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Anhydrobiosis and freezing-tolerance: adaptations that facilitate the establishment of Panagrolaimus nematodes in polar habitats.

McGill LM, Shannon AJ, Pisani D, Félix MA, Ramløv H, Dix I, Wharton DA, Burnell AM - PLoS ONE (2015)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Maynooth University, Maynooth, Co Kildare, Ireland.

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.

No MeSH data available.


Related in: MedlinePlus

Maximum likelihood ancestral state reconstructions of freezing-tolerant phenotypes of (a) non-acclimated and (b) cold-acclimated Panagrolaimus species and strains, under the assumption that all transition rates are equal and branch lengths are proportional to time.At each node a pie chart represents the proportional (0–1) likelihood of each ancestral character state, coloured as in the key. Survival data were converted to binary characters as follows: freezing survival > 20% = 1; freezing survival < 20% = 0. The nematodes were cold acclimated on nematode growth medium (NGM) plates at 10°C for 10 days.
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pone.0116084.g006: Maximum likelihood ancestral state reconstructions of freezing-tolerant phenotypes of (a) non-acclimated and (b) cold-acclimated Panagrolaimus species and strains, under the assumption that all transition rates are equal and branch lengths are proportional to time.At each node a pie chart represents the proportional (0–1) likelihood of each ancestral character state, coloured as in the key. Survival data were converted to binary characters as follows: freezing survival > 20% = 1; freezing survival < 20% = 0. The nematodes were cold acclimated on nematode growth medium (NGM) plates at 10°C for 10 days.

Mentions: Freezing survival data [Fig. 1(b)] were converted to binary characters as follows: a) non-acclimated nematodes—survival < 20% = 0, n = 14, survival ranges 0–19.6%; survival > 20% = 1, n = 10, survival ranges 23.8–56.3%; b) cold-acclimated nematodes—survival < 20% = 0, n = 8, survival ranges 2.29–18.0%; survival > 20% = 1, n = 16 survival ranges 24.9–82.7%. We consider that the ten nematode isolates whose non-acclimated freezing survival exceeds 20% show evidence of robust freezing tolerance, with eight of these isolates having survival values in the range 35%- 56%. Included in this group are P. davidi from Antarctica (35% non-acclimated survival) and P. superbus from Iceland (56% non-acclimated survival). Ancestral character state reconstructions of the freezing-tolerant phenotypes of unacclimated Panagrolaimus [Fig. 6(a)] is congruent with the evolutionary history of the ice growth-inhibition phenotype postulated above. Cold acclimation improves the freezing tolerance of the majority of Panagrolaimus strains, and it has a marked effect on the survival of some strains from the early-stemming lineages that are freezing sensitive when unacclimated. Reconstructions of the ancestral character state of the freezing-tolerant phenotypes of cold-acclimated nematodes reveal a complex evolutionary pattern [Fig. 6(b)], suggesting that inducible proto-cryobiotic phenotypes may have evolved as independent lineage-specific events in several of the early-diverging Panagrolaimus species. In addition, this latter dataset provides further support (p = 0.77) for the hypothesis that the ancestor of the davidi, superbus and JU Cape Verde clades was freezing tolerant.


Anhydrobiosis and freezing-tolerance: adaptations that facilitate the establishment of Panagrolaimus nematodes in polar habitats.

McGill LM, Shannon AJ, Pisani D, Félix MA, Ramløv H, Dix I, Wharton DA, Burnell AM - PLoS ONE (2015)

Maximum likelihood ancestral state reconstructions of freezing-tolerant phenotypes of (a) non-acclimated and (b) cold-acclimated Panagrolaimus species and strains, under the assumption that all transition rates are equal and branch lengths are proportional to time.At each node a pie chart represents the proportional (0–1) likelihood of each ancestral character state, coloured as in the key. Survival data were converted to binary characters as follows: freezing survival > 20% = 1; freezing survival < 20% = 0. The nematodes were cold acclimated on nematode growth medium (NGM) plates at 10°C for 10 days.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4352009&req=5

pone.0116084.g006: Maximum likelihood ancestral state reconstructions of freezing-tolerant phenotypes of (a) non-acclimated and (b) cold-acclimated Panagrolaimus species and strains, under the assumption that all transition rates are equal and branch lengths are proportional to time.At each node a pie chart represents the proportional (0–1) likelihood of each ancestral character state, coloured as in the key. Survival data were converted to binary characters as follows: freezing survival > 20% = 1; freezing survival < 20% = 0. The nematodes were cold acclimated on nematode growth medium (NGM) plates at 10°C for 10 days.
Mentions: Freezing survival data [Fig. 1(b)] were converted to binary characters as follows: a) non-acclimated nematodes—survival < 20% = 0, n = 14, survival ranges 0–19.6%; survival > 20% = 1, n = 10, survival ranges 23.8–56.3%; b) cold-acclimated nematodes—survival < 20% = 0, n = 8, survival ranges 2.29–18.0%; survival > 20% = 1, n = 16 survival ranges 24.9–82.7%. We consider that the ten nematode isolates whose non-acclimated freezing survival exceeds 20% show evidence of robust freezing tolerance, with eight of these isolates having survival values in the range 35%- 56%. Included in this group are P. davidi from Antarctica (35% non-acclimated survival) and P. superbus from Iceland (56% non-acclimated survival). Ancestral character state reconstructions of the freezing-tolerant phenotypes of unacclimated Panagrolaimus [Fig. 6(a)] is congruent with the evolutionary history of the ice growth-inhibition phenotype postulated above. Cold acclimation improves the freezing tolerance of the majority of Panagrolaimus strains, and it has a marked effect on the survival of some strains from the early-stemming lineages that are freezing sensitive when unacclimated. Reconstructions of the ancestral character state of the freezing-tolerant phenotypes of cold-acclimated nematodes reveal a complex evolutionary pattern [Fig. 6(b)], suggesting that inducible proto-cryobiotic phenotypes may have evolved as independent lineage-specific events in several of the early-diverging Panagrolaimus species. In addition, this latter dataset provides further support (p = 0.77) for the hypothesis that the ancestor of the davidi, superbus and JU Cape Verde clades was freezing tolerant.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Maynooth University, Maynooth, Co Kildare, Ireland.

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.

No MeSH data available.


Related in: MedlinePlus