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Do ecological characteristics drive the prevalence of Panulirus argus virus 1 (PaV1) in juvenile Caribbean spiny lobsters in a tropical reef lagoon?

ABSTRACT: PaV1 is a pathogenic virus found only to infect Caribbean spiny lobsters Panulirus argus, a major fishing resource. P. argus is a benthic mesopredator and has a complex life history, with several ontogenetic habitat changes. Habitat characteristics and species diversity of surrounding communities may have implications for disease dynamics. This is of more concern for juvenile lobsters, which are more susceptible to PaV1 and are far less mobile than adult lobsters. We targeted a population of juvenile P. argus in a reef lagoon in Mexico, where PaV1 was first observed in 2001. Prevalence has been since irregularly assessed, but in 2016 we began a more systematic assessment, with two sampling periods per year (June and November) in three different zones of the reef lagoon. To examine the relationship between PaV1 prevalence and potential ecological determinants, we assessed habitat complexity, cover of different substrates, and invertebrate community composition in all zones during the first four sampling periods (June and November 2016 and 2017). Habitat complexity and percent cover of some substrates varied with zone and sampling period. This was the case for seagrass and macroalgae, which nevertheless were the dominant substrates. The invertebrate community composition varied with sampling period, but not with zone. Probability of infection decreased with increasing lobster size, consistent with previous studies, but was not affected by zone (i.e., variations in ecological characteristics did not appear to be sufficiently large so as to influence prevalence of PaV1). This result possibly reflects the dominance of marine vegetation and suggests that lobsters can be sampled throughout the reef lagoon to assess PaV1 prevalence. Prevalence was higher in only one of seven sampling periods (November 2017), suggesting that the pathogen has leveled off to an enzootic level.

SUBMITTER: Davies CE

PROVIDER: S-EPMC7048287 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Do ecological characteristics drive the prevalence of Panulirus argus virus 1 (PaV1) in juvenile Caribbean spiny lobsters in a tropical reef lagoon?

Davies Charlotte E CE Briones-Fourzán Patricia P Barradas-Ortiz Cecilia C Negrete-Soto Fernando F Moo-Cocom Gema G Lozano-Álvarez Enrique E

PloS one 20200228 2

PaV1 is a pathogenic virus found only to infect Caribbean spiny lobsters Panulirus argus, a major fishing resource. P. argus is a benthic mesopredator and has a complex life history, with several ontogenetic habitat changes. Habitat characteristics and species diversity of surrounding communities may have implications for disease dynamics. This is of more concern for juvenile lobsters, which are more susceptible to PaV1 and are far less mobile than adult lobsters. We targeted a population of juv ...[more]

PMID: 32109265

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Project description: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.

Project description:The spiny lobster, Panulirus argus, has two classes of chemosensilla representing "olfaction" and "distributed chemoreception," as is typical for decapod crustaceans. Olfactory sensilla are found exclusively on antennular lateral flagella and are innervated only by olfactory receptor neurons (ORNs) that project into olfactory lobes organized into glomeruli in the brain. Distributed chemoreceptor sensilla are found on all body surfaces including the antennular lateral flagella (LF) and walking leg dactyls (dactyls), and are innervated by both chemoreceptor neurons (CRNs) and mechanoreceptor neurons that project into somatotopically organized neuropils. Here, we examined expression of three classes of chemosensory genes in transcriptomes of the LF (with ORNs and CRNs), dactyls (with only CRNs), and brain of P. argus: Ionotropic Receptors (IRs), which are related to ionotropic glutamate receptors and found in all protostomes including crustaceans; Gustatory Receptors (GRs), which are ionotropic receptors that are abundantly expressed in insects but more restricted in crustaceans; and Transient Receptor Potential (TRP) channels, a diverse set of sensor-channels that include several chemosensors in diverse animals. We identified 108 IRs, one GR, and 18 homologues representing all seven subfamilies of TRP channels. The number of IRs expressed in the LF is far greater than in dactyls, possibly reflecting the contribution of receptor proteins associated with the ORNs beyond those associated with CRNs. We found co-receptor IRs (IR8a, IR25a, IR76b, IR93a) and conserved IRs (IR21a, IR40a) in addition to the numerous divergent IRs in the LF, dactyl, and brain. Immunocytochemistry showed that IR25a is expressed in ORNs, CRNs, and a specific type of cell located in the brain near the olfactory lobes. While the function of IRs, TRP channels, and the GR was not explored, our results suggest that P. argus has an abundance of diverse putative chemoreceptor proteins that it may use in chemoreception.

Dataset Information

Do ecological characteristics drive the prevalence of Panulirus argus virus 1 (PaV1) in juvenile Caribbean spiny lobsters in a tropical reef lagoon?

Publications

Do ecological characteristics drive the prevalence of Panulirus argus virus 1 (PaV1) in juvenile Caribbean spiny lobsters in a tropical reef lagoon?

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