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Recent research on tardigrades uncovers a complex genetic basis for their extreme resilience, challenging previous assumptions about their ecological adaptations and pointing to independent evolutionary events in their capacity for anhydrobiosis.
Tardigrades may be nature’s last survivors. While these tiny, almost translucent animals are easily overlooked, they represent a diverse group that has successfully colonized freshwater, marine, and terrestrial environments on all continents, including Antarctica.
Commonly known as “water bears,” these unusual creatures may be among the most resilient organisms on the planet thanks to their unparalleled ability to survive in extreme conditions, with various species being resistant to drought, high doses of radiation, environments with little oxygen and both high and low temperatures and pressures.
While numerous genes have been suggested to contribute to this extreme tolerance, a comprehensive understanding of the origins and history of these unique adaptations remains elusive. In a new study published in Genome biology and evolutionscientists at the Institute for Advanced Biosciences at Keio University, the university of oslo Museum of Natural History and the University of Bristol reveal a surprisingly intricate network of gene duplications and losses associated with tardigrade extreme tolerance, highlighting the complex genetic landscape driving modern tardigrade ecology.
Understanding tardigrade gene families
As a form of extreme tolerance, tardigrades can survive almost complete desiccation by entering a dormant state called anhydrobiosis (that is to say, life without water), which allows them to reversibly stop their metabolism. Multiple tardigrade-specific gene families were previously found to be associated with anhydrobiosis.
Three of these gene families are called cytosolic, meteritochondrial and yesecretor toabundant heat yessoluble proteins (CAHS, MAHS and SAHS, respectively) depending on the cellular location in which the proteins are expressed. Some tardigrades appear to possess a variant pathway involving two families of abundant heat-soluble proteins first identified in tardigrades. Echiniscus testudo and is generally called EtAHS alpha and beta.
A photograph of the tardigrade. Ramazzottius varieornatus, at the center of a phylogeny of CAHS, the largest of the six desiccation-related protein families analyzed in this study. Credit: Kazuharu Arakawa, Keio Institute for Advanced Biosciences
Tardigrades also possess stress resistance genes that can be found in animals in general, such as the meiotic recombination gene 11 (MRE11), which has been implicated in desiccation tolerance in other animals. Unfortunately, since the identification of these gene families, there has been limited information available on most tardigrade lineages, making it difficult to draw conclusions about their origins, history, and ecological implications.
Investigating tardigrade evolution
To better shed light on the evolution of tardigrade extreme tolerance, the authors of the new study, James Fleming, Davide Pisani and Kazuharu Arakawa, identified sequences from these six gene families in 13 genera of tardigrades, including representatives of the two major lineages. of tardigrades. the Eutardigrades and Heterotardigrades. Their analysis revealed 74 CAHS, 8 MAHS, 29 SAHS, 22 EtAHS alpha, 18 EtAHS beta, and 21 MRE11 sequences, allowing them to construct the first tardigrade phylogenies for these gene families.
Since desiccation resistance likely arose as an adaptation to terrestrial environments, the authors hypothesized that they would find a link between gene duplications and losses in these gene families and habitat changes within tardigrades. “When we started the work, we expected to find that each clade would be clearly clustered around ancient duplications, with few independent losses. “That would help us easily relate them to our understanding of modern habitats and ecology,” says the study’s lead author, James Fleming. “It is an intuitive hypothesis,” he continues, “that the evolution of duplications of these desiccation-related genes should, in theory, contain remnants of the ecological history of these organisms, although in reality this turned out to be too simplistic. .”
Instead, the authors were surprised by the large number of independent duplications of heat-soluble genes, which painted a much more complex picture of the evolution of anhydrobiosis-related genes. However, it is worth noting that there was no clear link between strongly anhydrobiotic species and the number of anhydrobiosis-related genes a species possessed. “What we found was much more interesting,” Fleming says, “a complex web of independent gains and losses that don’t necessarily correlate with the ecologies of modern terrestrial species.”
Independent adaptations in tardigrade lineages
Despite the lack of a relationship between gene duplications and tardigrade ecology, the study provided crucial information about the major transitions that led to the acquisition of anhydrobiosis. The distinct distributions of gene families in the two main groups of tardigrades (CAHS, MAHS and SAHS in eutardigrades and EtAHS alpha and beta in heterotardigrades) suggest that two independent transitions from marine to limnoterrestrial environments occurred within tardigrades, one once in the Eutardigrade ancestor and once within the Heterotardigrades.
This research marks an important step forward in our understanding of the evolution of anhydrobiosis in tardigrades. It also provides a basis for future studies on tardigrade extreme tolerance, which will require the continued development of genomic resources from more diverse tardigrade lineages.
“Unfortunately, we do not have representatives of several important families, such as Isohypsibiidae, and this limits how strongly we can defend our conclusions,” Fleming says. “With more samples of marine and freshwater tardigrades, we will be able to better appreciate the adaptations of the terrestrial members of the group.” Unfortunately, some tardigrades can be especially elusive, presenting a major obstacle to such studies. As an example, Tanarctus bubulubus, one of Fleming’s favorite tardigrades, is too small to see with the naked eye and is only found in North Atlantic sediments, at depths of about 150 m. “Hopefully,” says Fleming, “large-scale sequencing efforts through the Earth Biogenome Project will gradually close this gap in our understanding, and it’s an effort I’m excited to see continue.”
Reference: “The evolution of temperature- and desiccation-related protein families in Tardigrada reveals a complex acquisition of extreme tolerance” by James F Fleming, Davide Pisani and Kazuharu Arakawa, 29 November 2023, Genome biology and evolution.
DOI: 10.1093/gbe/evad217