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An annotated CNS transcriptome of the medicinal leech, Hirudo verbana: De novo sequencing to characterize genes associated with nervous system activity
research-article
Author(s):
Adam J. Northcutt
1 ,
Eva K. Fischer
2 ,
Joshua G. Puhl
3 ,
Karen A. Mesce
3 ,
David J. Schulz
1
,
*
Publication date (Electronic):
20 July 2018
Journal:
PLoS ONE
Publisher:
Public Library of Science
Read this article at
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Abstract
The medicinal leech is one of the most venerated model systems for the study of fundamental nervous system principles, ranging from single-cell excitability to complex sensorimotor integration. Yet, molecular analyses have yet to be extensively applied to complement the rich history of electrophysiological study that this animal has received. Here, we generated the first de novo transcriptome assembly from the entire central nervous system of Hirudo verbana, with the goal of providing a molecular resource, as well as to lay the foundation for a comprehensive discovery of genes fundamentally important for neural function. Our assembly generated 107,704 contigs from over 900 million raw reads. Of these 107,704 contigs, 39,047 (36%) were annotated using NCBI’s validated RefSeq sequence database. From this annotated central nervous system transcriptome, we began the process of curating genes related to nervous system function by identifying and characterizing 126 unique ion channel, receptor, transporter, and enzyme contigs. Additionally, we generated sequence counts to estimate the relative abundance of each identified ion channel and receptor contig in the transcriptome through Kallisto mapping. This transcriptome will serve as a valuable community resource for studies investigating the molecular underpinnings of neural function in leech and provide a reference for comparative analyses.
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Most cited references70
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T G Burland (2000)
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- Abstract: found
- Article: not found
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The exponential growth in the volume of accessible biological information has generated a confusion of voices surrounding the annotation of molecular information about genes and their products. The Gene Ontology (GO) project seeks to provide a set of structured vocabularies for specific biological domains that can be used to describe gene products in any organism. This work includes building three extensive ontologies to describe molecular function, biological process, and cellular component, and providing a community database resource that supports the use of these ontologies. The GO Consortium was initiated by scientists associated with three model organism databases: SGD, the Saccharomyces Genome database; FlyBase, the Drosophila genome database; and MGD/GXD, the Mouse Genome Informatics databases. Additional model organism database groups are joining the project. Each of these model organism information systems is annotating genes and gene products using GO vocabulary terms and incorporating these annotations into their respective model organism databases. Each database contributes its annotation files to a shared GO data resource accessible to the public at http://www.geneontology.org/. The GO site can be used by the community both to recover the GO vocabularies and to access the annotated gene product data sets from the model organism databases. The GO Consortium supports the development of the GO database resource and provides tools enabling curators and researchers to query and manipulate the vocabularies. We believe that the shared development of this molecular annotation resource will contribute to the unification of biological information.
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Neuronal transcriptome of Aplysia: neuronal compartments and circuitry.
Sami H. Jezzini, William Farmerie, Peter V Lovell … (2006)
Molecular analyses of Aplysia, a well-established model organism for cellular and systems neural science, have been seriously handicapped by a lack of adequate genomic information. By sequencing cDNA libraries from the central nervous system (CNS), we have identified over 175,000 expressed sequence tags (ESTs), of which 19,814 are unique neuronal gene products and represent 50%-70% of the total Aplysia neuronal transcriptome. We have characterized the transcriptome at three levels: (1) the central nervous system, (2) the elementary components of a simple behavior: the gill-withdrawal reflex-by analyzing sensory, motor, and serotonergic modulatory neurons, and (3) processes of individual neurons. In addition to increasing the amount of available gene sequences of Aplysia by two orders of magnitude, this collection represents the largest database available for any member of the Lophotrochozoa and therefore provides additional insights into evolutionary strategies used by this highly successful diversified lineage, one of the three proposed superclades of bilateral animals.
