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A fast Na+/Ca2+-based action potential in a marine diatom.

Taylor AR - PLoS ONE (2009)

Bottom Line: Underpinning many of these electrical signals is a fast Na+-based action potential that has been fully characterised only in cells associated with the neuromuscular systems of multicellular animals.The biophysical and pharmacological characteristics together with the presence of a voltage activated Na+/Ca2+ channel homologue in the recently sequenced genome of the diatom Thalassiosira pseudonana, provides direct evidence supporting the hypothesis that this rapid signalling mechanism arose in ancestral unicellular eukaryotes and has been retained in at least two phylogenetically distant lineages of eukaryotes; opisthokonts and the stramenopiles.The functional role of the fast animal-like action potential in diatoms remains to be elucidated but is likely involved in rapid environmental sensing of these widespread and successful marine protists.

View Article: PubMed Central - PubMed

Affiliation: The Marine Biological Association of the UK, Citadel Hill, Plymouth, United Kingdom. taylora@uncw.edu

ABSTRACT

Background: Electrical impulses in animals play essential roles in co-ordinating an array of physiological functions including movement, secretion, environmental sensing and development. Underpinning many of these electrical signals is a fast Na+-based action potential that has been fully characterised only in cells associated with the neuromuscular systems of multicellular animals. Such rapid action potentials are thought to have evolved with the first metazoans, with cnidarians being the earliest representatives. The present study demonstrates that a unicellular protist, the marine diatom Odontella sinensis, can also generate a fast Na+/Ca2+ based action potential that has remarkably similar biophysical and pharmacological properties to invertebrates and vertebrate cardiac and skeletal muscle cells.

Methodology/principal findings: The kinetic, ionic and pharmacological properties of the rapid diatom action potential were examined using single electrode current and voltage clamp techniques. Overall, the characteristics of the fast diatom currents most closely resemble those of vertebrate and invertebrate muscle Na+/Ca2+ currents.

Conclusions/significance: This is the first demonstration of voltage-activated Na+ channels and the capacity to generate fast Na+-based action potentials in a unicellular photosynthetic organism. The biophysical and pharmacological characteristics together with the presence of a voltage activated Na+/Ca2+ channel homologue in the recently sequenced genome of the diatom Thalassiosira pseudonana, provides direct evidence supporting the hypothesis that this rapid signalling mechanism arose in ancestral unicellular eukaryotes and has been retained in at least two phylogenetically distant lineages of eukaryotes; opisthokonts and the stramenopiles. The functional role of the fast animal-like action potential in diatoms remains to be elucidated but is likely involved in rapid environmental sensing of these widespread and successful marine protists.

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Pharmacology of the diatom Na+ current.Peak Na+ currents were evoked by a voltage clamp pulse to −20 mV from a holding potential of between −100 mV and −90 mV before perfusion of various pharmacological agents. A) TTX had only a slight impact on the current even at relatively high concentrations and no effect of 1 µM STX was observed (n = 5, data not shown). The Na+ current was sensitive to block by lidocaine, Cd2+ and La3+ ions. In all cases the block was reversible (e.g. lidocaine) on washing out with fresh ASW. Scale bars indicate 10 nA and 5 ms and dotted line represents 0 nA. B) Summary of the effect of various Na+ channel antagonists on the peak sodium current in Odontella sinensis. Numbers of experiments and standard error bars are indicated for each treatment.
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pone-0004966-g004: Pharmacology of the diatom Na+ current.Peak Na+ currents were evoked by a voltage clamp pulse to −20 mV from a holding potential of between −100 mV and −90 mV before perfusion of various pharmacological agents. A) TTX had only a slight impact on the current even at relatively high concentrations and no effect of 1 µM STX was observed (n = 5, data not shown). The Na+ current was sensitive to block by lidocaine, Cd2+ and La3+ ions. In all cases the block was reversible (e.g. lidocaine) on washing out with fresh ASW. Scale bars indicate 10 nA and 5 ms and dotted line represents 0 nA. B) Summary of the effect of various Na+ channel antagonists on the peak sodium current in Odontella sinensis. Numbers of experiments and standard error bars are indicated for each treatment.

Mentions: Cardiac-type Na+ channels exhibit distinct pharmacological properties when compared to neuronal Na+ channels [14]. The pharmacology of the diatom Na+ current was therefore examined. The current was insensitive to the potent Na+ channel blocker tetrodotoxin (TTX) with only slight block induced with concentrations higher than 5 µM (Figure 4). Not unexpectedly the diatom Na+ current was also insensitive to the algal toxin saxitoxin (STX) that blocks at the same site as TTX (Figure 4). Such TTX insensitivity is common among cardiac and invertebrate Na+ channels studied to date. This group of TTX insensitive animal Na+ channels are however sensitive to lipophyllic blockers [14] and this was also the case with the diatom Na+ current, which was significantly blocked by the Na+ channel modulating local anaesthetic lidocaine (Figure 4). Cd2+ and La3+ which are blockers of the TTX-resistant Na+ channel [16] were also effective inhibitors of the diatom Na+ current (Figure 4).


