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The B vitamins nicotinamide (B3) and riboflavin (B2) stimulate metamorphosis in larvae of the deposit-feeding polychaete Capitella teleta: implications for a sensory ligand-gated ion channel.

Burns RT, Pechenik JA, Biggers WJ, Scavo G, Lehman C - PLoS ONE (2014)

Bottom Line: In contrast, neither lumichrome, thiamine HCl, pyridoxine HCl, nor vitamin B12 stimulated larvae of C. teleta to metamorphose at concentrations as high as 500 µM.Larvae also did not metamorphose in response to either nicotinamide or pyrazinecarboxamide in calcium-free seawater or with the addition of 4-acetylpyridine, a competitive inhibitor of the pyridine receptor.Together, these results suggest that larvae of C. teleta are responding to nicotinamide and riboflavin via a chemosensory pyridine receptor similar to that previously reported to be present on crayfish chela and involved with food recognition.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Tufts University, Medford, Massachusetts, United States of America.

ABSTRACT
Marine sediments can contain B vitamins, presumably incorporated from settled, decaying phytoplankton and microorganisms associated with decomposition. Because B vitamins may be advantageous for the energetically intensive processes of metamorphosis, post-metamorphic growth, and reproduction, we tested several B vitamins to determine if they would stimulate larvae of the deposit-feeding polychaete Capitella teleta to settle and metamorphose. Nicotinamide and riboflavin individually stimulated larvae of C. teleta to settle and metamorphose, generally within 1-2 hours at nicotinamide concentrations as low as 3 µM and riboflavin concentrations as low as 50 µM. More than 80% of the larvae metamorphosed within 30 minutes at a nicotinamide concentration of 7 µM. The pyridine channel agonist pyrazinecarboxamide also stimulated metamorphosis at very low concentrations. In contrast, neither lumichrome, thiamine HCl, pyridoxine HCl, nor vitamin B12 stimulated larvae of C. teleta to metamorphose at concentrations as high as 500 µM. Larvae also did not metamorphose in response to either nicotinamide or pyrazinecarboxamide in calcium-free seawater or with the addition of 4-acetylpyridine, a competitive inhibitor of the pyridine receptor. Together, these results suggest that larvae of C. teleta are responding to nicotinamide and riboflavin via a chemosensory pyridine receptor similar to that previously reported to be present on crayfish chela and involved with food recognition. Our data are the first to implicate B vitamins as possible natural chemical settlement cues for marine invertebrate larvae.

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The effects of pyrazinecarboxamide and nicotinamide on metamorphosis of C. teleta when tested equal concentrations.Each treatment consisted of 3 replicates with 8 larvae per replicate. Artificial seawater (Instant Ocean) acted as a negative control. Error bars represent +/−1 s.e.m.
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pone-0109535-g003: The effects of pyrazinecarboxamide and nicotinamide on metamorphosis of C. teleta when tested equal concentrations.Each treatment consisted of 3 replicates with 8 larvae per replicate. Artificial seawater (Instant Ocean) acted as a negative control. Error bars represent +/−1 s.e.m.

Mentions: Because concentrations of nicotinamide as low as 3–6 µM stimulated larvae of C. teleta to metamorphose quickly in our experiments, we hypothesized that larvae of C. teleta were sensing nicotinamide via a pyridine activated ion channel, something first characterized in the walking legs of the crayfish Austrapotamobius torrentium[30]–[32]. We therefore compared dose responses between nicotinamide and pyrazinecarboxamide, an agonist of the pyridine-activated ion channel, at 1 µM, 4 µM, and 8 µM. Another commonly occurring nutritive chemical, beta nicotinamide adenine dinucleotide (β-NAD), also stimulated the nicotinamide-activated ion-channel to open, with half-maximal rate of opening (KM) at 1 mM [31]. We therefore treated larvae of C. teleta with β-NAD at the concentrations of 0.5, 1, and 5 mM to determine if β-NAD also stimulated metamorphosis. As shown in Figure 3, the pyridine-activated ion channel agonist pyrazinecarboxamide was found to also stimulate larvae of C. teleta to metamorphose, and did so at similar concentrations as nicotinamide. Although both chemicals stimulated larvae of C. teleta to metamorphose in a dose-dependent fashion, pyrazinecarboxamide stimulated more individuals (about 70%) to metamorphose at 4 µM than did nicotinamide at the same concentration (Figure 3). β-NAD, however, did not stimulate any metamorphosis at 0.5, 1, or 5 mM.


