Comparative genomics of the tardigrades Hypsibius dujardini and Ramazzottius varieornatus

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.

Too Much Eukaryote LGT

“…Other animals and other eukaryotes are regularly reported to have 1–2% LGT in their genomes based on what appear to be widely accepted analytical tools. My point is this: If eukaryote LGT is occurring in nature at a rate that leads to an LGT content of 1–2% per genome, where are the cumulative effects? Why does it not accrue along lineages?…”

Demystifying Eukaryote Lateral Gene Transfer (Response to Martin 2017 DOI: 10.1002/bies.201700115)

“…A key pillar of Martin's argument is that the rate of eukaryote LGTs into specific lineages cannot be as high as estimated, otherwise the cumulative effects of these LGTs should be significant and readily detectable. To illustrate this point, Martin discusses LGTs inferred in the genomes of 12 Drosophila species by Yoshida et al He argues their estimates of LGT are too high, stating: “I find claims of 0.5% LGT per fly genome very difficult to digest.” However, Yoshida et al never made any such claim. They estimated LGT by flagging genes in a given Drosophila genome that displayed substantially greater similarity to non‐metazoan versus metazoan homologs.…”

Desiccation Does Not Drastically Increase the Accessibility of Foreign DNA to the Nuclear Genomes: Evidence from the Frequency of Endosymbiotic DNA Transfer

“…The DSBs induced by prolonged desiccation were suggested to open the "gateway to genetic exchange" and account for the elevated HGT frequency in bdelloid rotifers Boschetti, et al 2012;Flot, et al 2013;Hespeels, et al 2014;Eyres, et al 2015;Debortoli, et al 2016). However, the DSBs induced by prolonged desiccation in tardigrades (Neumann, et al 2009) did not result in an elevated level of HGTs (Yoshida, et al 2017). We first examine whether there are elevated levels of endosymbiotic DNA transfers (EDTs) in the desiccation-tolerant bdelloid rotifers and tardigrades.…”

“…The first analysis of a tardigrade draft genome (Hypsibius dujardini) suggested more extensive HGTs than bdelloid rotifers, 17.5% of its genes were identified as foreign genes originated from bacteria, plants, fungi, and archaea (Boothby, et al 2015). However, subsequent independent sequencing of the same species as well as another tardigrade species, Ramazzottius varieornatus, consistently showed that the percentage of foreign genes in tardigrades is much lower, with 2.3% as the reported upper bound (Arakawa 2016;Bemm, et al 2016;Delmont and Eren 2016;Hashimoto, et al 2016;Koutsovoulos, et al 2016;Yoshida, et al 2017). Most previously identified foreign genes should result from contamination of DNA from non-target organisms.…”

“…Most previously identified foreign genes should result from contamination of DNA from non-target organisms. Accordingly, tardigrades should not be regarded as a special group of animals with elevated levels of HGT (Yoshida, et al 2017).…”