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The Tardigrade Ramazzottius Varieornatus As a Model Animal for Astrobiological Studies

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The Tardigrade Ramazzottius Varieornatus As a Model Animal for Astrobiological Studies Biological Sciences in Space, Vol.22 No.3 (2008): 93-98Horikawa, D.D. © 2008 Jpn. Soc. Biol. Sci. Space The Tardigrade Ramazzottius varieornatus as a Model Animal for Astrobiological Studies Daiki D. Horikawa1, 2, 3† 1 NASA Ames Research Center, Moffett Field, CA 94035, USA 2 SETI Institute, 515 N. Whisman Road - Mountain View, CA 94043, USA 3 NASA Astrobiology Institute Abstract Tardigrades are invertebrate animals, some of which can enter into an ametabolic desiccated state called anhydrobiosis. In this state, tardigrades are extremotolerant and able to survive open space environments characterized by severe vacuum and intense radiation. For these reasons, tardigrades are expected to serve as important model organisms for astrobiological studies, particularly those focusing on how multicellular organisms can withstand the extreme environments of space and the possibility of extraterrestrial multicellular life forms. To develop tardigrades as model organisms, we established a culture system for the tardigrade species Ramazzottius varieornatus, a species that is tolerant to several types of extreme physical and chemical environmental conditions while in an anhydrobiotic, or “tun”, state. Based on studies using this culture system and the extremotolerance of this tardigrade in connection with its anhydrobiotic capacity, R. varieornatus is a suitable model organism for astrobiological studies and will provide new insight into the mechanisms underlying the ability of multicellular organisms to tolerate extreme environments. Key words: tardigrades, Ramazzottius varieornatus, anhydrobiosis, astrobiology, extremophiles Introduction probabilities of interplanetary transfer and the existence A major goal in the field of astrobiology is to of extraterrestrial multicellular organisms. determine whether life can be transferred from one Tardigrades are a classic example of extremotolerant planet to another or if life can potentially exist elsewhere multicellular organisms, exhibiting considerable in the universe. Evaluation of an organism’s survivability resistance to many environmental extremes (Rothschild after exposure to open-space environments is important and Mancinelli, 2001; Cavicchioli, 2002). Tardigrades to estimate the possibilities of transportation of life are small invertebrates (0.1–1.0 mm in body length) between planets and the existence of extraterrestrial found in environments ranging from the deep sea to high life. In contrast to unicellular organisms (Horneck et al., mountains all over the world. Even terrestrial tardigrades, 1994; Kobayashi et al., 2000), the use of multicellular however, require a film of water surrounding them for organisms for space exposure experiments has received activities such as feeding, growth, and reproduction. little attention, presumably because there are few species When the terrestrial species lack water, their body water with potential tolerance to actual space environmental characteristically decreases to between 1% to 3% wt/ parameters, including extremely high or low wt in association with body shrinkage (Crowe, 1972; temperatures, vacuum, and ultraviolet (UV) and ionizing Horikawa et al., 2006). The contracted dry animal, radiation. Some multicellular species, however, show referred to as a tun, shows no visible signs of life, but high resistance to extreme environmental conditions, can resume activity within 1 h (Horikawa and Higashi and therefore flight experiments with multicellular 2004) when placed in a drop of water. This ametabolic organisms are of great interest for estimating the state induced by dehydration is referred as anhydrobiosis existence of complex life forms on other planets, as (Keilin, 1959). Tardigrades in an anhydrobiotic state well as the existence of simple single-cell life-forms. exhibit extraordinary tolerance to a variety of extreme Such investigation might provide new insights into the environmental conditions, such as a wide range of temperatures from –273˚C (Becquerel, 1950) to 151˚C (Rahm, 1921); exposure to organic solvents such as –4 Article ID: 08220309 alcohols (Ramløv and Westh, 2001); vacuum (5 × 10 Pa) (Utsugi and Noda, 1995); high pressure (600 MPa) Review Article (Seki and Toyoshima, 1998); and thousands Gy of X-rays Received: December 17, 2008 (May et al., 1964), gamma-rays (Horikawa et al., 2006; Accepted: February 10, 2009 Jönsson, et al., 2005), and heavy ions (Horikawa, 2006). †To whom correspondence should be addressed: NASA Based on these characteristics, several investigators have Ames Research Center, Mail Stop 239-20, Bldg N239 Rm suggested that tardigrades have the potential to survive 377, Moffett Field, CA 94035, USA. Tel: +1-650-604- extraterrestrial environments (Copley, 1999). 