Author and article information
Contributors
Adam J. Northcutt:
ORCID: http://orcid.org/0000-0001-5815-1854
Role: ConceptualizationRole: Data curationRole: Formal analysisRole: VisualizationRole:
Writing – original draftRole: Writing – review & editing
Eva K. Fischer: Role: Data curationRole: Formal analysisRole: MethodologyRole: SoftwareRole: Writing
– review & editing
Joshua G. Puhl: Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Writing – review
& editing
Karen A. Mesce: Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole:
ResourcesRole: Writing – review & editing
David J. Schulz:
ORCID: http://orcid.org/0000-0003-4532-5362
Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: Project
administrationRole: SupervisionRole: VisualizationRole: Writing – original draftRole:
Writing – review & editing
Maurice J. Chacron: Role: Editor
Journal
Journal ID (nlm-ta): PLoS One
Journal ID (iso-abbrev): PLoS ONE
Journal ID (publisher-id): plos
Journal ID (pmc): plosone
Title:
PLoS ONE
Publisher:
Public Library of Science
(San Francisco, CA USA
)
ISSN
(Electronic):
1932-6203
Publication date
(Electronic):
20
July
2018
Publication date Collection: 2018
Volume: 13
Issue: 7
Electronic Location Identifier: e0201206
Affiliations
[1
]
Division of Biological Sciences, University of Missouri-Columbia, Columbia, Missouri,
United States of America
Author notes
* E-mail:
schulzd@
123456missouri.edu
Author information
Adam J. Northcutt
http://orcid.org/0000-0001-5815-1854
David J. Schulz
http://orcid.org/0000-0003-4532-5362
Article
Publisher ID: PONE-D-18-09992DOI: 10.1371/journal.pone.0201206
PMC ID: 6054404
PubMed ID: 30028871
SO-VID: dc4b5aaf-e7ff-42c4-9ea1-1d95a21353d0
Copyright © © 2018 Northcutt et al
License:
This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
History
Date
received
: 3
April
2018
Date
accepted
: 10
July
2018
Page count
Figures: 15,
Tables: 8,
Pages: 33
Funding
Funded by: funder-id http://dx.doi.org/10.13039/100000076, Directorate for Biological Sciences;
Award ID: 1454904
Award Recipient
:
Karen A. Mesce
This work was funded by a grant from the National Science Foundation (DBS-IOS #1454904)
awarded to Karen Mesce and David Schulz.
Categories
Subject:
Research Article
Subject:
Biology and Life Sciences
Subject:
Computational Biology
Subject:
Genome Analysis
Subject:
Transcriptome Analysis
Subject:
Biology and Life Sciences
Subject:
Genetics
Subject:
Genomics
Subject:
Genome Analysis
Subject:
Transcriptome Analysis
Subject:
Biology and Life Sciences
Subject:
Anatomy
Subject:
Nervous System
Subject:
Central Nervous System
Subject:
Medicine and Health Sciences
Subject:
Anatomy
Subject:
Nervous System
Subject:
Central Nervous System
Subject:
Biology and Life Sciences
Subject:
Organisms
Subject:
Eukaryota
Subject:
Animals
Subject:
Invertebrates
Subject:
Annelids
Subject:
Leeches
Subject:
Biology and Life Sciences
Subject:
Biophysics
Subject:
Ion Channels
Subject:
Transient Receptor Potential Channels
Subject:
Physical Sciences
Subject:
Physics
Subject:
Biophysics
Subject:
Ion Channels
Subject:
Transient Receptor Potential Channels
Subject:
Biology and Life Sciences
Subject:
Physiology
Subject:
Electrophysiology
Subject:
Ion Channels
Subject:
Transient Receptor Potential Channels
Subject:
Medicine and Health Sciences
Subject:
Physiology
Subject:
Electrophysiology
Subject:
Ion Channels
Subject:
Transient Receptor Potential Channels
Subject:
Biology and Life Sciences
Subject:
Physiology
Subject:
Electrophysiology
Subject:
Neurophysiology
Subject:
Ion Channels
Subject:
Transient Receptor Potential Channels
Subject:
Medicine and Health Sciences
Subject:
Physiology
Subject:
Electrophysiology
Subject:
Neurophysiology
Subject:
Ion Channels
Subject:
Transient Receptor Potential Channels
Subject:
Biology and Life Sciences
Subject:
Neuroscience
Subject:
Neurophysiology
Subject:
Ion Channels
Subject:
Transient Receptor Potential Channels
Subject:
Biology and Life Sciences
Subject:
Biochemistry
Subject:
Proteins
Subject:
Ion Channels
Subject:
Transient Receptor Potential Channels
Subject:
Biology and Life Sciences
Subject:
Biophysics
Subject:
Ion Channels
Subject:
Potassium Channels
Subject:
Physical Sciences
Subject:
Physics
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Biophysics
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Ion Channels
Subject:
