Anhydrobiosis and Freezing-Tolerance: Adaptations That Facilitate the Establishment of Panagrolaimus Nematodes in Polar Habitats

Abstract

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.

Decoupled responses of soil bacteria and their invertebrate consumer to warming, but not freeze–thaw cycles, in the Antarctic Dry Valleys

“…Samples were collected during January 2014, midway through the summer and gradually frozen to À20°C before transportation and long-term storage. Thus, all nematodes in this study were subjected to a shortened growing season and long period (> 16 months) of freezing and probable cryoprotective dehydration (McGill et al 2015) prior to the beginning of the experiment. The proportion of dead individuals at the beginning of our experiment was 30%, the proportion measured immediately after sampling in the field (i.e.…”

The ability to survive intracellular freezing in nematodes is related to the pattern and distribution of ice formed

“…The freezing survival of P. murrayi is intermediate between these two species and has only weak recrystallization inhibition activity (Wharton and Raymond, 2015). Several other Panagrolaimus species and strains can survive freezing, and extracts of these also inhibit recrystallization in a splat freezing assay and the growth of single crystals in a nanolitre osmometer (McGill et al, 2015). It seems likely that it is an ice active substance with recrystallization inhibition activity that is responsible for controlling the size of the ice spaces and that this is an important adaptation for the ability of some nematodes to survive intracellular freezing.…”

Staying young and fit? Ontogenetic and phylogenetic consequences of animal anhydrobiosis

“…These conditions include chemical and physical extremes, such as very low and very high temperatures (from absolute zero to more than 150°C), long drying periods (for hundreds of years), high levels of chemicals (like carbon dioxide, hydrogen sulfide, ethanol, 1‐hexanol, or the biocide methyl bromide gas), low and very high hydrostatic pressures, and very high doses of UV, X‐ray, γ‐ray, and heavy ionic radiation (see e.g. Hartman et al ., ; Clegg, ; Watanabe, ; Gladyshev & Meselson, ; Ono et al ., ; Rebecchi et al ., ; Altiero et al ., ; Guidetti et al ., ; Piscia et al ., ; Wharton, ; McGill et al ., ).…”