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Whole-body transcriptome analysis provides insights into the cascade of sequential expression events involved in growth, immunity, and metabolism during the molting cycle in Scylla paramamosain.

ABSTRACT: The molecular mechanisms underlying the dynamic process of crab molting are still poorly understood at the individual level. We investigated global expression changes in the mud crab, Scylla paramamosain, at the transcriptome level and revealed a cascade of sequential expression events for genes involved in various aspects of the molting process using whole-body sequencing of juvenile crabs. RNA-sequencing (RNA-seq) produced 139.49 Gb of clean reads and 20,436 differentially expressed genes (DEGs) among different molting stages. The expression patterns for genes involved in several molecular events critical for molting, such as cuticle reconstruction, cytoskeletal structure remodeling, hormone regulation, immune responses, and metabolism, were characterized and considered as mechanisms underlying molting in S. paramamosain. Among these genes, we identified 10,695 DEGs in adjacent molting stages. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses showed that significantly enriched pathways included structural constituents of cuticle, binding and chitin metabolic processes, steroid hormone biosynthesis, insulin resistance, and amino sugar metabolic processes. The expression profiles of 12 functional genes detected via RNA-seq were corroborated via real-time RT-PCR assays. The results revealed gene expression profiles across the molting cycle and identified possible activation pathways for future investigation of the underlying molecular mechanisms.

SUBMITTER: Liu L

PROVIDER: S-EPMC9259733 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Molting is a crucial lifelong process in the growth, development, and reproduction of crustaceans. In mud crab (Scylla paramamosain), new exoskeleton, gills, and appendages are formed after a molting, which contributes to a 40 to 90% increase in body weight. However, little is currently known about the associations between molting and the dynamic changes of microbiota and physiological characteristics in mud crabs. In this study, the effects of molting on changes of the microbiome, immune response, and digestive enzyme activities in mud crabs were investigated. The results showed dynamic changes in the abundances and community compositions of crab-associated microbiota harboring the gills, subcuticular epidermis, hepatopancreas, midgut, and hemolymph during molting. Renewed microbiota was observed in the gills and midgut of crabs at the postmolt stages, which seems to be related to the formation of a new exoskeleton after the molting. A significant positive correlation between the expression of two antimicrobial peptide (AMP) genes (SpALF5 and SpCrustin) and the relative abundance of two predominant microorganisms (Halomonas and Shewanella) in hemolymph was observed in the whole molt cycle, suggesting that AMPs play a role in modulating hemolymph microbiota. Furthermore, digestive enzymes might play a vital role in the changes of microbiota harboring the hepatopancreas and midgut, which provide suitable conditions for restoring and reconstructing host-microbiome homeostasis during molting. In conclusion, this study confirms that molting affects host-associated microbiota and further sheds light on the effects on the immune response and the digestive systems as well. IMPORTANCE Molting is crucial for crustaceans. In mud crab, its exoskeleton is renewed periodically during molting, and this process is an ideal model to study the effects of host development on its microbiota. Here, multiple approaches were used to investigate the changes in microbial taxa, immune response, and digestive enzyme activity with respect to molting in mud crab. The results found that a renewed microbiota was generated in the gills and midgut of crab after a molt. A significant positive correlation between changes in the relative abundances of microbes (such as Halomonas and Shewanella) and the expression of AMP genes (SpALF5 and SpCrustin) was observed in the hemolymph of crabs during the whole molt cycle, suggesting the modulation of hemolymph microbes by AMPs. Furthermore, the digestive enzymes were found to participate in the regulation of microbiota in hepatopancreas and midgut, consequently providing a suitable condition for the restoration and reconstruction of host-microbiome homeostasis during the molting. This study confirms that molting affects the microbial communities and concomitantly influences the immune and digestive systems in mud crabs. This is also the first time the homeostasis of the host and microbiome, and the associations between molting and physiological characteristics in crustaceans, have been revealed.

Project description:BackgroundMud crab, Scylla paramamosain, a euryhaline crustacean species, mainly inhabits the Indo-Western Pacific region. Wild mud crab spawn in high-salt condition and the salinity reduced with the growth of the hatching larvae. When the larvae grow up to megalopa, they migrate back to estuaries and coasts in virtue of the flood tide, settle and recruit adult habitats and metamorphose into the crablet stage. Adult crab can even survive in a wide salinity of 0-35 ppt. To investigate the mRNA profile after salinity stress, S. paramamosain megalopa were exposed to different salinity seawater (low, 14 ppt; control, 25 ppt; high, 39 ppt).ResultsFirstly, from the expression profiles of Na+/K+/2Cl- cotransporter, chloride channel protein 2, and ABC transporter, it turned out that the 24 h might be the most influenced duration in the short-term stress. We collected megalopa under different salinity for 24 h and then submitted to mRNA profiling. Totally, 57.87 Gb Clean Data were obtained. The comparative genomic analysis detected 342 differentially expressed genes (DEGs). The most significantly DEGs include gamma-butyrobetaine dioxygenase-like, facilitated trehalose transporter Tret1, sodium/potassium-transporting ATPase subunit alpha, rhodanese 1-like protein, etc. And the significantly enriched pathways were lysine degradation, choline metabolism in cancer, phospholipase D signaling pathway, Fc gamma R-mediated phagocytosis, and sphingolipid signaling pathway. The results indicate that in the short-term salinity stress, the megalopa might regulate some mechanism such as metabolism, immunity responses, osmoregulation to adapt to the alteration of the environment.ConclusionsThis study represents the first genome-wide transcriptome analysis of S. paramamosain megalopa for studying its stress adaption mechanisms under different salinity. The results reveal numbers of genes modified by salinity stress and some important pathways, which will provide valuable resources for discovering the molecular basis of salinity stress adaptation of S. paramamosain larvae and further boost the understanding of the potential molecular mechanisms of salinity stress adaptation for crustacean species.

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Whole-body transcriptome analysis provides insights into the cascade of sequential expression events involved in growth, immunity, and metabolism during the molting cycle in Scylla paramamosain.

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