Potassium Channels
Subject:
Biology and Life Sciences
Subject:
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Subject:
Electrophysiology
Subject:
Ion Channels
Subject:
Potassium Channels
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Medicine and Health Sciences
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Subject:
Ion Channels
Subject:
Potassium Channels
Subject:
Biology and Life Sciences
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Electrophysiology
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Subject:
Ion Channels
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Medicine and Health Sciences
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Ion Channels
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Neurophysiology
Subject:
Ion Channels
Subject:
Potassium Channels
Subject:
Biology and Life Sciences
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Biochemistry
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Proteins
Subject:
Ion Channels
Subject:
Potassium Channels
Subject:
Biology and Life Sciences
Subject:
Biophysics
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Ion Channels
Subject:
Physical Sciences
Subject:
Physics
Subject:
Biophysics
Subject:
Ion Channels
Subject:
Biology and Life Sciences
Subject:
Physiology
Subject:
Electrophysiology
Subject:
Ion Channels
Subject:
Medicine and Health Sciences
Subject:
Physiology
Subject:
Electrophysiology
Subject:
Ion Channels
Subject:
Biology and Life Sciences
Subject:
Physiology
Subject:
Electrophysiology
Subject:
Neurophysiology
Subject:
Ion Channels
Subject:
Medicine and Health Sciences
Subject:
Physiology
Subject:
Electrophysiology
Subject:
Neurophysiology
Subject:
Ion Channels
Subject:
Biology and Life Sciences
Subject:
Neuroscience
Subject:
Neurophysiology
Subject:
Ion Channels
Subject:
Biology and Life Sciences
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Biochemistry
Subject:
Proteins
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Subject:
Research and Analysis Methods
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Database and Informatics Methods
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Biological Databases
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Research and Analysis Methods
Subject:
Database and Informatics Methods
Subject:
Bioinformatics
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Sequence Analysis
Subject:
Sequence Databases
Subject:
Biology and Life Sciences
Subject:
Biophysics
Subject:
Ion Channels
Subject:
Ligand-Gated Ion Channels
Subject:
Physical Sciences
Subject:
Physics
Subject:
Biophysics
Subject:
Ion Channels
Subject:
Ligand-Gated Ion Channels
Subject:
Biology and Life Sciences
Subject:
Physiology
Subject:
Electrophysiology
Subject:
Ion Channels
Subject:
Ligand-Gated Ion Channels
Subject:
Medicine and Health Sciences
Subject:
Physiology
Subject:
Electrophysiology
Subject:
Ion Channels
Subject:
Ligand-Gated Ion Channels
Subject:
Biology and Life Sciences
Subject:
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Electrophysiology
Subject:
Neurophysiology
Subject:
Ion Channels
Subject:
Ligand-Gated Ion Channels
Subject:
Medicine and Health Sciences
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Subject:
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Subject:
Ion Channels
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Ligand-Gated Ion Channels
Subject:
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Subject:
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Subject:
Ion Channels
Subject:
Ligand-Gated Ion Channels
Subject:
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Subject:
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Subject:
Proteins
Subject:
Ion Channels
Subject:
Ligand-Gated Ion Channels
Custom metadata
Data Availability The
H. verbana Trinity assembled Transcriptome Shotgun Assembly (TSA) project has been deposited
at DDBJ/ENA/GenBank (BioProject No. PRJNA435743; BioSample No. SAMN08595902) under
the accession GGIQ00000000. The version described in this paper is the first version,
GGIQ01000000. The Sequence Read Archive (SRA) can be found at SRR6782848. Accession
numbers for all curated sequences are also provided in the manuscript in organized
tables.
ScienceOpen disciplines: Uncategorized
Data availability:
ScienceOpen disciplines: Uncategorized