A fast Na+/Ca2+-based action potential in a marine diatom.

Taylor AR - PLoS ONE (2009)

Pharmacology of the diatom Na+ current.Peak Na+ currents were evoked by a voltage clamp pulse to −20 mV from a holding potential of between −100 mV and −90 mV before perfusion of various pharmacological agents. A) TTX had only a slight impact on the current even at relatively high concentrations and no effect of 1 µM STX was observed (n = 5, data not shown). The Na+ current was sensitive to block by lidocaine, Cd2+ and La3+ ions. In all cases the block was reversible (e.g. lidocaine) on washing out with fresh ASW. Scale bars indicate 10 nA and 5 ms and dotted line represents 0 nA. B) Summary of the effect of various Na+ channel antagonists on the peak sodium current in Odontella sinensis. Numbers of experiments and standard error bars are indicated for each treatment.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2654917&req=5

pone-0004966-g004: Pharmacology of the diatom Na+ current.Peak Na+ currents were evoked by a voltage clamp pulse to −20 mV from a holding potential of between −100 mV and −90 mV before perfusion of various pharmacological agents. A) TTX had only a slight impact on the current even at relatively high concentrations and no effect of 1 µM STX was observed (n = 5, data not shown). The Na+ current was sensitive to block by lidocaine, Cd2+ and La3+ ions. In all cases the block was reversible (e.g. lidocaine) on washing out with fresh ASW. Scale bars indicate 10 nA and 5 ms and dotted line represents 0 nA. B) Summary of the effect of various Na+ channel antagonists on the peak sodium current in Odontella sinensis. Numbers of experiments and standard error bars are indicated for each treatment.
Mentions: Cardiac-type Na+ channels exhibit distinct pharmacological properties when compared to neuronal Na+ channels [14]. The pharmacology of the diatom Na+ current was therefore examined. The current was insensitive to the potent Na+ channel blocker tetrodotoxin (TTX) with only slight block induced with concentrations higher than 5 µM (Figure 4). Not unexpectedly the diatom Na+ current was also insensitive to the algal toxin saxitoxin (STX) that blocks at the same site as TTX (Figure 4). Such TTX insensitivity is common among cardiac and invertebrate Na+ channels studied to date. This group of TTX insensitive animal Na+ channels are however sensitive to lipophyllic blockers [14] and this was also the case with the diatom Na+ current, which was significantly blocked by the Na+ channel modulating local anaesthetic lidocaine (Figure 4). Cd2+ and La3+ which are blockers of the TTX-resistant Na+ channel [16] were also effective inhibitors of the diatom Na+ current (Figure 4).

Bottom Line: Underpinning many of these electrical signals is a fast Na+-based action potential that has been fully characterised only in cells associated with the neuromuscular systems of multicellular animals.The biophysical and pharmacological characteristics together with the presence of a voltage activated Na+/Ca2+ channel homologue in the recently sequenced genome of the diatom Thalassiosira pseudonana, provides direct evidence supporting the hypothesis that this rapid signalling mechanism arose in ancestral unicellular eukaryotes and has been retained in at least two phylogenetically distant lineages of eukaryotes; opisthokonts and the stramenopiles.The functional role of the fast animal-like action potential in diatoms remains to be elucidated but is likely involved in rapid environmental sensing of these widespread and successful marine protists.

View Article: PubMed Central - PubMed

Affiliation: The Marine Biological Association of the UK, Citadel Hill, Plymouth, United Kingdom. taylora@uncw.edu

ABSTRACT

Background: Electrical impulses in animals play essential roles in co-ordinating an array of physiological functions including movement, secretion, environmental sensing and development. Underpinning many of these electrical signals is a fast Na+-based action potential that has been fully characterised only in cells associated with the neuromuscular systems of multicellular animals. Such rapid action potentials are thought to have evolved with the first metazoans, with cnidarians being the earliest representatives. The present study demonstrates that a unicellular protist, the marine diatom Odontella sinensis, can also generate a fast Na+/Ca2+ based action potential that has remarkably similar biophysical and pharmacological properties to invertebrates and vertebrate cardiac and skeletal muscle cells.

Methodology/principal findings: The kinetic, ionic and pharmacological properties of the rapid diatom action potential were examined using single electrode current and voltage clamp techniques. Overall, the characteristics of the fast diatom currents most closely resemble those of vertebrate and invertebrate muscle Na+/Ca2+ currents.

Conclusions/significance: This is the first demonstration of voltage-activated Na+ channels and the capacity to generate fast Na+-based action potentials in a unicellular photosynthetic organism. The biophysical and pharmacological characteristics together with the presence of a voltage activated Na+/Ca2+ channel homologue in the recently sequenced genome of the diatom Thalassiosira pseudonana, provides direct evidence supporting the hypothesis that this rapid signalling mechanism arose in ancestral unicellular eukaryotes and has been retained in at least two phylogenetically distant lineages of eukaryotes; opisthokonts and the stramenopiles. The functional role of the fast animal-like action potential in diatoms remains to be elucidated but is likely involved in rapid environmental sensing of these widespread and successful marine protists.

Show MeSH