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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

The effect of tissue extracts from unacclimated Panagrolaimus strains on the growth, morphology and recrystallization of ice crystals.Panel (a). Crystals formed in the presence of extracts from freezing-tolerant strains (a-c) have a distinct faceted morphology characteristic of the activity of ice-active proteins; ice crystals formed in the presence of extracts from a freezing sensitive strains (d, e) and in buffer controls (f) are cylindrical, indicating an uninhibited growth of the crystals. a: P. davidi; b: P. superbus; c: Panagrolaimus sp. PS1159; d: Panagrolaimus sp. JU765; e: Panagrolaimus sp. JU1367; f: S buffer (0.1 M NaCl, 0.05 M potassium phosphate, pH 6.0). Scale bar = 25 μM). Panel (b). Splat frozen samples of a: Tris buffer (25 mM Tris HCl, pH 8.6) and tissue extracts from b: Panagrolaimus sp. PS1159 and c: Panagrolaimus sp. SN103 following annealing at -8°C for 30 min. Scale bar = 100μM.
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pone.0116084.g003: The effect of tissue extracts from unacclimated Panagrolaimus strains on the growth, morphology and recrystallization of ice crystals.Panel (a). Crystals formed in the presence of extracts from freezing-tolerant strains (a-c) have a distinct faceted morphology characteristic of the activity of ice-active proteins; ice crystals formed in the presence of extracts from a freezing sensitive strains (d, e) and in buffer controls (f) are cylindrical, indicating an uninhibited growth of the crystals. a: P. davidi; b: P. superbus; c: Panagrolaimus sp. PS1159; d: Panagrolaimus sp. JU765; e: Panagrolaimus sp. JU1367; f: S buffer (0.1 M NaCl, 0.05 M potassium phosphate, pH 6.0). Scale bar = 25 μM). Panel (b). Splat frozen samples of a: Tris buffer (25 mM Tris HCl, pH 8.6) and tissue extracts from b: Panagrolaimus sp. PS1159 and c: Panagrolaimus sp. SN103 following annealing at -8°C for 30 min. Scale bar = 100μM.

Mentions: Extracts from P. davidi contain an ice-active protein (IAP) which inhibits the growth and recrystallization ice crystals [30]. Using freezing-point nanolitre osmometry, we tested the ability of tissue extracts from 24 unacclimated Panagrolaimus strains, including P. davidi, to inhibit the growth of a single seed ice crystal [Fig. 3(a); S5 Fig.]. In water or buffer, ice normally grows on the prism planes (along the horizontal a axes) of the crystal lattice, with little perpendicular growth on the basal plane (along the c axis), so that the ice crystals have the appearance of flat, round or irregular discs [27]. The majority of IAPs preferentially bind to the prism plane (S6 Fig.), inhibiting the growth of ice along the a axes and creating hexagonal discs [27]. When assayed at a protein concentration of 2 μg μL-1 the ice crystals formed from extracts of P. davidi and ten other Panagrolaimus strains were hexagonal in shape and inhibition of ice growth on the a axes of these crystals was evident from their truncated pyramidal growth patterns. Ice crystals formed from extracts from the remaining strains had the appearance of flat, round discs, indicative of unrestricted ice growth along the a axes. Fig. 1 (b) shows that the strains whose unacclimated tissue extracts inhibit ice-crystal growth have robust freezing tolerance (>20% survival following exposure to -80°C for 24 h) and that extracts from all members of the clade that contains P. davidi are able to inhibit the growth of ice crystals.


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)

The effect of tissue extracts from unacclimated Panagrolaimus strains on the growth, morphology and recrystallization of ice crystals.Panel (a). Crystals formed in the presence of extracts from freezing-tolerant strains (a-c) have a distinct faceted morphology characteristic of the activity of ice-active proteins; ice crystals formed in the presence of extracts from a freezing sensitive strains (d, e) and in buffer controls (f) are cylindrical, indicating an uninhibited growth of the crystals. a: P. davidi; b: P. superbus; c: Panagrolaimus sp. PS1159; d: Panagrolaimus sp. JU765; e: Panagrolaimus sp. JU1367; f: S buffer (0.1 M NaCl, 0.05 M potassium phosphate, pH 6.0). Scale bar = 25 μM). Panel (b). Splat frozen samples of a: Tris buffer (25 mM Tris HCl, pH 8.6) and tissue extracts from b: Panagrolaimus sp. PS1159 and c: Panagrolaimus sp. SN103 following annealing at -8°C for 30 min. Scale bar = 100μM.
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pone.0116084.g003: The effect of tissue extracts from unacclimated Panagrolaimus strains on the growth, morphology and recrystallization of ice crystals.Panel (a). Crystals formed in the presence of extracts from freezing-tolerant strains (a-c) have a distinct faceted morphology characteristic of the activity of ice-active proteins; ice crystals formed in the presence of extracts from a freezing sensitive strains (d, e) and in buffer controls (f) are cylindrical, indicating an uninhibited growth of the crystals. a: P. davidi; b: P. superbus; c: Panagrolaimus sp. PS1159; d: Panagrolaimus sp. JU765; e: Panagrolaimus sp. JU1367; f: S buffer (0.1 M NaCl, 0.05 M potassium phosphate, pH 6.0). Scale bar = 25 μM). Panel (b). Splat frozen samples of a: Tris buffer (25 mM Tris HCl, pH 8.6) and tissue extracts from b: Panagrolaimus sp. PS1159 and c: Panagrolaimus sp. SN103 following annealing at -8°C for 30 min. Scale bar = 100μM.
Mentions: Extracts from P. davidi contain an ice-active protein (IAP) which inhibits the growth and recrystallization ice crystals [30]. Using freezing-point nanolitre osmometry, we tested the ability of tissue extracts from 24 unacclimated Panagrolaimus strains, including P. davidi, to inhibit the growth of a single seed ice crystal [Fig. 3(a); S5 Fig.]. In water or buffer, ice normally grows on the prism planes (along the horizontal a axes) of the crystal lattice, with little perpendicular growth on the basal plane (along the c axis), so that the ice crystals have the appearance of flat, round or irregular discs [27]. The majority of IAPs preferentially bind to the prism plane (S6 Fig.), inhibiting the growth of ice along the a axes and creating hexagonal discs [27]. When assayed at a protein concentration of 2 μg μL-1 the ice crystals formed from extracts of P. davidi and ten other Panagrolaimus strains were hexagonal in shape and inhibition of ice growth on the a axes of these crystals was evident from their truncated pyramidal growth patterns. Ice crystals formed from extracts from the remaining strains had the appearance of flat, round discs, indicative of unrestricted ice growth along the a axes. Fig. 1 (b) shows that the strains whose unacclimated tissue extracts inhibit ice-crystal growth have robust freezing tolerance (>20% survival following exposure to -80°C for 24 h) and that extracts from all members of the clade that contains P. davidi are able to inhibit the growth of ice crystals.

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