Tardigrades, also known as water bears, can tolerate high doses of radiation, low-oxygen environments, desiccation, and both high and low temperatures under a dormant state called anhydrobiosis, which is a reversible halt of metabolism upon almost complete desiccation. A large amount of research has focused on the genetic pathways related to these capabilities, and a number of genes have been identified and linked to the extremotolerant response of tardigrades. However, the history of these genes is unclear, and the origins and history of extremotolerant genes within tardigrades remain a mystery. In new research, scientists from Keio University, the University of Oslo and the University of Bristol generated the first phylogenies of six separate protein families linked with desiccation and radiation tolerance in tardigrades.
A photograph of the tardigrade Ramazzottius varieornatus, in the center of a phylogeny of CAHS, the largest of the six desiccation-related protein families analyzed by Fleming et al. Image credit: Kazuharu Arakawa, Keio Institute of Advanced Biosciences.
As one form of extremotolerance, tardigrades can survive almost complete desiccation by entering a dormant state called anhydrobiosis (i.e., life without water), which allows them to reversibly halt their metabolism.
Multiple tardigrade-specific gene families were previously found to be associated with this state.
Three of these gene families are referred to as cytosolic, mitochondrial, and secretory abundant heat soluble proteins (CAHS, MAHS, and SAHS, respectively) based on the cellular location in which the proteins are expressed.
Some tardigrade species appear to possess a variant pathway that involves two families of abundant heat soluble proteins first identified in the tardigrade Echiniscus testudo and usually referred to as EtAHS alpha and beta.
Tardigrades also possess stress resistance genes that can be found in animals more broadly, such as the meiotic recombination 11 (MRE11) gene, which has been implicated in desiccation 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 on their origins, history, and ecological implications.
To shed light on the evolution of tardigrade extremotolerance, lead author Dr. James Fleming and his colleagues identified sequences from these six gene families across 13 tardigrade genera, including representatives from both of the major tardigrade lineages, the Eutardigrada and Heterotardigrada.
Their analysis revealed 74 CAHS, 8 MAHS, 29 SAHS, 22 EtAHS alpha, 18 EtAHS beta, and 21 MRE11 sequences, allowing them to build the first tardigrade phylogenies for these gene families.
As resistance to desiccation is likely to have emerged as an adaptation to terrestrial environments, the researchers assumed that they would find a link between gene duplications and losses in these gene families and habitat changes within tardigrades.
“When we began the work, we expected to find that each clade would be clearly grouped around ancient duplications, with few independent losses,” Dr. Fleming said.
“That would help us easily tie them to an understanding of modern habitats and ecology.”
“It’s an intuitive hypothesis that the evolution of the 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 overly simplistic.”
Instead, the authors were surprised by the sheer number of independent duplications of heat-soluble genes, which painted a much more complex picture of anhydrobiosis-related gene evolution.
Notably, however, there was no clear link between strongly anhydrobiotic species and the number of anhydrobiosis-related genes a species possessed.
“What we found was far more exciting — a complex network of independent gains and losses that does not necessarily correlate to modern terrestrial species ecologies,” Dr. Fleming said.
The distinct distributions of gene families across the two major groups of tardigrades — CAHS, MAHS, and SAHS in the Eutardigrades and EtAHS alpha and beta in the Heterotardigrades — suggest that two independent transitions from marine to limno-terrestrial environments occurred within tardigrades, once in the Eutardigrade ancestor and once within the Heterotardigrades.
This research marks a significant step forward in our understanding of the evolution of anhydrobiosis in tardigrades.
It also provides a foundation for future studies into tardigrade extremotolerance, which will require the continued development of genomic resources from more diverse tardigrade lineages.
“We unfortunately have no representatives from several important families, such as the Isohypsibiidae, and this does limit how firmly we can stand by our conclusions,” Dr. Fleming said.
“With more freshwater and marine tardigrade samples, we will be better able to appreciate the adaptations of terrestrial members of the group.”
The results appear in the journal Genome Biology and Evolution.
_____
James F. Fleming et al. 2024. The Evolution of Temperature and Desiccation-Related Protein Families in Tardigrada Reveals a Complex Acquisition of Extremotolerance. Genome Biology and Evolution 16 (1): evad217; doi: 10.1093/gbe/evad217
Source : Breaking Science News