.
Arora’s research identified unique antioxidants in several extremotolerant eukaryotes, including bdelloid rotifers. These include naturally occurring chemical elements, small-molecule antioxidant complexes, and horizontally acquired antioxidant proteins like manganese superoxide dismutase. A manuscript detailing these findings is in the final stages of preparation for Nature Communications.
Additionally, KVD secured a proof-of-concept (POC) Innoviris project to develop novel antioxidant formulations inspired by the unique adaptations of these extremotolerant organisms.

Homologous chromosomes, meiosis and DNA DSB repair in the bdelloid rotifer Adineta vaga.