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Molecular characterization of putative neuropeptide, amine, diffusible gas and small molecule transmitter biosynthetic enzymes in the eyestalk ganglia of the American lobster, Homarus americanus

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Invertebrate Neuroscience

Abstract

The American lobster, Homarus americanus, is a model for investigating the neuromodulatory control of physiology and behavior. Prior studies have shown that multiple classes of chemicals serve as locally released/circulating neuromodulators/neurotransmitters in this species. Interestingly, while many neuroactive compounds are known from Homarus, little work has focused on identifying/characterizing the enzymes responsible for their biosynthesis, despite the fact that these enzymes are key components for regulating neuromodulation/neurotransmission. Here, an eyestalk ganglia-specific transcriptome was mined for transcripts encoding enzymes involved in neuropeptide, amine, diffusible gas and small molecule transmitter biosynthesis. Using known Drosophila melanogaster proteins as templates, transcripts encoding putative Homarus homologs of peptide precursor processing (signal peptide peptidase, prohormone processing protease and carboxypeptidase) and immature peptide modifying (glutaminyl cyclase, tyrosylprotein sulfotransferase, protein disulfide isomerase, peptidylglycine-α-hydroxylating monooxygenase and peptidyl-α-hydroxyglycine-α-amidating lyase) enzymes were identified in the eyestalk assembly. Similarly, transcripts encoding full complements of the enzymes responsible for dopamine [tryptophan-phenylalanine hydroxylase (TPH), tyrosine hydroxylase and DOPA decarboxylase (DDC)], octopamine (TPH, tyrosine decarboxylase and tyramine β-hydroxylase), serotonin (TPH or tryptophan hydroxylase and DDC) and histamine (histidine decarboxylase) biosynthesis were identified from the eyestalk ganglia, as were those responsible for the generation of the gases nitric oxide (nitric oxide synthase) and carbon monoxide (heme oxygenase), and the small molecule transmitters acetylcholine (choline acetyltransferase), glutamate (glutaminase) and GABA (glutamic acid decarboxylase). The presence and identity of the transcriptome-derived transcripts were confirmed using RT-PCR. The data presented here provide a foundation for future gene-based studies of neuromodulatory control at the level of neurotransmitter/modulator biosynthesis in Homarus.

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Acknowledgements

This study was funded by the National Science Foundation (IOS-1353023 and IOS-1354567), the National Institutes of Health (5P20RR016463-12 and 8P20GM103423-12), base CRIS funding (Project #2020-22620-022-00D), the Arnold and Mabel Beckman Foundation, the Cades Foundation of Honolulu, Hawaii, and a gift from the Henry L. and Grace Doherty Charitable Foundation to Bowdoin College. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U. S. Department of Agriculture. USDA is an equal opportunity provider and employer.

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Authors and Affiliations

  1. Békésy Laboratory of Neurobiology, Pacific Biosciences Research Center, School of Ocean and Earth Science and Technology, University of Hawaii at Manoa, 1993 East-West Road, Honolulu, HI, 96822, USA

    Andrew E. Christie, Micah G. Pascual & Andy Yu

  2. Department of Biology, Bowdoin College, 6500 College Station, Brunswick, ME, 04011, USA

    Meredith E. Stanhope, Helen I. Gandler, Tess J. Lameyer, Devlin N. Shea & Patsy S. Dickinson

  3. Pest Management and Biocontrol Research Unit, US Arid Land Agricultural Research Center, USDA Agricultural Research Services, Maricopa, AZ, 85138, USA

    J. Joe Hull

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  1. Andrew E. Christie
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  2. Meredith E. Stanhope
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  3. Helen I. Gandler
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Correspondence to Andrew E. Christie.

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Online Resource 1

Amino acid sequences of putative neuromodulator biosynthetic enzymes deduced from Homarus americanus eyestalk ganglia-specific transcripts. (A) Homarus americanus signal peptide peptidase (Homam-SPP). (B) Homarus americanus prohormone processing protease (Homam-PPP). (C) Homarus americanus carboxypeptidase (Homam-CP). (D) Homarus americanus glutaminyl cyclase (Homam-QC). (E) Homarus americanus tyrosylprotein sulfotransferase (Homam-TPST). (F1-2) Homarus americanus protein disulfide isomerase (Homam-PDI) variants. (G) Homarus americanus peptidylglycine α-hydroxylating monooxygenase (Homam-PHM). (H1-3) Homarus americanus peptidyl-α-hydroxyglycine-α-amidating lyase (Homam-PAL) proteins and variants. (I1-4) Homarus americanus tryptophan-phenylalanine hydroxylase (Homam-TPH) variants. (J) Homarus americanus tyrosine hydroxylase (Homam-TH). (K) Homarus americanus DOPA decarboxylase (Homam-DDC). (L) Homarus americanus tyrosine decarboxylase (Homam-TDC). (M) Homarus americanus tyramine β-hydroxylase (Homam-TBH). (N) Homarus americanus tryptophan hydroxylase (Homam-TRH). (O1-2) Homarus americanus histidine decarboxylase (Homam-HDC) partial proteins. (P1-5) Homarus americanus nitric oxide synthase (Homam-NOS) variants. (Q1-2) Homarus americanus heme oxygenase (Homam-HO) variants. (R) Homarus americanus choline acetyltransferase (Homam-CHAT). (S1-6) Homarus americanus glutaminase (Homam-GLS) proteins and variants. (T1-2) Homarus americanus glutamic acid decarboxylase (Homam-GAD) proteins. A “+” symbol on the amino- or carboxyl-terminus indicates the presence of additional unknown amino acids (DOC 73 kb)

Online Resource 2

Table of oligonucleotide primers used for RT-PCR (XLSX 11 kb)

Online Resource 3

Table of amino acid sequences used for phylogenetic analysis of hydroxylases (XLSX 61 kb)

Online Resource 4

Table of amino acid sequences used for phylogenetic analysis of decarboxylases (XLSX 62 kb)

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Christie, A.E., Stanhope, M.E., Gandler, H.I. et al. Molecular characterization of putative neuropeptide, amine, diffusible gas and small molecule transmitter biosynthetic enzymes in the eyestalk ganglia of the American lobster, Homarus americanus. Invert Neurosci 18, 12 (2018). https://doi.org/10.1007/s10158-018-0216-4

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