Yoshida Yuki, Koutsovoulos Georgios, Laetsch Dominik R, Stevens Lewis, Kumar Sujai, Horikawa Daiki D, Ishino Kyoko, Komine Shiori, Kunieda Takekazu, Tomita Masaru, Blaxter Mark, Arakawa Kazuharu
Institute for Advanced Biosciences, Keio University, Tsuruoka, Yamagata, Japan.
Systems Biology Program, Graduate School of Media and Governance, Keio University, Kanagawa, Japan.
PLoS Biol. 2017 Jul 27;15(7):e2002266. doi: 10.1371/journal.pbio.2002266. eCollection 2017 Jul.
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.
缓步动物门是一类小型底栖生物，一直处于后生动物进化、极端环境下的生存生物学以及水平基因转移在动物进化中的作用等讨论的核心。通过形态学分析，缓步动物门在泛节肢动物超门中被置于节肢动物门和有爪动物门（天鹅绒虫）的姐妹位置，但许多分子系统发育分析未能恢复这种关系。分子与形态学理解之间的这种矛盾可能对主要类群的进化模式具有重要启示。淡水陆生缓步动物具有极端的隐生能力，包括脱水隐生和低温隐生，蛭形轮虫、线虫以及其他生活在水膜中的动物也是如此。这些极端嗜极生物行为挑战了对正常水生生理学的理解：多细胞生物如何在没有液态水的情况下避免致命的细胞崩溃？据报道，小型底栖生物物种的水平基因转移（HGT）事件水平较高，但这在进化中，尤其是在极端嗜极生物生理学的进化中究竟有多重要尚不清楚。为了解决这些问题，我们对杜氏高生熊虫（一种淡水陆生缓步动物，只有在长时间预先暴露于干燥条件下才能进行脱水隐生）的基因组进行了重测序和重新组装，并将其与变异高生熊虫（一种对快速脱水具有耐受性的相关物种）的基因组进行了比较。这两个物种对脱水隐生具有截然不同的基因表达反应，杜氏高生熊虫有主要的转录变化，而变异高生熊虫的调控有限。我们鉴定出很少的水平转移基因，但其中一些被证明与进入脱水隐生有关。全基因组分子系统发育分析支持缓步动物门与线虫门的关系，而非缓步动物门与节肢动物门的关系，但罕见的基因组变化倾向于支持缓步动物门与节肢动物门的关系。
