Solute carriers in scallop genome: Gene expansion and expression regulation after exposure to toxic dinoflagellate

Xun, Xiaogang; Cheng, Jie; Wang, Jing; Li, Yangping; Li, Xu; Li, Moli; Lou, Jiarun; Kong, Yifan; Bao, Zhenmin; Hu, Xiaoli

doi:10.1016/j.chemosphere.2019.124968

Cited by 19 publications

(17 citation statements)

References 48 publications

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“…A gene of the SLC6 family was up-regulated in Pseudo-nitzschia multiseries under toxin-producing conditions [ 56 ], and this gene was also up-regulated in a domoic acid-producing Pseudo-nitzschia species in relation to two Pseudo-nitzschia species that do not produce domoic acid [ 57 ]. The SLC6 family is expanded in the genome of the scallops Chlamys farreri and Patinopecten yessoensis [ 58 , 59 ], in relation to other bivalves. In the A. opercularis [ 30 ] and in P. maximus digestive gland transcriptome, the number of transcripts belonging to this family is also very high (we found 58 in P. maximus ).…”

Section: Discussionmentioning

confidence: 99%

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Transcriptional Response in the Digestive Gland of the King Scallop (Pecten maximus) After the Injection of Domoic Acid

Ventoso

Pazos

Blanco

et al. 2021

Toxins

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Some diatom species of the genus Pseudo-nitzschia produce the toxin domoic acid. The depuration rate of domoic acid in Pecten maximus is very low; for this reason, king scallops generally contain high levels of domoic acid in their tissues. A transcriptomic approach was used to identify the genes differentially expressed in the P. maximus digestive gland after the injection of domoic acid. The differential expression analysis found 535 differentially expressed genes (226 up-regulated and 309 down-regulated). Protein–protein interaction networks obtained with the up-regulated genes were enriched in gene ontology terms, such as vesicle-mediated transport, response to stress, signal transduction, immune system process, RNA metabolic process, and autophagy, while networks obtained with the down-regulated genes were enriched in gene ontology terms, such as response to stress, immune system process, ribosome biogenesis, signal transduction, and mRNA processing. Genes that code for cytochrome P450 enzymes, glutathione S-transferase theta-1, glutamine synthase, pyrroline-5-carboxylate reductase 2, and sodium- and chloride-dependent glycine transporter 1 were among the up-regulated genes. Therefore, a stress response at the level of gene expression, that could be caused by the domoic acid injection, was evidenced by the alteration of several biological, cellular, and molecular processes.

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Section: Discussionmentioning

confidence: 99%

“…The SLC6 family is expanded in the genome of the scallops Chlamys farreri and Patinopecten yessoensis [58,59], in relation to other bivalves. In the A. opercularis [30] and in P. maximus digestive gland transcriptome, the number of transcripts belonging to this family is also very high (we found 58 in P. maximus).…”

Section: Discussionmentioning

confidence: 99%

Transcriptional Response in the Digestive Gland of the King Scallop (Pecten maximus) After the Injection of Domoic Acid

Ventoso

Pazos

Blanco

et al. 2021

Toxins

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“…In order to test for positive selection at individual amino acid codons, the specific site model was implemented using the program of the PAML (Yang, 2007;Xun et al, 2020) under maximum-likelihood (ML) and Nei and Gojobori (NG) approach. Site model supposes that different branches of the phylogenetic tree are subject to the same selection pressure, but different amino acid positions experience different selection pressures (Gao et al, 2019).To measure the selective pressure at the protein level, this model allows the ratio to vary among sites of the expanded C1Qs to estimate Non-synonymous (dN) and Synonymous (dS) substitution ratios (dN/dS or ω).…”

Section: Molecular Evolutionary Analysis Of Cfc1q Genesmentioning

confidence: 99%

Expansion of C1Q Genes in Zhikong Scallop and Their Expression Profiling After Exposure to the Toxic Dinoflagellates

Wang

Lian

et al. 2021

Front. Mar. Sci.

