Mass spectrometry analysis and transcriptome sequencing reveal glowing squid crystal proteins are in the same superfamily as firefly luciferase

The Japanese firefly squid Hotaru-ika ( Watasenia scintillans ) produces intense blue light from photophores at the tips of two arms. These photophores are densely packed with protein microcrystals that catalyse the bioluminescent reaction using ATP and the substrate coelenterazine disulfate. The sq...

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Published inScientific reports Vol. 6; no. 1; p. 27638
Main Authors Gimenez, Gregory, Metcalf, Peter, Paterson, Neil G., Sharpe, Miriam L.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 09.06.2016
Nature Publishing Group
Subjects
631/337/2019
631/45/612
Adenosine Triphosphate - metabolism
Animals
ATP
Bioluminescence
Crystals
Decapodiformes - enzymology
Decapodiformes - genetics
Enzymes
Fireflies - enzymology
Fireflies - genetics
Genomes
Humanities and Social Sciences
Light
Luciferases - chemistry
Luciferases - genetics
Luciferases - metabolism
Luciferin
Mass spectrometry
multidisciplinary
Photophores
Polyethylene glycol
Proteins
Science
Scientific imaging
Sequence Homology, Amino Acid
Sucrose
Transcriptome
New Zealand
Online AccessGet full text

