Molecular Analysis of Atypical Family 18 Chitinase from Fujian Oyster Crassostrea angulata and Its Physiological Role in the Digestive System

Yang, Bingye; Zhang, Mingming; Li, Lingling; Pu, Fei; Wang, You; Ke, Caihuan

doi:10.1371/journal.pone.0129261

Cited by 7 publications

(7 citation statements)

References 31 publications

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“…In previous studies, chitinase activity was reported in C. virginica, M. edulis, and C. angulata crystalline structures (Smucker and Wright 1984;Birkbeck and McHenery 1984;Yang et al 2015), as well as in C. angulata larval stages (Yang et al 2015). As chitinases are required for the degradation of chitin-containing structures, such as algae, we hypothesize that the depletion of chitinase (CHIT1) mRNA was most likely a signal of reduced digestive function.…”

Section: Reduced Carbohydrate Metabolism and Absorption Ratementioning

confidence: 72%

Understanding the mechanisms involved in the high sensitivity of Pecten maximus larvae to aeration

et al. 2018

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Among reared bivalves, some "novel species", such as the great scallop, Pecten maximus, have experienced more difficulty with routine reproduction due to their high sensitivity to biological, chemical, and physical stress during stages of early development. Working with high larval densities requires the use of aeration systems to provide optimal larval suspension and feed distribution. The high susceptibility of the great scallop to aeration in small-volume systems may impose an important limitation in hatchery-based practices. The present study aimed to investigate the processes impacted by aeration in P. maximus veliger larvae exposed to continuous aeration in small-volume tanks (10 L). Aeration appeared as major stressor that was responsible for early mortality among exposed animals (at 96 h after aeration started, haa) when exposure started 13 days after fertilization. Exposed larvae and controls were collected at 12, 24 and 72 haa, and a total of 18 cDNA libraries, each representing a pool of approximately 7,500 larvae, were sequenced, obtaining 358,817,016 raw reads. RNA-seq data were first used to build a de novo transcriptome assembly, and differential transcript abundance was assessed in exposed and control groups; thus, the molecular mechanisms involved in high sensitivity to aeration were deciphered. More than 2,000 transcripts were differentially expressed between exposed and control larvae across the entire time series (logFC > 1, FDR < 5%). Functional analysis revealed that transcriptional changes in larvae exposed to aeration mainly involved the genes that regulate digestive activity and energy metabolism, immune defense, inflammation, apoptosis, larval growth, and development. The results of this study demonstrate that, overall, aeration affects the feeding capacity and energy metabolism of larvae, with expected consequences on the animal's fitness, including its swimming efficiency. Aeration also triggered immune responses and apoptosis, which then increased through opportunistic infections. Notably, infections may be a consequence of a bacterial bloom triggered by the first mortality events that occurred in the culture. This study provides insights into the interactions between environmental variables and great scallop larvae physiology, and the results may contribute to the development of strategies for improving larval rearing practices and ensuring long-term sustainability of P. maximus aquaculture. Highlights ► Pecten maximus is highly susceptible to mild aeration, a desirable rearing practice yielding optimal larvae and feed distribution. ► Water turbulence reduced lipid and carbohydrate metabolism in scallop larvae, thus resulting in delayed growth and development. ► As a symptom of stress condition, larvae died, exhausted due to continuous swimming and inability to feed. ► These findings may contribute to develop strategies for improving rearing practices and for long-term sustainability of scallop aquaculture.

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Section: Reduced Carbohydrate Metabolism and Absorption Ratementioning

confidence: 72%

Understanding the mechanisms involved in the high sensitivity of Pecten maximus larvae to aeration

et al. 2018

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“… 49 − 51 Since then, this treatment has been applied to the study of digestive function in marine mollusks. 52 , 53 Accordingly, to further investigate the role that CgFFAR4 plays in digestion, we subjected the oysters to starvation. The high CgFFAR4 levels in the hepatopancreas and stomach and CgFFAR4 downregulation upon starvation ( Figure 4 A) indicate that this protein plays an essential role in food digestion in C. gigas .…”

Section: Discussionmentioning

confidence: 99%

Characterization of Free Fatty Acid Receptor 4 and Its Involvement in Nutritional Control and Immune Response in Pacific Oysters (Crassostrea gigas)

