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18
Features
August 2008 © 2008 The Biochemical Society
Water
Key words: anhydrobiosis,
cryptobiosis, tardigrade,
trehalose, vitrication
Tardigrades and anhydrobiosis
Water bears and water loss
The Phylum Tardigrada consists of about 900 known species of microscopic animals that are often
referred to by their endearing popular names, water bears or moss piglets (translated from the
German expressions Wasser Bär and Mooschweinchen). The group is considered a sister group to the
arthropods, with animals typically less than 0.5 mm in length1. As tardigrades are of no direct medi‑
cal or agricultural importance, their study is conned to a small, but highly productive, international
community of researchers.
Animal and Plant Kingdoms. Typically they occur at set
stages in the life cycle of the organisms, particularly the
seeds of various owering plants and the resistant eggs
of animal species such as tapeworms and brine shrimps.
However, in tardigrades, the latent state can occur at any
stage of the life cycle (egg or adult) and on repeated oc‑
casions. eir ability to employ latent states (in which
metabolism is virtually undetectable) has been a noted
feature of tardigrade biology since the animals were rst
observed by the pioneering microscopists of the 18th
Century6. is has been one of the enduring attractions
of tardigrades as an object of study, leading early observ‑
ers to describe tardigrades as exhibiting ‘resurrection’1.
More recently, it has been asked, if specimens failed to
emerge from dormancy, was it because they died while
they were dead?7 Excitement over the remarkable physi‑
ology of these animals has, however, resulted in some
claims that may have been a little exaggerated and given
rise to sensational journalism8. Such overenthusiastic
claims include suggestions that tardigrades could sur‑
vive space travel; be transported around the globe in
high‑level wind currents or survive desiccation for peri‑
ods in excess of a century. However, it appears that hard
Tardigrades are oen a favourite of the amateur micro‑
scopist as they are so easy to nd and rewarding to observe.
eir slow lumbering gait (tardi=slow, grado=walker) is
not only amusing to watch, but also makes their move‑
ments easy to track under the microscope. Many of the
species are more or less transparent, so the inner work‑
ings of the intricate buccal apparatus and the transition
of the food through the gut can be observed without
requiring any special preparation. Other species are
bright orange (Figure 1), carrying an intricate arrange‑
ment of dorsal armour plating (Figure 2).
e paradox of their biology is that, although all tar‑
digrades are strictly aquatic (needing to be surrounded
by water to support their activities), those occupying
terrestrial habitats account for the bulk of species within
the group. Tardigrades feature among the fauna found
in a variety of habitats where water is oen scarce2. Suit‑
able habitats need to hold temporary water lms. It is the
thickness of this water lm that appears to be important
in aiding tardigrade locomotion over the substratum3. A
thin water lm presses the tardigrade’s body close to the
substratum and allows the claws to gain purchase and
move the animal along. When the microhabitat is satu‑
rated, the animals can lose this purchase and dri un‑
controllably in the water. Suitable microhabitats include
lichens, leaf axils of some plants, soils and sediments,
and most famously moss cushions4. Whether the mosses
are growing in urban environments (roofs and walls) or
natural environments (rock surfaces or tree bark), they
are typically subjected to repeated episodes of desicca‑
tion and rehydration. e tardigrades cope with this by
entering a state of suspended animation during dry peri‑
ods. is is a characteristic that has a signicant impact
on the ecology of tardigrades1,5 and is shared with other
animals inhabiting these microenvironments, including
nematodes and rotifers.
Latent or dormant states are quite common in the
Ian M. Kinchin (King’s College London)
Figure 1. Fresh specimen of Echiniscus granulatus (Tardi‑
grada) showing the natural orange colouration of this spe‑
cies. The animal’s body length is 350 µm. (Photo by author.)
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19
Features
August 2008 © 2008 The Biochemical Society
Water
Water bears and water loss
evidence to support such claims is conspicuously absent.