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Abstract The Japanese firefly squid Hotaru-ika ( Watasenia scintillans ) produces intense blue light from photophores at the tips of two arms. These photophores are densely packed with protein microcrystals that catalyse the bioluminescent reaction using ATP and the substrate coelenterazine disulfate. The squid is the only organism known to produce light using protein crystals. We extracted microcrystals from arm tip photophores and identified the constituent proteins using mass spectrometry and transcriptome libraries prepared from arm tip tissue. The crystals contain three proteins, wsluc1–3, all members of the ANL superfamily of adenylating enzymes. They share 19 to 21% sequence identity with firefly luciferases, which produce light using ATP and the unrelated firefly luciferin substrate. We propose that wsluc1–3 form a complex that crystallises inside the squid photophores and that in the crystal one or more of the proteins catalyses the production of light using coelenterazine disulfate and ATP. These results suggest that ANL superfamily enzymes have independently evolved in distant species to produce light using unrelated substrates.
AbstractList The Japanese firefly squid Hotaru-ika ( Watasenia scintillans ) produces intense blue light from photophores at the tips of two arms. These photophores are densely packed with protein microcrystals that catalyse the bioluminescent reaction using ATP and the substrate coelenterazine disulfate. The squid is the only organism known to produce light using protein crystals. We extracted microcrystals from arm tip photophores and identified the constituent proteins using mass spectrometry and transcriptome libraries prepared from arm tip tissue. The crystals contain three proteins, wsluc1–3, all members of the ANL superfamily of adenylating enzymes. They share 19 to 21% sequence identity with firefly luciferases, which produce light using ATP and the unrelated firefly luciferin substrate. We propose that wsluc1–3 form a complex that crystallises inside the squid photophores and that in the crystal one or more of the proteins catalyses the production of light using coelenterazine disulfate and ATP. These results suggest that ANL superfamily enzymes have independently evolved in distant species to produce light using unrelated substrates.
The Japanese firefly squid Hotaru-ika (Watasenia scintillans) produces intense blue light from photophores at the tips of two arms. These photophores are densely packed with protein microcrystals that catalyse the bioluminescent reaction using ATP and the substrate coelenterazine disulfate. The squid is the only organism known to produce light using protein crystals. We extracted microcrystals from arm tip photophores and identified the constituent proteins using mass spectrometry and transcriptome libraries prepared from arm tip tissue. The crystals contain three proteins, wsluc1-3, all members of the ANL superfamily of adenylating enzymes. They share 19 to 21% sequence identity with firefly luciferases, which produce light using ATP and the unrelated firefly luciferin substrate. We propose that wsluc1-3 form a complex that crystallises inside the squid photophores, and that in the crystal one or more of the proteins catalyses the production of light using coelenterazine disulfate and ATP. These results suggest that ANL superfamily enzymes have independently evolved in distant species to produce light using unrelated substrates.The Japanese firefly squid Hotaru-ika (Watasenia scintillans) produces intense blue light from photophores at the tips of two arms. These photophores are densely packed with protein microcrystals that catalyse the bioluminescent reaction using ATP and the substrate coelenterazine disulfate. The squid is the only organism known to produce light using protein crystals. We extracted microcrystals from arm tip photophores and identified the constituent proteins using mass spectrometry and transcriptome libraries prepared from arm tip tissue. The crystals contain three proteins, wsluc1-3, all members of the ANL superfamily of adenylating enzymes. They share 19 to 21% sequence identity with firefly luciferases, which produce light using ATP and the unrelated firefly luciferin substrate. We propose that wsluc1-3 form a complex that crystallises inside the squid photophores, and that in the crystal one or more of the proteins catalyses the production of light using coelenterazine disulfate and ATP. These results suggest that ANL superfamily enzymes have independently evolved in distant species to produce light using unrelated substrates.
The Japanese firefly squid Hotaru-ika (Watasenia scintillans) produces intense blue light from photophores at the tips of two arms. These photophores are densely packed with protein microcrystals that catalyse the bioluminescent reaction using ATP and the substrate coelenterazine disulfate. The squid is the only organism known to produce light using protein crystals. We extracted microcrystals from arm tip photophores and identified the constituent proteins using mass spectrometry and transcriptome libraries prepared from arm tip tissue. The crystals contain three proteins, wsluc1-3, all members of the ANL superfamily of adenylating enzymes. They share 19 to 21% sequence identity with firefly luciferases, which produce light using ATP and the unrelated firefly luciferin substrate. We propose that wsluc1-3 form a complex that crystallises inside the squid photophores, and that in the crystal one or more of the proteins catalyses the production of light using coelenterazine disulfate and ATP. These results suggest that ANL superfamily enzymes have independently evolved in distant species to produce light using unrelated substrates.
ArticleNumber 27638
Author Paterson, Neil G.
Gimenez, Gregory
Metcalf, Peter
Sharpe, Miriam L.
Author_xml – sequence: 1
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  organization: Otago Genomics & Bioinformatics Facility, University of Otago
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  surname: Metcalf
  fullname: Metcalf, Peter
  organization: School of Biological Sciences, University of Auckland
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  givenname: Neil G.
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  givenname: Miriam L.
  surname: Sharpe
  fullname: Sharpe, Miriam L.
  organization: Department of Biochemistry, University of Otago
BackLink https://www.ncbi.nlm.nih.gov/pubmed/27279452$$D View this record in MEDLINE/PubMed
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Snippet The Japanese firefly squid Hotaru-ika ( Watasenia scintillans ) produces intense blue light from photophores at the tips of two arms. These photophores are...
The Japanese firefly squid Hotaru-ika (Watasenia scintillans) produces intense blue light from photophores at the tips of two arms. These photophores are...
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StartPage 27638
SubjectTerms 631/337/2019
631/45/612
Adenosine Triphosphate - metabolism
Animals
ATP
Bioluminescence
Crystals
Decapodiformes - enzymology
Decapodiformes - genetics
Enzymes
Fireflies - enzymology
Fireflies - genetics
Genomes
Humanities and Social Sciences
Light
Luciferases - chemistry
Luciferases - genetics
Luciferases - metabolism
Luciferin
Mass spectrometry
multidisciplinary
Photophores
Polyethylene glycol
Proteins
Science
Scientific imaging
Sequence Homology, Amino Acid
Sucrose
Transcriptome
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Title Mass spectrometry analysis and transcriptome sequencing reveal glowing squid crystal proteins are in the same superfamily as firefly luciferase
URI https://link.springer.com/article/10.1038/srep27638
https://www.ncbi.nlm.nih.gov/pubmed/27279452
https://www.proquest.com/docview/1795534913
https://www.proquest.com/docview/1795877668
https://pubmed.ncbi.nlm.nih.gov/PMC4899746
Volume 6
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