Single cell transcriptomes reveal expression patterns of chemoreceptor genes in olfactory sensory neurons of the Caribbean spiny lobster, Panulirus argus

Abstract Background Crustaceans express several classes of receptor genes in their antennules, which house olfactory sensory neurons (OSNs) and non-olfactory chemosensory neurons. Transcriptomics studies reveal that candidate chemoreceptor proteins include variant Ionotropic Receptors (IRs) includin...

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Main Authors: Mihika T. Kozma, Hanh Ngo-Vu, Matthew T. Rump, Yuriy V. Bobkov, Barry W. Ache, Charles D. Derby
Format: Article
Language:English
Published: BMC 2020-09-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-020-07034-7
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author Mihika T. Kozma
Hanh Ngo-Vu
Matthew T. Rump
Yuriy V. Bobkov
Barry W. Ache
Charles D. Derby
author_facet Mihika T. Kozma
Hanh Ngo-Vu
Matthew T. Rump
Yuriy V. Bobkov
Barry W. Ache
Charles D. Derby
author_sort Mihika T. Kozma
collection DOAJ
description Abstract Background Crustaceans express several classes of receptor genes in their antennules, which house olfactory sensory neurons (OSNs) and non-olfactory chemosensory neurons. Transcriptomics studies reveal that candidate chemoreceptor proteins include variant Ionotropic Receptors (IRs) including both co-receptor IRs and tuning IRs, Transient Receptor Potential (TRP) channels, Gustatory Receptors, epithelial sodium channels, and class A G-protein coupled receptors (GPCRs). The Caribbean spiny lobster, Panulirus argus, expresses in its antennules nearly 600 IRs, 17 TRP channels, 1 Gustatory Receptor, 7 epithelial sodium channels, 81 GPCRs, 6 G proteins, and dozens of enzymes in signaling pathways. However, the specific combinatorial expression patterns of these proteins in single sensory neurons are not known for any crustacean, limiting our understanding of how their chemosensory systems encode chemical quality. Results The goal of this study was to use transcriptomics to describe expression patterns of chemoreceptor genes in OSNs of P. argus. We generated and analyzed transcriptomes from 7 single OSNs, some of which were shown to respond to a food odor, as well as an additional 7 multicell transcriptomes from preparations containing few (2–4), several (ca. 15), or many (ca. 400) OSNs. We found that each OSN expressed the same 2 co-receptor IRs (IR25a, IR93a) but not the other 2 antennular coIRs (IR8a, IR76b), 9–53 tuning IRs but only one to a few in high abundance, the same 5 TRP channels plus up to 5 additional TRPs, 12–17 GPCRs including the same 5 expressed in every single cell transcriptome, the same 3 G proteins plus others, many enzymes in the signaling pathways, but no Gustatory Receptors or epithelial sodium channels. The greatest difference in receptor expression among the OSNs was the identity of the tuning IRs. Conclusions Our results provide an initial view of the combinatorial expression patterns of receptor molecules in single OSNs in one species of decapod crustacean, including receptors directly involved in olfactory transduction and others likely involved in modulation. Our results also suggest differences in receptor expression in OSNs vs. other chemosensory neurons.
