Abstract
BackgroundThe American lobster, Homarus americanus, is an important species as an economically valuable fishery, a key member in marine ecosystems, and a well-studied model for central pattern generation, the neural networks that control rhythmic motor patterns. Despite multi-faceted scientific interest in this species, currently our genetic resources for the lobster are limited. In this study, we de novo assemble a transcriptome for Homarus americanus using central nervous system (CNS), muscle, and hybrid neurosecretory tissues and compare gene expression across these tissue types. In particular, we focus our analysis on genes relevant to central pattern generation and the identity of the neurons in a neural network, which is defined by combinations of genes distinguishing the neuronal behavior and phenotype, including ion channels, neurotransmitters, neuromodulators, receptors, transcription factors, and other gene products.ResultsUsing samples from the central nervous system (brain, abdominal ganglia), abdominal muscle, and heart (cardiac ganglia, pericardial organs, muscle), we used RNA-Seq to characterize gene expression patterns across tissues types. We also compared control tissues with those challenged with the neuropeptide proctolin in vivo. Our transcriptome generated 34,813 transcripts with known protein annotations. Of these, 5,000-10,000 of annotated transcripts were significantly differentially expressed (DE) across tissue types. We found 421 transcripts for ion channels and identified receptors and/or proteins for over 20 different neurotransmitters and neuromodulators. Results indicated tissue-specific expression of select neuromodulator (allostatin, myomodulin, octopamine, nitric oxide) and neurotransmitter (glutamate, acetylcholine) pathways. We also identify differential expression of ion channel families, including kainite family glutamate receptors, inward-rectifying K+ (IRK) channels, and transient receptor potential (TRP) A family channels, across central pattern generating tissues.ConclusionsOur transcriptome-wide profiles of the rhythmic pattern generating abdominal and cardiac nervous systems in Homarus americanus reveal candidates for neuronal features that drive the production of motor output in these systems.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2373-3) contains supplementary material, which is available to authorized users.
Highlights
The American lobster, Homarus americanus, is an important species as an economically valuable fishery, a key member in marine ecosystems, and a well-studied model for central pattern generation, the neural networks that control rhythmic motor patterns
Mapping Entrez Gene IDs to Gene Ontology (GO) annotations identified 11,383 GO categories represented in our transcriptome, including 7,161 gene products attributed to biological processes, 1,090 attributed to cellular components, and 3,132 attributed to molecular function
We found several transcription factors with a high proportion (>40 %) of transcripts differentially expressed (DE) and upregulated in our nervous system tissues, including ceh-36 the Otx-type homeobox gene involved in chemosensory neuron differentiation, ttx-1 an Otx-type transcription factor involved in thermosensory neuron identity, and ets-5 an ETS domain transcription factor involved in CO2/O2 sensory neurons [71]
Summary
The American lobster, Homarus americanus, is an important species as an economically valuable fishery, a key member in marine ecosystems, and a well-studied model for central pattern generation, the neural networks that control rhythmic motor patterns. The continuous, measurable physical output of these networks allows for straightforward comparisons between actual behavior and network activity These networks perform complex motor tasks in a coordinated, rhythmic fashion while still adapting the behavior to environmental contingencies [3, 4]. The accessibility of these networks combined with this juxtaposition between precision and flexibility has sparked decades of research on the subject, especially in invertebrate models like the American lobster Homarus americanus where these networks are relatively simple (tens or hundreds, rather than thousands, of neurons) compared to their vertebrate counterparts
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