Anhydrobiosis and freezing-tolerance: adaptations that facilitate the establishment of Panagrolaimus nematodes in polar habitats.
Anhydrobiotic animals can survive the loss of both free and bound water from their cells. While in this state they are also resistant to freezing. This physiology adapts anhydrobiotes to harsh environments and it aids their dispersal. Panagrolaimus davidi, a bacterial feeding anhydrobiotic nematode isolated from Ross Island Antarctica, can survive intracellular ice formation when fully hydrated. A capacity to survive freezing while fully hydrated has also been observed in some other Antarctic nematodes. We experimentally determined the anhydrobiotic and freezing-tolerance phenotypes of 24 Panagrolaimus strains from tropical, temperate, continental and polar habitats and we analysed their phylogenetic relationships. We found that several other Panagrolaimus isolates can also survive freezing when fully hydrated and that tissue extracts from these freezing-tolerant nematodes can inhibit the growth of ice crystals. We show that P. davidi belongs to a clade of anhydrobiotic and freezing-tolerant panagrolaimids containing strains from temperate and continental regions and that P. superbus, an early colonizer at Surtsey island, Iceland after its volcanic formation, is closely related to a species from Pennsylvania, USA. Ancestral state reconstructions show that anhydrobiosis evolved deep in the phylogeny of Panagrolaimus. The early-diverging Panagrolaimus lineages are strongly anhydrobiotic but weakly freezing-tolerant, suggesting that freezing tolerance is most likely a derived trait. The common ancestors of the davidi and the superbus clades were anhydrobiotic and also possessed robust freezing tolerance, along with a capacity to inhibit the growth and recrystallization of ice crystals. Unlike other endemic Antarctic nematodes, the life history traits of P. davidi do not show evidence of an evolved response to polar conditions. Thus we suggest that the colonization of Antarctica by P. davidi and of Surtsey by P. superbus may be examples of recent "ecological fitting" of freezing-tolerant anhydrobiotic propagules to the respective abiotic conditions in Ross Island and Surtsey.
Department of Biology, Maynooth University, Maynooth, Co Kildare, Ireland.
Lorraine M
LM
McGill
Department of Biology, Maynooth University, Maynooth, Co Kildare, Ireland; Technology Sciences Group Europe LLP, Concordia House, St James Business Park, Knaresborough, North Yorkshire, HG5 8QB, United Kingdom.
Adam J
AJ
Shannon
School of Biological Sciences and School of Earth Sciences, University of Bristol, Woodland Road, BS8 1UG, Bristol, United Kingdom.
Davide
D
Pisani
Institute of Biology of the Ecole Normale Supérieure, 46 rue d'Ulm, 75230 Paris cedex 05, France.
Marie-Anne
MA
Félix
Department of Science, Systems and Models, Roskilde University, Universitetsvej 1, P.O.Box 260, DK-4000 Roskilde, Denmark.
Hans
H
Ramløv
Department of Biology, Maynooth University, Maynooth, Co Kildare, Ireland.
Ilona
I
Dix
Department of Zoology, University of Otago, PO Box 56, Dunedin 9054, New Zealand.
David A
DA
Wharton
Department of Biology, Maynooth University, Maynooth, Co Kildare, Ireland.
Ann M
AM
Burnell
D000222:Adaptation, Physiological; D000818:Animals; D001110:Arctic Regions; D005615:Freezing; D007055:Iceland; D009348:Nematoda / Q000145:classification / Q000502:physiology*; D010802:Phylogeny; D025341:Principal Component Analysis