Toxin- and species-dependent regulation of ATP-binding cassette (ABC) transporters in scallops after exposure to paralytic shellfish toxin-producing dinoflagellates

Wang, Huizhen; Liu, Shiqi; Xun, Xiaogang; Li, Moli; Lou, Jiarun; Zhang, Yihan; Shi, Jiaoxia; Hu, Jiang; Bao, Zhenmin; Hu, Xiaoli

doi:10.1016/j.aquatox.2020.105697

Cited by 22 publications

(11 citation statements)

References 50 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The algae cells were cultivated independently and then harvested at the late exponential growth phase. Before the exposure experiment, the PST profiles in the two Alexandrium dinoflagellates were measured by a high-performance liquid chromatography with tandem mass spectrometry (HPLC-MS/MS) analysis following the steps described in a previous study [58]. Each scallop was fed 2500 cells/mL/day of dinoflagellates.…”

Section: Transcriptomic Analysis Of the Caspase Homologues In Response To Pstsmentioning

confidence: 99%

The Caspase Homologues in Scallop Chlamys farreri and Their Expression Responses to Toxic Dinoflagellates Exposure

Wei

Ding

et al. 2022

Toxins

Self Cite

View full text Add to dashboard Cite

The cysteine aspartic acid-specific protease (caspase) family is distributed across vertebrates and invertebrates, and its members are involved in apoptosis and response to cellular stress. The Zhikong scallop (Chlamys farreri) is a bivalve mollusc that is well adapted to complex marine environments, yet the diversity of caspase homologues and their expression patterns in the Zhikong scallop remain largely unknown. Here, we identified 30 caspase homologues in the genome of the Zhikong scallop and analysed their expression dynamics during all developmental stages and following exposure to paralytic shellfish toxins (PSTs). The 30 caspase homologues were classified as initiators (caspases-2/9 and caspases-8/10) or executioners (caspases-3/6/7 and caspases-3/6/7-like) and displayed increased copy numbers compared to those in vertebrates. Almost all of the caspase-2/9 genes were highly expressed throughout all developmental stages from zygote to juvenile, and their expression in the digestive gland and kidney was slightly influenced by PSTs. The caspase-8/10 genes were highly expressed in the digestive gland and kidney, while PSTs inhibited their expression in these two organs. After exposure to different Alexandrium PST-producing algae (AM-1 and ACDH), the number of significantly up-regulated caspase homologues in the digestive gland increased with the toxicity level of PST derivatives, which might be due to the higher toxicity of GTXs produced by AM-1 compared to the N-sulphocarbamoyl analogues produced by ACDH. However, the effect of these two PST-producing algae strains on caspase expression in the kidney seemed to be stronger, possibly because the PST derivatives were transformed into highly toxic compounds in scallop kidney, and suggested an organ-dependent response to PSTs. These results indicate the dedicated control of caspase gene expression and highlight their contribution to PSTs in C. farreri. This work provides a further understanding of the role of caspase homologues in the Zhikong scallop and can guide future studies focussing on the role of caspases and their interactions with PSTs.

show abstract

Section: Transcriptomic Analysis Of the Caspase Homologues In Response To Pstsmentioning

confidence: 99%

The Caspase Homologues in Scallop Chlamys farreri and Their Expression Responses to Toxic Dinoflagellates Exposure

Wei

Ding

et al. 2022

Toxins

Self Cite

View full text Add to dashboard Cite

show abstract

“…We previously detected PST profiles and concentrations in gills at each time point and found that gills were characterized by the domination of GTX2/3 and GTX1/4, which closely resembled that of the toxic algae fed to scallops [ 6 ], and also contained a small amount of the transformed types STX and NEO, which may be absorbed from the kidney, the main organ for PST transformation ( Figure S1 ) [ 4 ]. The content of PST increased slightly during the first five days, then increased sharply and reached a peak at 15 days after exposure ( Figure S1a ) [ 4 ].…”

Section: Resultsmentioning

confidence: 99%

“…Unlike humans and other mammals, bivalves possess toxin-resistant amino acids in Nav protein, thus they are able to tolerate high concentrations of PST [ 2 , 4 ]. In addition, gene family analysis indicated that the genes related to detoxification, antioxidation, and immune stress, such as glutathione S-transferase ( GST ) [ 5 ], ATP-binding cassette transporter ( ABC ) [ 6 ], superoxide dismutase ( SOD ) [ 7 ], glutathione peroxidase ( GPx ) [ 8 ], and 70-kDa heat shock protein ( HSP70 ) [ 9 ], were significantly altered in expression after exposure to PST-producing Alexandrium , implying the involvement of various biological processes in PST resistance.…”