Even so, when tardigrades are in dormant states, they
exhibit increased resistance to environmental extremes
(such as cold, heat, drought and ionizing radiation), al‑
lowing them to colonize habitats that would be too hos‑
tile and unpredictable for most aquatic animals.
Although tardigrades can enter various latent states
(cryptobiosis) that are triggered by adverse changes in
various environmental factors, including temperature
(cryobiosis), salinity (osmobiosis) and oxygen (anoxy‑
biosis), it is the response to the removal of water (anhydro‑
biosis) that has more oen been the focus of study.
Various factors inuence the eectiveness of anhydro‑
biosis by promoting a low rate of drying that is crucial
for the animals to survive the experience. Lowering the
rate of desiccation facilitates a metabolic preparatory
stage during which the animals undergo anatomical and
metabolic adjustments that are required for them to suc‑
cessfully see through periods of drought when activity is
not possible.
First, the nature of the surrounding microhabitat can
help to control the rate of water loss. Moss cushions have
their own adaptations to water loss (including the curl‑
ing of leaves as they dry), providing ideal microenviron‑
ments for the resident fauna. Other microhabitats such
as soils tend to dry unevenly, resulting in the encapsula‑
tion of animals in small pockets of water. It has also been
reported that tardigrades exhibit clumping behaviour to
retard water loss1, although it is not clear whether the
patterns observed are merely the results of tardigrades
being trapped together in receding water lms.
e most obvious anatomical feature of desiccated
tardigrades is the way they fold up with the result of re‑
ducing the exposed surface area. is is described as tun
formation. e animals undergo considerable longitudi‑
nal contraction that is facilitated by regions of thinner
cuticle across the dorsum, allowing folds in the skin. e
legs are also withdrawn into the body.
e adult animals are not the only focus of interest
in tardigrade biology. e complexity of tardigrade egg
shells is presumed to be a factor in their survival (Figure
3). e function of the elaborate ornamentation that is a
feature of the eggs of so many species is not really under‑
stood, but a number of hypotheses have been suggested1.
e projections on the surface may help maintain the
egg’s position within an unstable substratum or they may
Figure 2. Echiniscus madonnae scanning electron photomicrograph ©Lukasz Michalczyk and
Lukasz Kaczmarek (www.tardigrada.net).
Figure 3. Egg of Macrobiotus magdalenae scanning electron photomicrograph ©Lukasz
Michalczyk and Lukasz Kaczmarek (www.tardigrada.net).
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Features
August 2008 © 2008 The Biochemical Society
Water
help to avoid predation by preventing penetration by the stylets of predatory nema‑
todes. Alternatively, the ornamentation may have a role in the control of water loss by
trapping pockets of water between the projections.
Tardigrades achieve a degree of dehydration that not only involves the loss of free
water forming the aqueous solutions of the body, but also the loss of bound water, which
is required to maintain the structure of vital hydrated macromolecules such as proteins,
membrane phospholipids and nucleic acids. e problem for anhydrobiotic tardigrades
is to maintain structural integrity while simultaneously removing the water. Destruc‑
tion of these hydrated macromolecules would cause irreversible damage and result
in death. e bound water is replaced by compounds to maintain structural integrity
during dehydration and which are easily removed during rehydration. Non‑reducing
sugars, such as trehalose, have been identied in high concentrations in anhydrobiotic
animals, performing a protective role in tardigrades9,10.
Various hypotheses for the mechanism of membrane protection mediated by
sugars such as trehalose have been developed9. In the water‑replacement model, the
central argument is that the hydroxy groups within the trehalose molecule (Figure 4)
form hydrogen bonds with polar surfaces on cellular membranes to replace the lost
water. is then inhibits the structural deformations that would normally accompany
dehydration. Other hypotheses consider the entrapment of water by sugar molecules
aggregating at water surfaces and the vitrication of tissues (trehalose can form an
amorphous glass upon dehydration) in which structural deformations would be mini‑
mized. ere is probably a combination of these eects at work to protect the tissues
from damage and degradation in the anhydrobiotic organism9.