6165; Fax: +1-650-604-1088; E-mail: Daiki.Horikawa-1@ nasa.gov The tardigrades Richtersius coronifer and Milnesium 93 Model Multicellular Organism for Astrobiological Studies tardigradum in an anhydrobiotic state were exposed to To date, however, there have been few reports on open-space environments in a low Earth orbit for 10 d tardigrade culture conditions that will allow for stable within the Biopan 6 research facility operated by the and continuous tardigrade research. To further develop European Space Agency and a few individuals of the tardigrades as a model for astrobiological studies, we M. tardigradum survived exposure to a combination of recently established culture systems for the tardigrade space vacuum and the full spectral range of UV radiation species Ramazzottius varieornatus using a green alga, (Jönsson et al., 2008), indicating the potential of these Chlorella vulgaris, as food (Horikawa et al., 2008). Our multicellular organisms to survive unprotected space findings indicate that this species has high anhydrobiotic travel. These findings have prompted researchers to focus ability and is tolerant to several types of extreme on tardigrades for astrobiological studies. Elucidation environmental conditions (Horikawa et al., 2008). Here, of the mechanisms underlying the tardigrade’s tolerance I review the culture systems, life history, anhydrobiosis, to extreme environmental conditions may provide and environmental tolerance of R. varieornatus and information about potential survival strategies of propose that this species, particularly among tardigrades, multicellular organisms in extraterrestrial environments. is a suitable model animal for astrobiological studies. Fig. 1. A natural habitat of . (A) The landscape of the bridge in Sapporo, Hokkaido, Japan, and (B) dry moss vegetation where inhabits the pavement of the bridge. Fig. 2. Light micrographs of (A) an adult of and (B) adults reared on a culture plate with the green algae (green material). The arrowheads indicate eggs produced. Scale bar = 100 µm (A). 94 Horikawa, D.D. Culture systems and life history of R. varieornatus There are several possible molecular protectants R. varieornatus, originally collected from the dry involved in stabilizing macromolecules and cells involved moss vegetation on a bridge in Sapporo, Japan, was in anhydrobiosis in R.varieornatus. The disaccharide cultured with the green alga C. vulgaris (Chlorella trehalose is considered to be a desiccation protectant that Industry Co., Ltd., Tokyo, Japan) as food (Horikawa generally accumulates during entry into anhydrobiosis et al., 2008)(Fig. 1A, B; Fig.2 A). Agar gel was coated in anhydrobiotic invertebrates (reviewed by Watanabe onto the bottom of a Petri dish (35 mm in diameter) as 2006), including several species of tardigrades (Westh a culture medium with a thin layer of water covering & Ramløv 1991, Hengherr et al., 2008), but whether the agar. A culture dish containing approximately 60 trehalose accumulates in R. varieornatus is unknown. individuals was covered with a lid to inhibit water The kinds of protectants responsible for successful evaporation and kept at 25˚C in the dark. Tardigrades anhydrobiosis in R. varieornatus is one of the most were transferred to new culture dishes every 3 to 6 d. interesting features to address in further tardigrade When tardigrades were transferred to new culture dishes, research. In view of their relatively high desiccation they were anesthetized by pouring CO2–dissolved water tolerance, this species is expected to contribute to studies into the culture dish, picked up using a pipette, and then of desiccation tolerance in multicellular organisms. transferred to new culture dishes. Fresh C. vulgaris was added to the culture dishes each time the tardigrades Tolerance of R. varieornatus to extreme were transferred. environmental conditions Under the culture conditions described, the average Previous evaluation of the tolerance of R. varieornatus life span of R. varieornatus was approximately 35 d, to extreme physical and chemical environmental and the maximum life span was 87 d (Horikawa et conditions indicated that high proportion (greater than al., 2008). The average number of eggs produced by a 85%) of anhydrobiotic adults of R. varieornatus resumed single individual was 7.85, and the first egg laying was activity after exposure to 90˚C, –196˚C, 4000 Gy of 4He observed 9 d after hatching (Horikawa et al., 2008). ions, or 99.8% acetonitrile (Horikawa et al., 2008)(Fig. 4). Of the eggs produced, 83% hatched, and the average While no hydrated individuals survived exposure to 90˚C embryonic stage was 5.7 d (Horikawa et al., 2008). R. and 99.8% acetonitrile, 22.3% of them survived freezing varieornatus has a shorter life span and embryonic stage at –196˚C for 15 min,
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