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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

Correlation between freezing-tolerance and anhydrobiosis in Panagrolaimus.(a) Spearman rank correlation between freezing-tolerance and anhydrobiosis in all 24 Panagrolaimus strains (r = 0.0033, N.S.). (b) Spearman rank correlation between freezing-tolerance and anhydrobiosis in Panagrolaimus PCA Group 3 and Group 4 strains (Spearman’s r = 0.718, p < 0.05). The data points are shaded as follows: PCA Group 1, purple; Group 2, red; Group 3 blue; Group 4 green.
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pone.0116084.g004: Correlation between freezing-tolerance and anhydrobiosis in Panagrolaimus.(a) Spearman rank correlation between freezing-tolerance and anhydrobiosis in all 24 Panagrolaimus strains (r = 0.0033, N.S.). (b) Spearman rank correlation between freezing-tolerance and anhydrobiosis in Panagrolaimus PCA Group 3 and Group 4 strains (Spearman’s r = 0.718, p < 0.05). The data points are shaded as follows: PCA Group 1, purple; Group 2, red; Group 3 blue; Group 4 green.

Mentions: A correlation between freezing-tolerance and anhydrobiotic phenotypes might occur in Panagrolaimus because of an overlap in the biochemical protection responses of the nematodes to desiccation and freezing; or because of their shared phylogeny; or because they occupy an environment where correlated selection for freezing-tolerance and anhydrobiosis may occur. Studies in insects that overwinter in temperate and polar environments frequently show evidence of cross-tolerance between the physiological responses to cold stress and desiccation stress, where the mechanisms that protect against one of these stresses also provide protection against the other (reviewed by Sinclair et al. [69]). Correlation analysis [Fig. 4(a)] shows that the freezing and anhydrobiotic phenotypes of all 24 Panagrolaimus strains are not correlated (Spearman’s r = 0.0033, p = 0.99), indicating that the biochemical and physiological responses of these nematodes to desiccation and freezing are unlikely to provide cross-tolerance. It is noteworthy that the nematodes in PCA Group 2 that possess the highest desiccation tolerance have substantially weaker freezing tolerance than PCA Group 3 and 4 nematodes [Fig. 4(a)]. PCA Group 2 nematodes are tropical and sub-tropical in origin, whereas the isolates from PCA Groups 3 and 4 were isolated in temperate and polar regions (with the exception of JB051 from Senegal). It is unlikely that the tropical and sub-tropical Panagrolaimus isolates have been exposed to correlated selection for freezing-tolerance and anhydrobiosis in their recent evolutionary history, however the isolates from temperate and polar regions are more likely to experience such correlated selection. PCA Groups 3 and 4 strains show a strong positive relationship between their freezing-tolerance and anhydrobiotic phenotypes [Fig. 4(b)], (Spearman’s r = 0.718, p = 0.016*). To assess whether this correlation may be the result of correlated selection for these traits, we generated an rDNA D3 phylogeny for PCA Groups 3 and 4 and we used a PGLS approach which estimates Pagel’s λ simultaneously with the regression parameters to provide a correction of trait covariance based on the phylogenetic signal of the data [50]. The results obtained (PGLS Adjusted R2 = 0.5568, p = 0.005**, λ = 0) also show that freezing-tolerance and anhydrobiosis are correlated traits in the Panagrolaimus strains from PCA Groups 3 and 4. However these results need to be interpreted conservatively because, given the estimated λ = 0 value for these traits in the PCA Group 3 and 4 phylogeny, the PGLS correlation was estimated under the assumption that all the panagrolaimid isolates in PCA Groups 3 and 4 are equally distantly related to each other.


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)

Correlation between freezing-tolerance and anhydrobiosis in Panagrolaimus.(a) Spearman rank correlation between freezing-tolerance and anhydrobiosis in all 24 Panagrolaimus strains (r = 0.0033, N.S.). (b) Spearman rank correlation between freezing-tolerance and anhydrobiosis in Panagrolaimus PCA Group 3 and Group 4 strains (Spearman’s r = 0.718, p < 0.05). The data points are shaded as follows: PCA Group 1, purple; Group 2, red; Group 3 blue; Group 4 green.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0116084.g004: Correlation between freezing-tolerance and anhydrobiosis in Panagrolaimus.(a) Spearman rank correlation between freezing-tolerance and anhydrobiosis in all 24 Panagrolaimus strains (r = 0.0033, N.S.). (b) Spearman rank correlation between freezing-tolerance and anhydrobiosis in Panagrolaimus PCA Group 3 and Group 4 strains (Spearman’s r = 0.718, p < 0.05). The data points are shaded as follows: PCA Group 1, purple; Group 2, red; Group 3 blue; Group 4 green.
Mentions: A correlation between freezing-tolerance and anhydrobiotic phenotypes might occur in Panagrolaimus because of an overlap in the biochemical protection responses of the nematodes to desiccation and freezing; or because of their shared phylogeny; or because they occupy an environment where correlated selection for freezing-tolerance and anhydrobiosis may occur. Studies in insects that overwinter in temperate and polar environments frequently show evidence of cross-tolerance between the physiological responses to cold stress and desiccation stress, where the mechanisms that protect against one of these stresses also provide protection against the other (reviewed by Sinclair et al. [69]). Correlation analysis [Fig. 4(a)] shows that the freezing and anhydrobiotic phenotypes of all 24 Panagrolaimus strains are not correlated (Spearman’s r = 0.0033, p = 0.99), indicating that the biochemical and physiological responses of these nematodes to desiccation and freezing are unlikely to provide cross-tolerance. It is noteworthy that the nematodes in PCA Group 2 that possess the highest desiccation tolerance have substantially weaker freezing tolerance than PCA Group 3 and 4 nematodes [Fig. 4(a)]. PCA Group 2 nematodes are tropical and sub-tropical in origin, whereas the isolates from PCA Groups 3 and 4 were isolated in temperate and polar regions (with the exception of JB051 from Senegal). It is unlikely that the tropical and sub-tropical Panagrolaimus isolates have been exposed to correlated selection for freezing-tolerance and anhydrobiosis in their recent evolutionary history, however the isolates from temperate and polar regions are more likely to experience such correlated selection. PCA Groups 3 and 4 strains show a strong positive relationship between their freezing-tolerance and anhydrobiotic phenotypes [Fig. 4(b)], (Spearman’s r = 0.718, p = 0.016*). To assess whether this correlation may be the result of correlated selection for these traits, we generated an rDNA D3 phylogeny for PCA Groups 3 and 4 and we used a PGLS approach which estimates Pagel’s λ simultaneously with the regression parameters to provide a correction of trait covariance based on the phylogenetic signal of the data [50]. The results obtained (PGLS Adjusted R2 = 0.5568, p = 0.005**, λ = 0) also show that freezing-tolerance and anhydrobiosis are correlated traits in the Panagrolaimus strains from PCA Groups 3 and 4. However these results need to be interpreted conservatively because, given the estimated λ = 0 value for these traits in the PCA Group 3 and 4 phylogeny, the PGLS correlation was estimated under the assumption that all the panagrolaimid isolates in PCA Groups 3 and 4 are equally distantly related to each other.

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