The B vitamins nicotinamide (B3) and riboflavin (B2) stimulate metamorphosis in larvae of the deposit-feeding polychaete Capitella teleta: implications for a sensory ligand-gated ion channel.

Burns RT, Pechenik JA, Biggers WJ, Scavo G, Lehman C - PLoS ONE (2014)

The effects of pyrazinecarboxamide and nicotinamide on metamorphosis of C. teleta when tested equal concentrations.Each treatment consisted of 3 replicates with 8 larvae per replicate. Artificial seawater (Instant Ocean) acted as a negative control. Error bars represent +/−1 s.e.m.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4229104&req=5

pone-0109535-g003: The effects of pyrazinecarboxamide and nicotinamide on metamorphosis of C. teleta when tested equal concentrations.Each treatment consisted of 3 replicates with 8 larvae per replicate. Artificial seawater (Instant Ocean) acted as a negative control. Error bars represent +/−1 s.e.m.
Mentions: Because concentrations of nicotinamide as low as 3–6 µM stimulated larvae of C. teleta to metamorphose quickly in our experiments, we hypothesized that larvae of C. teleta were sensing nicotinamide via a pyridine activated ion channel, something first characterized in the walking legs of the crayfish Austrapotamobius torrentium[30]–[32]. We therefore compared dose responses between nicotinamide and pyrazinecarboxamide, an agonist of the pyridine-activated ion channel, at 1 µM, 4 µM, and 8 µM. Another commonly occurring nutritive chemical, beta nicotinamide adenine dinucleotide (β-NAD), also stimulated the nicotinamide-activated ion-channel to open, with half-maximal rate of opening (KM) at 1 mM [31]. We therefore treated larvae of C. teleta with β-NAD at the concentrations of 0.5, 1, and 5 mM to determine if β-NAD also stimulated metamorphosis. As shown in Figure 3, the pyridine-activated ion channel agonist pyrazinecarboxamide was found to also stimulate larvae of C. teleta to metamorphose, and did so at similar concentrations as nicotinamide. Although both chemicals stimulated larvae of C. teleta to metamorphose in a dose-dependent fashion, pyrazinecarboxamide stimulated more individuals (about 70%) to metamorphose at 4 µM than did nicotinamide at the same concentration (Figure 3). β-NAD, however, did not stimulate any metamorphosis at 0.5, 1, or 5 mM.

Bottom Line: In contrast, neither lumichrome, thiamine HCl, pyridoxine HCl, nor vitamin B12 stimulated larvae of C. teleta to metamorphose at concentrations as high as 500 µM.Larvae also did not metamorphose in response to either nicotinamide or pyrazinecarboxamide in calcium-free seawater or with the addition of 4-acetylpyridine, a competitive inhibitor of the pyridine receptor.Together, these results suggest that larvae of C. teleta are responding to nicotinamide and riboflavin via a chemosensory pyridine receptor similar to that previously reported to be present on crayfish chela and involved with food recognition.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Tufts University, Medford, Massachusetts, United States of America.

ABSTRACT
Marine sediments can contain B vitamins, presumably incorporated from settled, decaying phytoplankton and microorganisms associated with decomposition. Because B vitamins may be advantageous for the energetically intensive processes of metamorphosis, post-metamorphic growth, and reproduction, we tested several B vitamins to determine if they would stimulate larvae of the deposit-feeding polychaete Capitella teleta to settle and metamorphose. Nicotinamide and riboflavin individually stimulated larvae of C. teleta to settle and metamorphose, generally within 1-2 hours at nicotinamide concentrations as low as 3 µM and riboflavin concentrations as low as 50 µM. More than 80% of the larvae metamorphosed within 30 minutes at a nicotinamide concentration of 7 µM. The pyridine channel agonist pyrazinecarboxamide also stimulated metamorphosis at very low concentrations. In contrast, neither lumichrome, thiamine HCl, pyridoxine HCl, nor vitamin B12 stimulated larvae of C. teleta to metamorphose at concentrations as high as 500 µM. Larvae also did not metamorphose in response to either nicotinamide or pyrazinecarboxamide in calcium-free seawater or with the addition of 4-acetylpyridine, a competitive inhibitor of the pyridine receptor. Together, these results suggest that larvae of C. teleta are responding to nicotinamide and riboflavin via a chemosensory pyridine receptor similar to that previously reported to be present on crayfish chela and involved with food recognition. Our data are the first to implicate B vitamins as possible natural chemical settlement cues for marine invertebrate larvae.

Show MeSH
Related in: MedlinePlus