Hydrobiologia (2020) 847:2779–2799 https://doi.org/10.1007/s10750-019-04144-6 (0123456789().,-volV)( 0123456789().,-volV) MEIOFAUNA IN FRESHWATER ECOSYSTEMS Review Paper Extreme-tolerance mechanisms in meiofaunal organisms: a case study with tardigrades, rotifers and nematodes Lorena Rebecchi . Chiara Boschetti . Diane R. Nelson Received: 1 August 2019 / Revised: 20 November 2019 / Accepted: 27 November 2019 / Published online: 16 December 2019 Ó Springer Nature Switzerland AG 2019 Abstract To persist in extreme environments, some environmental conditions. Because of their unique meiofaunal taxa have adopted outstanding resistance resistance, tardigrades and rotifers have been proposed strategies. Recent years have seen increased enthusi- as model organisms in the fields of exobiology and asm for understanding extreme-resistance mecha- space research. They are also increasingly considered nisms evolved by tardigrades, nematodes and in medical research with the hope that their resistance rotifers, such as the capability to tolerate complete mechanisms could be used to improve the tolerance of desiccation and freezing by entering a state of human cells to extreme stress. This review will reversible suspension of metabolism called anhydro- analyse the dormancy strategies in tardigrades, rotifers biosis and cryobiosis, respectively. In contrast, the less and nematodes with emphasis on mechanisms of common phenomenon of diapause, which includes extreme stress tolerance to identify convergent and encystment and cyclomorphosis, is defined by a unique strategies occurring in these distinct groups. suspension of growth and development with a reduc- We also examine the ecological and evolutionary tion in metabolic activity induced by stressful consequences of extreme tolerance by summarizing recent advances in this field. Guest editors: Nabil Majdi, Jenny M. Schmid-Araya Keywords Anhydrobiosis Á Cryptobiosis Á & Walter Traunspurger / Patterns and Processes of Meiofauna in Freshwater Ecosystems Desiccation Á Diapause Á Dormancy Á Encystment L. Rebecchi Department of Life Sciences, Modena and Reggio Emilia University, Modena, Italy Introduction L. Rebecchi (&) Department of Life Sciences, University of Modena and Tardigrades, rotifers and nematodes are considered Reggio Emilia, Via G. Campi 213/D, 41125 Modena, Italy permanent and essential members of freshwater and e-mail: [email protected] terrestrial meiofaunal communities that can undergo C. Boschetti dormancy during their life stages (Rundle et al., 2002; School of Biological and Marine Sciences, University of Hengherr & Schill, 2018; Schill & Hengherr, 2018; Plymouth, Plymouth, UK Bertolani et al., 2019). Tardigrades, commonly called ‘‘water bears’’, are D. R. Nelson Department of Biological Sciences, East Tennessee State micrometazoans categorized into two main classes University, Johnson City, TN, USA 123 2780 Hydrobiologia (2020) 847:2779–2799 (Eutardigrada and Heterotardigrada) with 1298 spe- specific and exceptional resistance and adaptive cies described from marine, freshwater and terrestrial strategies (Fontaneto, 2019). Accordingly, life in these habitats (Degma et al., 2019). The highest number of environments is adapted to a dual existence, flourish- species belongs to the class eutardigrades and to the ing when the habitat contains liquid water, and family Echiniscidae within the heterotardigrades and dormant when liquid water is not available and has been described from terrestrial habitats, where dormant states are linked to a temporary suspension they are inactive unless surrounded by a film of water. of active life with reduction or interruption of The smallest numbers are true limnic species, but metabolism and/or arrested development. Dormancy several species are limnoterrestrial and can colonize includes any form of resting stage, regardless of the both terrestrial and freshwater habitats (Nelson et al., cues required for induction or termination (Hand, 2015). Rotifera, also called ‘‘wheel animals’’, is a 1991;Ca´ceres, 1997). Tardigrades, rotifers and nema- phylum of microscopic metazoans, comprising about todes exhibit both forms of dormancy: quiescence 2000 species (Segers, 2007) traditionally divided in (cryptobiosis) and diapause (encystment, cyclomor- three main classes: (1) Bdelloidea live in freshwater phosis and resting eggs) (e.g. Crowe & Madin, 1975; and terrestrial ephemeral aquatic environments and Ricci, 1987; Guidetti et al., 2011a). only reproduce by apomictic parthenogenesis; (2) Among the various forms of dormancy, cryptobio- Monogononta live in freshwater and marine environ- sis (‘‘hidden life’’, Keilin, 1959) is under exogenous ments and reproduce by cyclical parthenogenesis and control, being directly induced and maintained by (3) Seisonida, with only a few exclusively marine adverse environmental conditions, and it is immedi- species (Ricci, 1987; Wallace & Snell, 1991; Melone ately reversed by the removal of the external stimuli. It et al., 1998; Mark Welch & Meselson, 2000; Ricci & originated independently several times in the history Melone, 2000; Segers, 2007). A fourth class, the of life, as it is present in diverse groups of bacteria, exclusively parasitic Acanthocephala, has recently metazoans, fungi and plants (Clegg, 2001). Crypto- been added, although its exact relationship with the biosis includes different strategies such as anhydro- other taxa is still debated (e.g. Sørensen et al., 2005; biosis, cryobiosis, anoxybiosis and osmobiosis Sielaff et al., 2016). The majority of nematodes, also directly induced by desiccation, sub-zero tempera- called ‘‘roundworms’’, are small free-living animals tures, low oxygen pressure and osmotic extremes, inhabiting the thin layer of water surrounding soil respectively (Keilin, 1959; Wright et al., 1992). particles and in aquatic sediments, although some taxa Cryptobiosis allows tardigrades, rotifers and nema- have become endoparasitic and can reach metres in todes to survive periods of desiccation, whereas few length (Lee, 2002). Some taxa have evolved the ability freshwater and marine species are known to have this to resist desiccation during various stages of their life adaptive strategy (Ricci & Pagani, 1997; Ricci, 1998; cycles (Womersley, 1987; Ricci & Pagani, 1997; Eyres et al., 2015; Guidetti et al., 2011a, b; Clausen Shannon et al., 2005, Erkut et al., 2011). et al., 2014; Møbjerg et al., 2011). Conversely, Tardigrades, rotifers and nematodes are meiofaunal encystment and the production of resting eggs are a aquatic animals common in lakes, rivers, streams and state of diapause controlled by both exogenous and ponds, but paradoxically they are able to colonize and endogenous stimuli and is more common in freshwater persist in desiccation-prone environments, such as and marine species. Although tardigrades, rotifers and freshwater (e.g. temporary ponds, Antarctic lakes, nematodes exhibit both forms of dormancy, there are cryoconite holes) and terrestrial (e.g. mosses and differences among taxa. Tardigrades, as well as lichens) habitats where liquid water is not always insects, can undergo both diapause (encystment and available (Rundle et al., 2002; Nelson et al., cyclomorphosis) (Guidetti & Møbjerg, 2019) and the 2015, 2018). In these habitats, water loss can occur production of resting eggs (Hansen & Katholm, 2002; via evaporation or freezing, with diel, seasonal, annual Altiero et al., 2010). In comparison, in rotifers the two or longer fluctuations in the duration of the wet phase. main types of dormancy are restricted to two separate Since tardigrades, rotifers and nematodes are inca- taxa. The class Bdelloidea can resist adverse environ- pable of active migration to more suitable habitats, mental conditions via quiescence and directly respond occupancy of these unpredictable habitats requires to environmental stimuli at any life stage, from eggs to organisms to be versatile, tolerant or to possess adults, although with age-dependent degrees of 123 Hydrobiologia (2020) 847:2779–2799 2781 resistance (Ricci, 1987, 1998;O¨ rstan, 1995, 1998), In response to the gradual onset of adverse envi- while the other main class, the Monogononta, only ronmental conditions (e.g. temperature, oxygen ten- engage in diapause via the production of resting eggs, sion, pH), encystment in tardigrades begins with the which tend to stop at a specific and common devel- ejection of the sclerified parts of the buccal-pharyn- opmental stage and are generally very resistant to geal apparatus (‘‘simplex stage’’). Instead of under- various environmental stresses, including desiccation going normal ecdysis, however, one to three new (e.g. Balompapueng et al., 1997;Ca´ceres, 1997; cuticles are serially produced in addition to the Schro¨der, 2005; Garcı´a-Roger et al., 2006, Boschetti retained external (old) cuticle (Fig. 1). The animal’s et al., 2010, Ziv et al., 2017). Within nematodes, size is reduced by longitudinal contraction, body dormancy is more scattered across taxa. For example movements cease completely, metabolism is signifi- some genera or species can survive desiccation (e.g. cantly reduced and the mouth and cloaca are closed. Wharton, 1996; Tyson et al., 2012), while other Modified claws and buccal-pharyngeal apparatus are species only have limited resistance at specific life synthesized, but non-functional. At this stage, the cyst stages (e.g. Erkut et al., 2011; Erkut & Kurzchalia, resembles an onion or a Russian doll (‘‘Matryoshka’’) 2015). (Guidetti et al., 2006), often with one cuticle becoming