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Occurrence of Isopenicillin-N-Synthase Homologs in Bioluminescent Ctenophores and Implications for Coelenterazine Biosynthesis.

Francis WR, Shaner NC, Christianson LM, Powers ML, Haddock SH - PLoS ONE (2015)

Bottom Line: Pairwise identities and substitution rates reveal an unusually high degree of identity even between the most unrelated species.Additionally, two related groups of non-heme iron oxidases were found across all ctenophores, including those which are non-luminous, arguing against the involvement of these two gene groups in luminescence.Important residues for iron-binding are conserved across all proteins in the three groups, suggesting this function is still present.

View Article: PubMed Central - PubMed

Affiliation: Monterey Bay Aquarium Research Institute, 7700 Sandholdt Rd, Moss Landing, CA 95039, United States of America; Department of Ocean Sciences, University of California Santa Cruz, Santa Cruz, CA, United States of America.

ABSTRACT
The biosynthesis of the luciferin coelenterazine has remained a mystery for decades. While not all organisms that use coelenterazine appear to make it themselves, it is thought that ctenophores are a likely producer. Here we analyze the transcriptome data of 24 species of ctenophores, two of which have published genomes. The natural precursors of coelenterazine have been shown to be the amino acids L-tyrosine and L-phenylalanine, with the most likely biosynthetic pathway involving cyclization and further modification of the tripeptide Phe-Tyr-Tyr ("FYY"). Therefore, we searched the ctenophore transcriptome data for genes with the short peptide "FYY" as part of their coding sequence. We recovered a group of candidate genes for coelenterazine biosynthesis in the luminous species which encode a set of highly conserved non-heme iron oxidases similar to isopenicillin-N-synthase. These genes were absent in the transcriptomes and genome of the two non-luminous species. Pairwise identities and substitution rates reveal an unusually high degree of identity even between the most unrelated species. Additionally, two related groups of non-heme iron oxidases were found across all ctenophores, including those which are non-luminous, arguing against the involvement of these two gene groups in luminescence. Important residues for iron-binding are conserved across all proteins in the three groups, suggesting this function is still present. Given the known functions of other members of this protein superfamily are involved in heterocycle formation, we consider these genes to be top candidates for laboratory characterization or gene knockouts in the investigation of coelenterazine biosynthesis.

No MeSH data available.


Related in: MedlinePlus

Multiple sequence alignment of Mnemiopsis proteins.ML032920-35201 is the putative full-length protein that connects ML032920a and ML35201a. MLRB263549-p indicates it is a partial sequence, as exons are missing in the scaffolds. The consensus sequence is indicated below, where identical residues are shown by ‘*’ and similar residues are shown by ‘.’. Black boxes indicate the highly conserved residues putatively involved in iron and 2-oxoglutarate binding.
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pone.0128742.g003: Multiple sequence alignment of Mnemiopsis proteins.ML032920-35201 is the putative full-length protein that connects ML032920a and ML35201a. MLRB263549-p indicates it is a partial sequence, as exons are missing in the scaffolds. The consensus sequence is indicated below, where identical residues are shown by ‘*’ and similar residues are shown by ‘.’. Black boxes indicate the highly conserved residues putatively involved in iron and 2-oxoglutarate binding.

Mentions: We then examined the unfiltered gene models of M. leidyi and found two additional FYY-containing gene products in tandem on scaffold ML2635. The first one (MLRB263543) appeared to be complete and the second one (MLRB263549) was incomplete, as several exons were clearly missing. Based on the alignment to the other proteins (Fig 3), some of the missing exons would fall in regions with low sequencing coverage, represented only by “N”s in the genomic scaffold. The two proteins appeared to be nearly identical to each other, varying at three residues. Thus, we found two complete genes and two incomplete genes with the FYY ending.


Occurrence of Isopenicillin-N-Synthase Homologs in Bioluminescent Ctenophores and Implications for Coelenterazine Biosynthesis.

Francis WR, Shaner NC, Christianson LM, Powers ML, Haddock SH - PLoS ONE (2015)

Multiple sequence alignment of Mnemiopsis proteins.ML032920-35201 is the putative full-length protein that connects ML032920a and ML35201a. MLRB263549-p indicates it is a partial sequence, as exons are missing in the scaffolds. The consensus sequence is indicated below, where identical residues are shown by ‘*’ and similar residues are shown by ‘.’. Black boxes indicate the highly conserved residues putatively involved in iron and 2-oxoglutarate binding.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4488382&req=5

pone.0128742.g003: Multiple sequence alignment of Mnemiopsis proteins.ML032920-35201 is the putative full-length protein that connects ML032920a and ML35201a. MLRB263549-p indicates it is a partial sequence, as exons are missing in the scaffolds. The consensus sequence is indicated below, where identical residues are shown by ‘*’ and similar residues are shown by ‘.’. Black boxes indicate the highly conserved residues putatively involved in iron and 2-oxoglutarate binding.
Mentions: We then examined the unfiltered gene models of M. leidyi and found two additional FYY-containing gene products in tandem on scaffold ML2635. The first one (MLRB263543) appeared to be complete and the second one (MLRB263549) was incomplete, as several exons were clearly missing. Based on the alignment to the other proteins (Fig 3), some of the missing exons would fall in regions with low sequencing coverage, represented only by “N”s in the genomic scaffold. The two proteins appeared to be nearly identical to each other, varying at three residues. Thus, we found two complete genes and two incomplete genes with the FYY ending.

Bottom Line: Pairwise identities and substitution rates reveal an unusually high degree of identity even between the most unrelated species.Additionally, two related groups of non-heme iron oxidases were found across all ctenophores, including those which are non-luminous, arguing against the involvement of these two gene groups in luminescence.Important residues for iron-binding are conserved across all proteins in the three groups, suggesting this function is still present.

View Article: PubMed Central - PubMed

Affiliation: Monterey Bay Aquarium Research Institute, 7700 Sandholdt Rd, Moss Landing, CA 95039, United States of America; Department of Ocean Sciences, University of California Santa Cruz, Santa Cruz, CA, United States of America.

ABSTRACT
The biosynthesis of the luciferin coelenterazine has remained a mystery for decades. While not all organisms that use coelenterazine appear to make it themselves, it is thought that ctenophores are a likely producer. Here we analyze the transcriptome data of 24 species of ctenophores, two of which have published genomes. The natural precursors of coelenterazine have been shown to be the amino acids L-tyrosine and L-phenylalanine, with the most likely biosynthetic pathway involving cyclization and further modification of the tripeptide Phe-Tyr-Tyr ("FYY"). Therefore, we searched the ctenophore transcriptome data for genes with the short peptide "FYY" as part of their coding sequence. We recovered a group of candidate genes for coelenterazine biosynthesis in the luminous species which encode a set of highly conserved non-heme iron oxidases similar to isopenicillin-N-synthase. These genes were absent in the transcriptomes and genome of the two non-luminous species. Pairwise identities and substitution rates reveal an unusually high degree of identity even between the most unrelated species. Additionally, two related groups of non-heme iron oxidases were found across all ctenophores, including those which are non-luminous, arguing against the involvement of these two gene groups in luminescence. Important residues for iron-binding are conserved across all proteins in the three groups, suggesting this function is still present. Given the known functions of other members of this protein superfamily are involved in heterocycle formation, we consider these genes to be top candidates for laboratory characterization or gene knockouts in the investigation of coelenterazine biosynthesis.

No MeSH data available.


Related in: MedlinePlus