Wang

et al. 2020

ACS Omega

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Free fatty acid receptor 4 (FFAR4) has various physiological functions, including energy regulation and immunological homeostasis. We examined the only FFAR4 homologue in the Pacific oyster Crassostrea gigas ( CgFFAR4 ), which functions as a sensor of long-chain fatty acids. CgFFAR4 is 1098 bp long and contains a seven-transmembrane G protein-coupled receptor domain. CgFFAR4 expression was high in the hepatopancreas, but it was downregulated after fasting, indicating that it plays an essential role in food digestion. Lipopolysaccharide stimulation downregulated CgFFAR4 level, probably as an immune response of the animal. Reduced glycogen level alongside decreased insulin receptor, insulin receptor substrate, and C. gigas glycogen synthase transcription levels after CgFFAR4 knockdown revealed that CgFFAR4 was involved in the regulation of fatty acid and glycogen levels via the insulin pathway. Accordingly, this is the first study on an invertebrate FFAR and provides new insights into the role of this receptor in immune response and nutritional control.

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“…As an essential component of the innate immunity against chitin‐coated pathogens, Chit1 also regulates inflammatory processes (Elmonem, van den Heuvel, & Levtchenko, ; Van Eijk et al., ). However, due to its digestive function in mussels (Birkbeck & McHenery, ; Lesser & Macmanes, ), oysters (Yang et al., ) and insectivorous scorpions (Fuzita et al., ), it is also another example of the dual roles of genes in digestion and immunity. Interestingly, the upregulation of Chit1 corresponded to the upregulation of a number of cuticle proteins in the parasites infecting Texel hosts (Figures , , and ), suggesting that direct targeting of the parasite's chitin cuticle might have led to the parasite's response of strengthening the weakened exoskeleton with increased cuticle production.…”

Section: Discussionmentioning

confidence: 99%

“…As an essential component of the innate immunity against chitin-coated pathogens, Chit1 also regulates inflammatory processes (Elmonem, van den Heuvel, & Levtchenko, 2016;Van Eijk et al, 2005). However, due to its digestive function in mussels (Birkbeck & McHenery, 1984;Lesser & Macmanes, 2016), oysters (Yang et al, 2015) and insectivorous scorpions (Fuzita et al, 2015), it is also another example of the dual roles of genes in digestion and immunity.…”

Section: Intestinalismentioning

confidence: 99%

Dual transcriptomics reveals co‐evolutionary mechanisms of intestinal parasite infections in blue mussels Mytilus edulis

et al. 2018

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On theoretical grounds, antagonistic co-evolution between hosts and their parasites should be a widespread phenomenon but only received little empirical support so far. Consequently, the underlying molecular mechanisms and evolutionary steps remain elusive, especially in nonmodel systems. Here, we utilized the natural history of invasive parasites to document the molecular underpinnings of co-evolutionary trajectories. We applied a dual-species transcriptomics approach to experimental cross-infections of blue mussel Mytilus edulis hosts and their invasive parasitic copepods Mytilicola intestinalis from two invasion fronts in the Wadden Sea. We identified differentially regulated genes from an experimental infection contrast for hosts (infected vs. control) and a sympatry contrast (sympatric vs. allopatric combinations) for both hosts and parasites. The damage incurred by Mytilicola infection and the following immune response of the host were mainly reflected in cell division processes, wound healing, apoptosis and the production of reactive oxygen species (ROS). Furthermore, the functional coupling of host and parasite sympatry contrasts revealed the concerted regulation of chitin digestion by a Chitotriosidase 1 homolog in hosts with several cuticle proteins in the parasite. Together with the coupled regulation of ROS producers and antagonists, these genes represent candidates that mediate the different evolutionary trajectories within the parasite's invasion. The host-parasite combination-specific coupling of these effector mechanisms suggests that underlying recognition mechanisms create specificity and local adaptation. In this way, our study demonstrates the use of invasive species' natural history to elucidate molecular mechanisms of host-parasite co-evolution in the wild.

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Molecular Analysis of Atypical Family 18 Chitinase from Fujian Oyster Crassostrea angulata and Its Physiological Role in the Digestive System

Cited by 7 publications

References 31 publications

Understanding the mechanisms involved in the high sensitivity of Pecten maximus larvae to aeration

Understanding the mechanisms involved in the high sensitivity of Pecten maximus larvae to aeration

Characterization of Free Fatty Acid Receptor 4 and Its Involvement in Nutritional Control and Immune Response in Pacific Oysters (Crassostrea gigas)

Dual transcriptomics reveals co‐evolutionary mechanisms of intestinal parasite infections in blue mussels Mytilus edulis

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