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C1Q (Complement 1Q) is an important recognition molecule in the immunological complement system, which could also be putatively involved in the stress responses induced by endotoxins or exotoxins, potentially through detoxification processes. Marine bivalves are well adapted to highly complex aquatic environments with various stressors. As filter feeders, they have to cope with highly potent microalgae-derived neurotoxins, such as paralytic shellfish toxin (PSTs). Zhikong scallops, Chlamys farreri, are commercially important bivalve with the remarkable ability to accumulate PSTs. Exploring the C1Qs related to PST accumulation in C. farreri could benefit our understanding of the adaptations of bivalve species. In the present study, we systematically analyzed C1Q genes in C. farreri. In total, 97 CfC1Q genes mainly from the expanded C1Q-B subfamily were identified, from which the C1QL, C1QTNF, and C1QDC1 members in C. farreri were revealed to be under positive selection. Spatiotemporal expression analysis revealed that most CfC1QLs and CfC1QDC1s were highly expressed during the post-umbo stage and in hepatopancreas, while most CfC1QTNF members were highly expressed after the creeping larva stage and in mantle. The hepatopancreas and kidney in C. farreri are two toxin-rich organs with the highest concentrations of PSTs, acting as major “centers” for toxin accumulation and transformation, respectively. Therefore, after feeding the scallops with PST-producing dinoflagellates Alexandrium minutum and Alexandrium catenella, we determined the expression patterns of CfC1Qs in these two organs. In kidney, more than 85% of CfC1QLs and CfC1QDC1s showed drastic up-regulation with both diets. However, among these members with significant induction, a different response manner was detected after feeding with A. minutum and A. catenella, respectively as acute and chronic response patterns. In comparison, far fewer CfC1Qs showing significant up-regulation in hepatopancreas with both toxic diets and only mild regulation pattern could be found. This organ-, toxin-, and time-dependent genetic regulation of CfC1Qs may contribute to the virulence difference on account of the tissue-specific or dinoflagellate-specific different toxin analogs composition, implying the possible involvement of CfC1Qs in PST transport and homeostasis. Our findings imply the functional diversity of scallop C1Q genes in coping with PST accumulation, which might be developed as potential molecular indicators for monitoring toxin accumulation in edible mollusks or provide insight into the lineage-specific adaptation of scallops for dealing with microalgal toxin challenges.

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“…Previously, adult C. farreri was challenged with the PST-producing dinoflagellates A. minutum (strain AM-1) and A. catenella (strain ACDH) via feeding prior to sample collection [66]. No other noxious metabolites were previously reported in these two strains, but the main PST analogs in AM-1 and ACDH were gonyautoxins (GTX1-4) and N-sulfocarbamoyl-gonyautoxins (C-1,2), respectively [25,66,67]. The dinoflagellate cultures were grown in L1 medium at 17 • C/25 • C with a light: dark cycle of 12:12 h and were collected during the exponential growth phase at a cell density approaching 5 × 10 4 cells mL −1 [68,69].…”

Section: Expression Response Of Sod Genes To a Minutum And A Catenementioning

confidence: 99%

Genome-Wide Identification and Characterization of SODs in Zhikong Scallop Reveals Gene Expansion and Regulation Divergence after Toxic Dinoflagellate Exposure

et al. 2019

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As filter-feeding animals mainly ingesting microalgae, bivalves could accumulate paralytic shellfish toxins (PSTs) produced by harmful algae through diet. To protect themselves from the toxic effects of PSTs, especially the concomitant oxidative damage, the production of superoxide dismutase (SOD), which is the only eukaryotic metalloenzyme capable of detoxifying superoxide, may assist with toxin tolerance in bivalves. To better understand this process, in the present study, we performed the first systematic analysis of SOD genes in bivalve Chlamys farreri, an important aquaculture species in China. A total of six Cu/Zn-SODs (SOD1-6) and two Mn-SODs (SOD7, SOD8) were identified in C. farreri, with gene expansion being revealed in Cu/Zn-SODs. In scallops exposed to two different PSTs-producing dinoflagellates, Alexandrium minutum and A. catenella, expression regulation of SOD genes was analyzed in the top ranked toxin-rich organs, the hepatopancreas and the kidney. In hepatopancreas, which mainly accumulates the incoming PSTs, all of the six Cu/Zn-SODs showed significant alterations after A. minutum exposure, with SOD1, 2, 3, 5, and 6 being up-regulated, and SOD4 being down-regulated, while no significant change was detected in Mn-SODs. After A. catenella exposure, up-regulation was observed in SOD2, 4, 6, and 8, and SOD7 was down-regulated. In the kidney, where PSTs transformation occurs, SOD4, 5, 6, and 8 were up-regulated, and SOD7 was down-regulated in response to A. minutum feeding. After A. catenella exposure, all the Cu/Zn-SODs except SOD1 were up-regulated, and SOD7 was down-regulated in kidney. Overall, in scallops after ingesting different toxic algae, SOD up-regulation mainly occurred in the expanded Cu/Zn-SOD group, and SOD6 was the only member being up-regulated in both toxic organs, which also showed the highest fold change among all the SODs, implying the importance of SOD6 in protecting scallops from the stress of PSTs. Our results suggest the diverse function of scallop SODs in response to the PST-producing algae challenge, and the expansion of Cu/Zn-SODs might be implicated in the adaptive evolution of scallops or bivalves with respect to antioxidant defense against the ingested toxic algae.

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Solute carriers in scallop genome: Gene expansion and expression regulation after exposure to toxic dinoflagellate

Cited by 19 publications

References 48 publications

Transcriptional Response in the Digestive Gland of the King Scallop (Pecten maximus) After the Injection of Domoic Acid

Transcriptional Response in the Digestive Gland of the King Scallop (Pecten maximus) After the Injection of Domoic Acid

Expansion of C1Q Genes in Zhikong Scallop and Their Expression Profiling After Exposure to the Toxic Dinoflagellates

Genome-Wide Identification and Characterization of SODs in Zhikong Scallop Reveals Gene Expansion and Regulation Divergence after Toxic Dinoflagellate Exposure

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