Tardigrades Give Up Their Secrets

Comparative genomics of the tardigrades Hypsibius dujardini and Ramazzottius varieornatus | PLOS Biology

There is something appealing about a tardigrade! There is a certain air of mystery about them - like, for instance, what on Earth are they?

They are justly famous for their ability to withstand just about any extreme environmental conditions other than extreme heat. They are just a few millimetres long and can withstand years of dehydration, being blown about in dust; they can withstand years of freezing. They can even go into space and withstand ionising radiation. They will live in your guttering through a long, hot dry summer, apparently lifeless, and within a few minutes of it raining, will be crawling about happily as though nothing has happened.

Until this study we weren't even sure where they fitted in with the rest of the animal kingdom. Were they primitive or degenerate arthropods; were they nematode worms with legs or some other distinct multicellular organism on a branch of their own? Well, actually, they are related to both nematodes and arthropods, distantly. The question was which are they closest to? The study doesn't settle the matter but it sheds a lot more light on the subject.

This paper addresses that while not reaching a firm conclusion, but it refutes another idea - that they are some sort of hybrid between animals and bacteria with even maybe a little plant or fungal DNA incorporated for good measure. This idea gained traction a year or so ago when an earlier DNA analysis showed up pieces of DNA from other species. The suggestion was that maybe tardigrades' DNA fragmented when they dried out and them reassembled when they got wet again. Over time, pieces of other dehydrated DNA in the environment, originating in other species that had also adapted to these extreme conditions, had been incorporated in the genome, giving the tardigrade genome a collection of pre-adapted genes for natural selection to select from.

It was a nice idea, but wrong. It is now accepted that that analysis was of contaminated samples. Although there was some evidence of occasional horizontal gene transfer it was nothing like that reported in the earlier paper.

The team also believe they may have solved the mystery of how tardigrade cells survive desiccation. By looking at which genes are turned on during dissication they identified a protein that seems to take the place of water in the cells, helping to preserve the microscopic structures. Other proteins appear to protect the tardigrade's DNA from damage and may help explain how they can withstand radiation.

Abstract
Tardigrada, a phylum of meiofaunal organisms, have been at the center of discussions of the evolution of Metazoa, the biology of survival in extreme environments, and the role of horizontal gene transfer in animal evolution. Tardigrada are placed as sisters to Arthropoda and Onychophora (velvet worms) in the superphylum Panarthropoda by morphological analyses, but many molecular phylogenies fail to recover this relationship. This tension between molecular and morphological understanding may be very revealing of the mode and patterns of evolution of major groups. Limnoterrestrial tardigrades display extreme cryptobiotic abilities, including anhydrobiosis and cryobiosis, as do bdelloid rotifers, nematodes, and other animals of the water film. These extremophile behaviors challenge understanding of normal, aqueous physiology: how does a multicellular organism avoid lethal cellular collapse in the absence of liquid water? Meiofaunal species have been reported to have elevated levels of horizontal gene transfer (HGT) events, but how important this is in evolution, and particularly in the evolution of extremophile physiology, is unclear. To address these questions, we resequenced and reassembled the genome of H. dujardini, a limnoterrestrial tardigrade that can undergo anhydrobiosis only after extensive pre-exposure to drying conditions, and compared it to the genome of R. varieornatus, a related species with tolerance to rapid desiccation. The 2 species had contrasting gene expression responses to anhydrobiosis, with major transcriptional change in H. dujardini but limited regulation in R. varieornatus. We identified few horizontally transferred genes, but some of these were shown to be involved in entry into anhydrobiosis. Whole-genome molecular phylogenies supported a Tardigrada+Nematoda relationship over Tardigrada+Arthropoda, but rare genomic changes tended to support Tardigrada+Arthropoda.

Author summary
Tardigrades are justly famous for their abilities to withstand environmental extremes. Many freshwater and terrestrial species can undergo anhydrobiosis—life without water—and thereby withstand desiccation, freezing, and other insults. We explored the comparative biology of anhydrobiosis in 2 species of tardigrade that differ in the mechanisms they use to enter anhydrobiosis. Using newly assembled and improved genomes, we find that Ramazzottius varieornatus, a species that can withstand rapid desiccation, differs from Hypsibius dujardini, a species that requires extended preconditioning, in not showing a major transcriptional response to anhydrobiosis induction. We identified a number of genetic systems in the tardigrades that likely play conserved, central roles in anhydrobiosis as well as species-unique components. Compared to previous estimates, our improved genomes show much reduced levels of horizontal gene transfer into tardigrade genomes, but some of the identified horizontal gene transfer (HGT) genes appear to be involved in anhydrobiosis. Using the improved genomes, we explored the evolutionary relationships of tardigrades and other molting animals, particularly nematodes and arthropods. We identified conflicting signals between sequence-based analyses, which found a relationship between tardigrades and nematodes, and analyses based on rare genomic changes, which tended to support the traditional tardigrade-arthropod link.

Yoshida Y, Koutsovoulos G, Laetsch DR, Stevens L, Kumar S, Horikawa DD, et al. (2017)
Comparative genomics of the tardigrades Hypsibius dujardini and Ramazzottius varieornatus.
PLoS Biol 15(7): e2002266. DOI: 10.1371/journal.pbio.2002266

© 2017 The authors
Published open access
Reprinted under a Creative Commons Attribution 4.0 International License (CC-BY 4.0)

Physically, especially given their short stubby legs, tardigrades look closer to the arthropods, although their legs are not the typical arthropod jointed legs that give the phylum its name. However the genome more closely resembles that of a nematode, especially in respect of its HOX genes. Most multicellular animals have about ten HOX genes each of which controls the development of part of the embryo. Tardigrades however, have only five - like nematodes - and the five they lack are the same five that nematodes lack.

So, unlikely as it may seem, genetic evidence has swung the pendulum over to the nematode side of the debate.

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