title: Diffusible gas transmitter signaling in the copepod crustacean Calanus finmarchicus: identification of the biosynthetic enzymes of nitric oxide (NO), carbon monoxide (CO) and hydrogen sulfide (H2S) using a de novo assembled transcriptome.
abstract: Neurochemical signaling is a major component of physiological/behavioral control throughout the animal kingdom. Gas transmitters are perhaps the most ancient class of molecules used by nervous systems for chemical communication. Three gases are generally recognized as being produced by neurons: nitric oxide (NO), carbon monoxide (CO) and hydrogen sulfide (H2S). As part of an ongoing effort to identify and characterize the neurochemical signaling systems of the copepod Calanus finmarchicus, the biomass dominant zooplankton in much of the North Atlantic Ocean, we have mined a de novo assembled transcriptome for sequences encoding the neuronal biosynthetic enzymes of these gases, i.e. nitric oxide synthase (NOS), heme oxygenase (HO) and cystathionine β-synthase (CBS), respectively. Using Drosophila proteins as queries, two NOS-, one HO-, and one CBS-encoding transcripts were identified. Reverse BLAST and structural analyses of the deduced proteins suggest that each is a true member of its respective enzyme family. RNA-Seq data collected from embryos, early nauplii, late nauplii, early copepodites, late copepodites and adults revealed the expression of each transcript to be stage specific: one NOS restricted primarily to the embryo and the other was absent in the embryo but expressed in all other stages, no CBS expression in the embryo, but present in all other stages, and HO expressed across all developmental stages. Given the importance of gas transmitters in the regulatory control of a number of physiological processes, these data open opportunities for investigating the roles these proteins play under different life-stage and environmental conditions in this ecologically important species.
authors.affiliation: Békésy Laboratory of Neurobiology, Pacific Biosciences Research Center, University of Hawaii at Manoa, 1993 East-West Road, Honolulu, HI 96822, USA. Electronic address: crabman@pbrc.hawaii.edu.
authors.forename: Andrew E
authors.initials: AE
authors.lastname: Christie
authors.affiliation: Békésy Laboratory of Neurobiology, Pacific Biosciences Research Center, University of Hawaii at Manoa, 1993 East-West Road, Honolulu, HI 96822, USA.
authors.forename: Tiana M
authors.initials: TM
authors.lastname: Fontanilla
authors.affiliation: Békésy Laboratory of Neurobiology, Pacific Biosciences Research Center, University of Hawaii at Manoa, 1993 East-West Road, Honolulu, HI 96822, USA.
authors.forename: Vittoria
authors.initials: V
authors.lastname: Roncalli
authors.affiliation: Békésy Laboratory of Neurobiology, Pacific Biosciences Research Center, University of Hawaii at Manoa, 1993 East-West Road, Honolulu, HI 96822, USA.
authors.forename: Matthew C
authors.initials: MC
authors.lastname: Cieslak
authors.affiliation: Békésy Laboratory of Neurobiology, Pacific Biosciences Research Center, University of Hawaii at Manoa, 1993 East-West Road, Honolulu, HI 96822, USA.
authors.forename: Petra H
authors.initials: PH
authors.lastname: Lenz
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D001483:Base Sequence; D053898:Biosynthetic Pathways / Q000235:genetics; D002248:Carbon Monoxide / Q000378:metabolism*; D033342:Copepoda / Q000201:enzymology* / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism; D003541:Cystathionine beta-Synthase / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D004058:Diffusion; D020224:Expressed Sequence Tags; D005260:Female; D018507:Gene Expression Regulation, Developmental; D006419:Heme Oxygenase (Decyclizing) / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D006862:Hydrogen Sulfide / Q000378:metabolism*; D007527:Isoenzymes / Q000378:metabolism; D008969:Molecular Sequence Data; D009569:Nitric Oxide / Q000378:metabolism*; D019001:Nitric Oxide Synthase / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D010802:Phylogeny; D017434:Protein Structure, Tertiary; D016415:Sequence Alignment; D015398:Signal Transduction / Q000235:genetics*; D059467:Transcriptome / Q000235:genetics; D014714:Vertebrates / Q000378:metabolism
chemical_list: D007527:Isoenzymes; D009569:Nitric Oxide; D002248:Carbon Monoxide; D019001:Nitric Oxide Synthase; D006419:Heme Oxygenase (Decyclizing); D003541:Cystathionine beta-Synthase; D006862:Hydrogen Sulfide
keywords: Cystathionine β-synthase (CBS); Heme oxygenase (HO); Illumina sequencing; Neuromodulator; Neurotransmitter; Nitric oxide synthase (NOS)
references.citation: PLoS One. 2014 Feb 19;9(2):e88589
references.pmid: 24586345
references.citation: Dev Comp Immunol. 2009 Sep;33(9):1000-10
references.pmid: 19416737
references.citation: Am J Psychiatry. 2000 Nov;157(11):1738-51
references.pmid: 11058466
references.citation: Pigment Cell Melanoma Res. 2008 Apr;21(2):184-91
references.pmid: 18426411
references.citation: J Exp Biol. 2007 Sep;210(Pt 18):3245-54
references.pmid: 17766302
references.citation: Gen Comp Endocrinol. 2014 Jan 1;195:28-39