Observations on tardigrades and nematodes (in which the process of anhydro‑
biosis appears to have developed in a similar manner, as an example of convergent
evolution) suggest that anhydrobiotic success is related to the nutritional health of the
animals, particularly the possession of adequate lipid reserves that, in tardigrades, are
stored in free‑oating body cavity cells. e anatomic and metabolic preparations for
anhydrobiosis consume a considerable amount of energy and so, although tardigrades
can successfully undergo repeated episodes of dehydration, they need sucient time
in between to feed and build up their food reserves. e
lipids in the body cavity cells serve a number of func‑
tions, including the maintenance of spatial distribution
of the tissues in the shrunken animals to prevent reac‑
tions between molecules that are usually separated in the
active animals as well as providing a reserve from which
trehalose (and other membrane‑protectant chemicals)
are synthesized. ose animals which apparently fail to
remove all of their water appear to succumb to a variety
of fungal infections upon rehydration of the surround‑
ing environment1.
Although there has been considerable research un‑
dertaken to reveal the secrets of anhydrobiosis in tardi‑
grades over the last 40 years, there are still gaps in our
understanding of the process. Understanding the details
of molecular interactions that facilitate the tolerance to
the stresses exerted by extreme water loss is of interest
not only to those studying the ecology and physiology of
tardigrades, but also for the fundamental understanding
of the importance of water to biology in general, and the
eld of biostabilization11 in particular. e promise of this
eld in the future, and the real possibility of employing
trehalose for the stabilization of macromolecules, cells
and tissues for medical benets seems a million miles
away from Antonie van Leeuwenhoek and his peers
marvelling at the little animalcules they could observe in
water droplets, showing that you can never tell where an
interest in natural history may lead. ■
Many thanks to Lukasz Michalczyk and Lukasz Kaczmarek
for the photographs in Figures 2 and 3.
Ian Kinchin gained his rst degree in
biological sciences and followed this with
a Masters thesis on the ultrastructure
and taxonomy of tardigrades. He taught
biology at various levels for nearly 20 years
before moving into teacher education.
He gained a PhD in science education and currently works as
a senior lec turer in higher education within King’s Institute of
Learning and Teaching at King’s College London, where he
supports the development of teaching skills among university
lecturers. email: ian.kinchin@kcl.ac.uk
References
1. Kinchin, I.M. (1994) The Biology of Tardigrades, Portland Press, London
2. Williams, D.D. (1987) The Ecology of Temporary Waters, Croom Helm,
London
3. Greven, H. and Schüttler, L. (2001) Zool. Anz. 240, 341–344
4. Kinchin, I.M. (1995) Biologist 42, 166–170
5. Wright, J.C., Westh, P. and Ramløv, H. (1992) Biol. Rev. Cambridge Philos.
Soc. 67, 1–29
6. Wright, J.C. (2001) Zool. Anz. 240, 563–582
7. Crowe, J.H. (1975) Mem. Ist. Ital. Idrobiol. Dott. Marco de Marchi 32
(Suppl.), 37–59
8. Jönsson, K.I. and Bertolani, R. (2001) J. Zool. 255, 121–123
9. Crowe, J.H. (2007) Adv. Exp. Med. Biol. 594, 143–158
10. Hengherr, S., Heyer, A.G., Köhler, H.‑R. and Schill, R.O. (2008) FEBS J. 275,
281–288
11. Hightower, L. (2000) Cell Stress Chaperones 5, 161–162
CH2OH
HOH2C
⋅ 2H2O
O
O
O
H
HOH
OH
OH OH
H
HH
H
H
HOH
H
HO
Figure 4. The structural formula of the non‑reducing disaccharide, trehalose. One of a suite of
compounds described as compatible solutes or osmolytes that confer tolerance to dehydration
of living tissues.
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