Tardigrade genomes reveal secrets of extreme survival

Tardigrades may be nature's ultimate survivors. While it is easy to overlook these small, almost transparent animals, they represent a diverse group that has successfully colonized freshwater, marine, and terrestrial environments on every continent, including Antarctica.

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… Classify Being resistant to drought, high doses of radiation, low oxygen environments, and high and low temperatures and pressures.

While many genes have been proposed to contribute to this extreme tolerance, a comprehensive understanding of the origins and history of these unique adaptations has remained elusive. In a new study published in Genome biology and evolutionscientists at Keio University's Institute for Advanced Biosciences University of Oslo Natural History Museum, and University of Bristol It reveals a surprisingly complex network of gene duplications and losses associated with the extreme endurance of tardigrades, highlighting the complex genetic landscape that drives the ecology of modern tardigrades.

Understanding Tardigrade Gene Families

As a form of extreme endurance, tardigrades can survive almost complete dehydration by entering a state of diapause called anhydrobiosis.any, Life without water), allowing them to reversibly stop their metabolism. Multiple tardigrade-specific gene families have previously been found to be associated with ahydrobiosis.

Three of these gene families are referred to as CI beg you, MMitochondria, and sSecreted aAmple HHe eats sSoluble proteins (CAHS, MAHS, and SAHS, respectively) based on the cellular location in which the proteins are expressed. Some tardigrades appear to have a different pathway involving two families of abundant, heat-soluble proteins that were first identified in tardigrades. Equinesus test They are usually referred to as alpha and beta EtAHS.

Picture of a tardigrade Ramazotius variornatus, in the middle of the CAHS lineage, is the largest of the six drought-associated 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 broader animals, such as the meiotic recombination 11 (MRE11) gene, which has been implicated in drought tolerance in other animals. Unfortunately, since the identification of these gene families, limited information has been available from most tardigrade lineages, making it difficult to draw conclusions about their origins, history, and ecological implications.

Investigation of the evolution of tardigrades

To better shed light on the evolution of tardigrades' extreme tolerance, the authors of the new study — James Fleming, David Pisani, and Kazuharu Arakawa — identified sequences from these six gene families across 13 genera of tardigrades, including representatives from each of the major tardigrade lineages. 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 drought resistance likely emerged as an adaptation to terrestrial environments, the researchers hypothesized that they would find a link between gene duplication and loss 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 versions, with few independent losses. This would help us easily link them to understanding modern habitats and ecology,” says the study’s lead author, James Fleming. “It is an intuitive hypothesis that the evolution of transcription of these drought-related genes should, in theory, contain remnants of the environmental history of these organisms, although in reality, this turns out to be an oversimplification.”

Instead, the researchers were surprised by the huge number of independent copies of heat-soluble genes, which painted a more complex picture of the evolution of genes related to anhydrobiosis. However, it is worth noting that there was no clear link between strong anhydrobiological species and the number of anhydrobiologically related genes a species possesses. “What we found was much more exciting,” Fleming says, “a complex network of independent gains and losses that are not necessarily linked to the environments of modern terrestrial species.”

Autonomous adaptations in tardigrade lineages

Although there was no relationship between gene duplication and the environment of tardigrades, the study provided crucial insight into the key transformations that led to the acquisition of ahydrobiosis. The distinct distributions of gene families across the two major groups of tardigrades—CAHS, MAHS, and SAHS in Eutardigrades and EtAHS alpha and beta in Heterotardigrades—suggest that two independent transitions from marine to terrestrial limpid environments occurred within tardigrades, once in the Eutardigrade ancestor and once in Within Heterotardigrades.

This research represents an important step forward in our understanding of the evolution of ahydrobiosis in tardigrades. It also provides a basis for future studies on extreme tardigrade tolerance, which will require continued development of genomic resources from more diverse tardigrade lineages.

“Unfortunately, we don't have representatives from several important families, such as the Isohypsibiidae, and this limits the extent to which we can stick to our conclusions,” Fleming says. “With more samples of freshwater and marine tardigrades, we will be better able to estimate the adaptations of members of the terrestrial group.” Unfortunately, some tardigrades may be particularly elusive, representing a major obstacle to such studies. For example, Tanarctus populus, one of Fleming's favorite tardigrades, is so small that it cannot be seen with the naked eye, and is only found in sediments in the North Atlantic Ocean at depths of about 150 metres. “We hope that large-scale sequencing initiatives through the Earth Biogenome Project will steadily fill this gap in our understanding, and I am excited to see it continue,” Fleming says.

Reference: “Evolution of temperature and drought-related protein families in tardigrades reveals complex acquisition of extreme tolerance” by James F. Fleming, David Pisani, and Kazuharu Arakawa, 29 November 2023, Genome biology and evolution.
doi: 10.1093/jpe/evad217