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A fast recoiling silk-like elastomer facilitates nanosecond nematocyst discharge.

Beckmann A, Xiao S, Müller JP, Mercadante D, Nüchter T, Kröger N, Langhojer F, Petrich W, Holstein TW, Benoit M, Gräter F, Özbek S - BMC Biol. (2015)

Bottom Line: Similar to spider silk proteins, to which it is related at sequence level, Cnidoin possesses high elasticity and fast coiling propensity as predicted by molecular dynamics simulations and quantified by force spectroscopy.Cnidoin represents the molecular factor involved in kinetic energy storage and release during the ultra-fast nematocyst discharge.Furthermore, it implies an early evolutionary origin of protein elastomers in basal metazoans.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Evolution and Genomics, University of Heidelberg, Centre for Organismal Studies, Im Neuenheimer Feld 329, 69120, Heidelberg, Germany. Anna.beckmann@cos.uni-heidelberg.de.

ABSTRACT

Background: The discharge of the Cnidarian stinging organelle, the nematocyst, is one of the fastest processes in biology and involves volume changes of the highly pressurised (150 bar) capsule of up to 50%. Hitherto, the molecular basis for the unusual biomechanical properties of nematocysts has been elusive, as their structure was mainly defined as a stress-resistant collagenous matrix.

Results: Here, we characterise Cnidoin, a novel elastic protein identified as a structural component of Hydra nematocysts. Cnidoin is expressed in nematocytes of all types and immunostainings revealed incorporation into capsule walls and tubules concomitant with minicollagens. Similar to spider silk proteins, to which it is related at sequence level, Cnidoin possesses high elasticity and fast coiling propensity as predicted by molecular dynamics simulations and quantified by force spectroscopy. Recombinant Cnidoin showed a high tendency for spontaneous aggregation to bundles of fibrillar structures.

Conclusions: Cnidoin represents the molecular factor involved in kinetic energy storage and release during the ultra-fast nematocyst discharge. Furthermore, it implies an early evolutionary origin of protein elastomers in basal metazoans.

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Molecular elasticity of Cnidoin peptides from MD simulations. (A) two representative (collapsed and extended) conformations of a Cnidoin peptide unit. To obtain force-extension curves, N-terminal C-alpha atoms (blue spheres) were fixed, while the C-termini (red spheres) were subjected to a force acted along the extension (red arrows). (B) mean forces calculated from umbrella sampling. The force profiles of two different Cnidoin repeat units (squares) were fitted with the worm-like chain model (solid lines). Resulting free energy profiles along the end-to-end distance are shown in the inset. (C) residue-averaged hydrophobic surface burial of two Cnidoin peptides measured by disappearance of solvent accessible surface area (ΔSASA). (D) PPII conformation content in the Cnidoin peptides along peptide extension. (C) and (D) use the same colour code as (B). MD, molecular dynamics; PPII, polyproline II.
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Fig5: Molecular elasticity of Cnidoin peptides from MD simulations. (A) two representative (collapsed and extended) conformations of a Cnidoin peptide unit. To obtain force-extension curves, N-terminal C-alpha atoms (blue spheres) were fixed, while the C-termini (red spheres) were subjected to a force acted along the extension (red arrows). (B) mean forces calculated from umbrella sampling. The force profiles of two different Cnidoin repeat units (squares) were fitted with the worm-like chain model (solid lines). Resulting free energy profiles along the end-to-end distance are shown in the inset. (C) residue-averaged hydrophobic surface burial of two Cnidoin peptides measured by disappearance of solvent accessible surface area (ΔSASA). (D) PPII conformation content in the Cnidoin peptides along peptide extension. (C) and (D) use the same colour code as (B). MD, molecular dynamics; PPII, polyproline II.

Mentions: To complementary assess the elasticity of Cnidoin, we calculated the force-extension profile of two representative repeat units of Cnidoin using umbrella sampling [20]. To this end, Cnidoin peptide conformations were extensively sampled at varying end-to-end distances dZ (Figure 5A). Resulting average resisting forces against Cnidoin extension are shown in Figure 5B, with the resulting free energy shown in the inset. We observed a force plateau followed by a steep increase in force at larger extensions. The mean forces were fitted by the WLC model (solid line in Figure 5B), [36], which predicted persistence lengths of 0.89 ± 0.1 and 0.66 ± 0.06 nm for the Cnidoin repeat units shown in Figure 5B in red and black, respectively. Therefore, Cnidoin is found to be as elastic as silk disordered peptides, which have formerly been reported to have a persistence length of 0.74 nm in MD simulations in the force range probed here [20]. Hence, the MD simulations confirm the finding from AFM experiments of a featureless force-extension curve resembling a disordered protein such as silk. We note that for both silk [20,37] and Cnidoin investigated here, the persistence length from simulations is higher than in experiments, although the second simulated Cnidoin repeat unit lies within the experimental range (Figure 5B, red line).Figure 5


A fast recoiling silk-like elastomer facilitates nanosecond nematocyst discharge.