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spelling doaj.art-e3a29208f2bf409aad5f6a87c117b5aa2022-12-21T21:52:08ZengBMCBMC Genomics1471-21642020-09-0121111910.1186/s12864-020-07034-7Single cell transcriptomes reveal expression patterns of chemoreceptor genes in olfactory sensory neurons of the Caribbean spiny lobster, Panulirus argusMihika T. Kozma0Hanh Ngo-Vu1Matthew T. Rump2Yuriy V. Bobkov3Barry W. Ache4Charles D. Derby5Neuroscience Institute, Georgia State UniversityNeuroscience Institute, Georgia State UniversityNeuroscience Institute, Georgia State UniversityWhitney Laboratory, University of FloridaWhitney Laboratory, University of FloridaNeuroscience Institute, Georgia State UniversityAbstract Background Crustaceans express several classes of receptor genes in their antennules, which house olfactory sensory neurons (OSNs) and non-olfactory chemosensory neurons. Transcriptomics studies reveal that candidate chemoreceptor proteins include variant Ionotropic Receptors (IRs) including both co-receptor IRs and tuning IRs, Transient Receptor Potential (TRP) channels, Gustatory Receptors, epithelial sodium channels, and class A G-protein coupled receptors (GPCRs). The Caribbean spiny lobster, Panulirus argus, expresses in its antennules nearly 600 IRs, 17 TRP channels, 1 Gustatory Receptor, 7 epithelial sodium channels, 81 GPCRs, 6 G proteins, and dozens of enzymes in signaling pathways. However, the specific combinatorial expression patterns of these proteins in single sensory neurons are not known for any crustacean, limiting our understanding of how their chemosensory systems encode chemical quality. Results The goal of this study was to use transcriptomics to describe expression patterns of chemoreceptor genes in OSNs of P. argus. We generated and analyzed transcriptomes from 7 single OSNs, some of which were shown to respond to a food odor, as well as an additional 7 multicell transcriptomes from preparations containing few (2–4), several (ca. 15), or many (ca. 400) OSNs. We found that each OSN expressed the same 2 co-receptor IRs (IR25a, IR93a) but not the other 2 antennular coIRs (IR8a, IR76b), 9–53 tuning IRs but only one to a few in high abundance, the same 5 TRP channels plus up to 5 additional TRPs, 12–17 GPCRs including the same 5 expressed in every single cell transcriptome, the same 3 G proteins plus others, many enzymes in the signaling pathways, but no Gustatory Receptors or epithelial sodium channels. The greatest difference in receptor expression among the OSNs was the identity of the tuning IRs. Conclusions Our results provide an initial view of the combinatorial expression patterns of receptor molecules in single OSNs in one species of decapod crustacean, including receptors directly involved in olfactory transduction and others likely involved in modulation. Our results also suggest differences in receptor expression in OSNs vs. other chemosensory neurons.http://link.springer.com/article/10.1186/s12864-020-07034-7CrustaceaG-protein coupled receptorIonotropic receptorOlfactionOlfactory sensory neuronSingle cell transcriptome
spellingShingle Mihika T. Kozma
Hanh Ngo-Vu
Matthew T. Rump
Yuriy V. Bobkov
Barry W. Ache
Charles D. Derby
Single cell transcriptomes reveal expression patterns of chemoreceptor genes in olfactory sensory neurons of the Caribbean spiny lobster, Panulirus argus
BMC Genomics
Crustacea
G-protein coupled receptor
Ionotropic receptor
Olfaction
Olfactory sensory neuron
Single cell transcriptome
title Single cell transcriptomes reveal expression patterns of chemoreceptor genes in olfactory sensory neurons of the Caribbean spiny lobster, Panulirus argus
title_full Single cell transcriptomes reveal expression patterns of chemoreceptor genes in olfactory sensory neurons of the Caribbean spiny lobster, Panulirus argus
title_fullStr Single cell transcriptomes reveal expression patterns of chemoreceptor genes in olfactory sensory neurons of the Caribbean spiny lobster, Panulirus argus
title_full_unstemmed Single cell transcriptomes reveal expression patterns of chemoreceptor genes in olfactory sensory neurons of the Caribbean spiny lobster, Panulirus argus
title_short Single cell transcriptomes reveal expression patterns of chemoreceptor genes in olfactory sensory neurons of the Caribbean spiny lobster, Panulirus argus
title_sort single cell transcriptomes reveal expression patterns of chemoreceptor genes in olfactory sensory neurons of the caribbean spiny lobster panulirus argus
topic Crustacea
G-protein coupled receptor
Ionotropic receptor
Olfaction
Olfactory sensory neuron
Single cell transcriptome
url http://link.springer.com/article/10.1186/s12864-020-07034-7
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