references.pmid: 24148657
references.citation: J Exp Biol. 2004 Jul;207(Pt 16):2845-57
references.pmid: 15235013
references.citation: Biochem Biophys Res Commun. 2008 Dec 26;377(4):1156-61
references.pmid: 18983822
references.citation: Comp Biochem Physiol Part D Genomics Proteomics. 2012 Jun;7(2):124-60
references.pmid: 22305610
references.citation: Dev Dyn. 2007 Nov;236(11):3047-60
references.pmid: 17948307
references.citation: Nucleic Acids Res. 1997 Sep 1;25(17):3389-402
references.pmid: 9254694
references.citation: Comp Biochem Physiol Part D Genomics Proteomics. 2013 Sep;8(3):165-93
references.pmid: 23727418
references.citation: Science. 2002 May 31;296(5573):1692-4
references.pmid: 12040196
references.citation: J Mol Med (Berl). 2012 Mar;90(3):255-63
references.pmid: 22314625
references.citation: Annu Rev Biochem. 2010;79:445-70
references.pmid: 20370423
references.citation: Fish Shellfish Immunol. 2012 Apr;32(4):503-12
references.pmid: 22200639
references.citation: Fish Shellfish Immunol. 2010 Apr;28(4):701-11
references.pmid: 20109558
references.citation: Dokl Biol Sci. 2011 Mar-Apr;437:94-6
references.pmid: 21562955
references.citation: J Comp Neurol. 2002 Dec 9;454(2):158-67
references.pmid: 12412140
references.citation: Annu Rev Neurosci. 2003;26:105-31
references.pmid: 14527267
references.citation: Eur J Neurosci. 2005 May;21(10):2767-81
references.pmid: 15926924
references.citation: Sci Signal. 2009 Apr 28;2(68):re2
references.pmid: 19401594
references.citation: Gen Comp Endocrinol. 2013 Jun 15;187:117-35
references.pmid: 23578900
references.citation: Genome Biol. 2009;10(3):R25
references.pmid: 19261174
references.citation: Neuroreport. 2000 Apr 27;11(6):1273-6
references.pmid: 10817606
references.citation: Photochem Photobiol. 2010 Nov-Dec;86(6):1278-84
references.pmid: 21091482
references.citation: Mol Biol Evol. 2013 Apr;30(4):772-80
references.pmid: 23329690
references.citation: Trends Microbiol. 2009 May;17(5):212-8
references.pmid: 19375324
references.citation: Cell Tissue Res. 2011 Jul;345(1):41-67
references.pmid: 21597913
references.citation: Comp Biochem Physiol Part D Genomics Proteomics. 2012 Jun;7(2):110-23
references.pmid: 22277925
references.citation: Science. 2011 Feb 4;331(6017):555-61
references.pmid: 21292972
references.citation: Trends Microbiol. 2006 Oct;14(10):456-62
references.pmid: 16908154
references.citation: Development. 2009 Jan;136(1):85-93
references.pmid: 19019991
references.citation: Biol Bull. 2012 Oct;223(2):178-91
references.pmid: 23111130
references.citation: Fish Shellfish Immunol. 2010 Jan;28(1):49-55
references.pmid: 19800009
references.citation: Comp Biochem Physiol B Biochem Mol Biol. 2006 May;144(1):11-7
references.pmid: 16516518
references.citation: J Neurosci. 2001 Mar 1;21(5):1610-8
references.pmid: 11222651
references.citation: Nitric Oxide. 2011 Nov 30;25(4):396-406
references.pmid: 21971212
references.citation: Comp Biochem Physiol Part D Genomics Proteomics. 2013 Mar;8(1):45-57
references.pmid: 23262277
references.citation: J Neurosci. 2004 Mar 17;24(11):2813-24
references.pmid: 15028775
references.citation: J Exp Biol. 2001 Apr;204(Pt 7):1319-32
references.pmid: 11249841
references.citation: Fish Shellfish Immunol. 2010 Sep;29(3):469-79
references.pmid: 20580828
references.citation: Nature. 2003 Dec 11;426(6967):661-4
references.pmid: 14668864
references.citation: J Neurobiol. 2004 Jun;59(3):331-42
references.pmid: 15146549
references.citation: Physiol Rev. 2012 Apr;92(2):791-896
references.pmid: 22535897
references.citation: Fish Shellfish Immunol. 2010 Mar;28(3):453-60
references.pmid: 20026409
references.citation: J Neurobiol. 2002 Aug;52(2):144-55
references.pmid: 12124752
references.citation: Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):10996-1002
references.pmid: 11572959
references.citation: Trends Neurosci. 2001 Feb;24(2):99-106
references.pmid: 11164940
references.citation: Nitric Oxide. 2006 May;14(3):219-27
references.pmid: 16403661
references.citation: J Exp Biol. 2012 Nov 1;215(Pt 21):3813-22
references.pmid: 22855617
references.citation: Eur J Neurosci. 2008 Jun;27(11):2783-802
references.pmid: 18588525
references.citation: Front Physiol. 2013 Feb 21;4:27
references.pmid: 23437016
references.citation: Proc Natl Acad Sci U S A. 2011 Oct 4;108(40):16831-6
references.pmid: 21930912
references.citation: Nucleic Acids Res. 2012 Jan;40(Database issue):D290-301
references.pmid: 22127870
references.citation: Science. 2000 Mar 24;287(5461):2185-95
references.pmid: 10731132
references.citation: J Exp Biol. 2007 Sep;210(Pt 18):3179-87
references.pmid: 17766295
references.citation: J Exp Biol. 2000 Dec;203(Pt 23):3595-602
references.pmid: 11060220
references.citation: Curr Pharm Biotechnol. 2012 May;13(6):760-8
references.pmid: 22201612
references.citation: J Neurochem. 2010 Apr;113(1):14-26
references.pmid: 20067586
references.citation: Comp Biochem Physiol A Mol Integr Physiol. 2011 Jan;158(1):150-62
references.pmid: 20959144
references.citation: J Comp Neurol. 2003 Dec 15;467(3):293-306
references.pmid: 14608595