Beckmann A, Xiao S, Müller JP, Mercadante D, Nüchter T, Kröger N, Langhojer F, Petrich W, Holstein TW, Benoit M, Gräter F, Özbek S - BMC Biol. (2015)

Molecular elasticity of Cnidoin peptides from MD simulations. (A) two representative (collapsed and extended) conformations of a Cnidoin peptide unit. To obtain force-extension curves, N-terminal C-alpha atoms (blue spheres) were fixed, while the C-termini (red spheres) were subjected to a force acted along the extension (red arrows). (B) mean forces calculated from umbrella sampling. The force profiles of two different Cnidoin repeat units (squares) were fitted with the worm-like chain model (solid lines). Resulting free energy profiles along the end-to-end distance are shown in the inset. (C) residue-averaged hydrophobic surface burial of two Cnidoin peptides measured by disappearance of solvent accessible surface area (ΔSASA). (D) PPII conformation content in the Cnidoin peptides along peptide extension. (C) and (D) use the same colour code as (B). MD, molecular dynamics; PPII, polyproline II.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4321713&req=5

Fig5: Molecular elasticity of Cnidoin peptides from MD simulations. (A) two representative (collapsed and extended) conformations of a Cnidoin peptide unit. To obtain force-extension curves, N-terminal C-alpha atoms (blue spheres) were fixed, while the C-termini (red spheres) were subjected to a force acted along the extension (red arrows). (B) mean forces calculated from umbrella sampling. The force profiles of two different Cnidoin repeat units (squares) were fitted with the worm-like chain model (solid lines). Resulting free energy profiles along the end-to-end distance are shown in the inset. (C) residue-averaged hydrophobic surface burial of two Cnidoin peptides measured by disappearance of solvent accessible surface area (ΔSASA). (D) PPII conformation content in the Cnidoin peptides along peptide extension. (C) and (D) use the same colour code as (B). MD, molecular dynamics; PPII, polyproline II.
Mentions: To complementary assess the elasticity of Cnidoin, we calculated the force-extension profile of two representative repeat units of Cnidoin using umbrella sampling [20]. To this end, Cnidoin peptide conformations were extensively sampled at varying end-to-end distances dZ (Figure 5A). Resulting average resisting forces against Cnidoin extension are shown in Figure 5B, with the resulting free energy shown in the inset. We observed a force plateau followed by a steep increase in force at larger extensions. The mean forces were fitted by the WLC model (solid line in Figure 5B), [36], which predicted persistence lengths of 0.89 ± 0.1 and 0.66 ± 0.06 nm for the Cnidoin repeat units shown in Figure 5B in red and black, respectively. Therefore, Cnidoin is found to be as elastic as silk disordered peptides, which have formerly been reported to have a persistence length of 0.74 nm in MD simulations in the force range probed here [20]. Hence, the MD simulations confirm the finding from AFM experiments of a featureless force-extension curve resembling a disordered protein such as silk. We note that for both silk [20,37] and Cnidoin investigated here, the persistence length from simulations is higher than in experiments, although the second simulated Cnidoin repeat unit lies within the experimental range (Figure 5B, red line).Figure 5

Bottom Line: Similar to spider silk proteins, to which it is related at sequence level, Cnidoin possesses high elasticity and fast coiling propensity as predicted by molecular dynamics simulations and quantified by force spectroscopy.Cnidoin represents the molecular factor involved in kinetic energy storage and release during the ultra-fast nematocyst discharge.Furthermore, it implies an early evolutionary origin of protein elastomers in basal metazoans.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Evolution and Genomics, University of Heidelberg, Centre for Organismal Studies, Im Neuenheimer Feld 329, 69120, Heidelberg, Germany. Anna.beckmann@cos.uni-heidelberg.de.

ABSTRACT

Background: The discharge of the Cnidarian stinging organelle, the nematocyst, is one of the fastest processes in biology and involves volume changes of the highly pressurised (150 bar) capsule of up to 50%. Hitherto, the molecular basis for the unusual biomechanical properties of nematocysts has been elusive, as their structure was mainly defined as a stress-resistant collagenous matrix.

Results: Here, we characterise Cnidoin, a novel elastic protein identified as a structural component of Hydra nematocysts. Cnidoin is expressed in nematocytes of all types and immunostainings revealed incorporation into capsule walls and tubules concomitant with minicollagens. Similar to spider silk proteins, to which it is related at sequence level, Cnidoin possesses high elasticity and fast coiling propensity as predicted by molecular dynamics simulations and quantified by force spectroscopy. Recombinant Cnidoin showed a high tendency for spontaneous aggregation to bundles of fibrillar structures.

Conclusions: Cnidoin represents the molecular factor involved in kinetic energy storage and release during the ultra-fast nematocyst discharge. Furthermore, it implies an early evolutionary origin of protein elastomers in basal metazoans.

Show MeSH
Related in: MedlinePlus