Section: Introductionmentioning

confidence: 99%

Transcriptome and Network Analyses Reveal the Gene Set Involved in PST Accumulation and Responses to Toxic Alexandrium minutum Exposure in the Gills of Chlamys farreri

Wang

Lou

et al. 2022

IJMS

Self Cite

View full text Add to dashboard Cite

Bivalve molluscs are filter-feeding organisms that can accumulate paralytic shellfish toxins (PST) through ingesting toxic marine dinoflagellates. While the effects of PST accumulation upon the physiology of bivalves have been documented, the underlying molecular mechanism remains poorly understood. In this study, transcriptomic analysis was performed in the gills of Zhikong scallop (Chlamys farreri) after 1, 3, 5, 10, and 15 day(s) exposure of PST-producing dinoflagellate Alexandrium minutum. Higher numbers of differentially expressed genes (DEGs) were detected at day 1 (1538) and day 15 (989) than that at day 3 (77), day 5 (82), and day 10 (80) after exposure, and most of the DEGs were only regulated at day 1 or day 15, highlighting different response mechanisms of scallop to PST-producing dinoflagellate at different stages of exposure. Functional enrichment results suggested that PST exposure induced the alterations of nervous system development processes and the activation of xenobiotic metabolism and substance transport processes at the acute and chronic stages of exposure, respectively, while the immune functions were inhibited by PST and might ultimately cause the activation of apoptosis. Furthermore, a weighted gene co-expression network was constructed, and ten responsive modules for toxic algae exposure were identified, among which the yellow module was found to be significantly correlated with PST content. Most of the hub genes in the yellow module were annotated as solute carriers (SLCs) with eight being OCTN1s, implying their dominant roles in regulating PST accumulation in scallop gills. Overall, our results reveal the gene set responding to and involved in PST accumulation in scallop gills, which will deepen our understanding of the molecular mechanism of bivalve resistance to PST.

show abstract

“…These two toxic strains of Alexandrium were cultured independently in F/2 medium under a light–dark cycle of 14h:10h and were collected when the cell density reached 3 × 10 5 cells/mL in the exponential growth phase [ 39 , 40 ]. Before the feeding experiment, the PST profiles of two toxic strains were measured by high-performance liquid chromatography with tandem mass spectrometry (HPLC-MS/MS) analysis following the methods described in our previous study [ 41 ]. The main types of PST in ACDH and AM-1 were N-sulphocarbamoyl derivatives (C1/C2) and gonyautoxins (GTXs, mainly GTX1-4), respectively, and no other noxious metabolites were previously reported in these two strains [ 41 ].…”

Section: Methodsmentioning

confidence: 99%

“…Before the feeding experiment, the PST profiles of two toxic strains were measured by high-performance liquid chromatography with tandem mass spectrometry (HPLC-MS/MS) analysis following the methods described in our previous study [ 41 ]. The main types of PST in ACDH and AM-1 were N-sulphocarbamoyl derivatives (C1/C2) and gonyautoxins (GTXs, mainly GTX1-4), respectively, and no other noxious metabolites were previously reported in these two strains [ 41 ]. C. farreri and P. yessoensis were acclimated in filtered and aerated seawater at 12.5 ± 0.5 °C for three weeks and then maintained independently with aeration during the exposure experiments.…”

Section: Methodsmentioning

confidence: 99%

Expression Plasticity of Peroxisomal Acyl-Coenzyme A Oxidase Genes Implies Their Involvement in Redox Regulation in Scallops Exposed to PST-Producing Alexandrium

Wang

Tang

et al. 2022

Marine Drugs

Self Cite

View full text Add to dashboard Cite

Filter-feeding bivalves can accumulate paralytic shellfish toxins (PST) produced by toxic microalgae, which may induce oxidative stress and lipid peroxidation. Peroxisomal acyl-coenzyme A oxidases (ACOXs) are key enzymes functioning in maintaining redox and lipid homeostasis, but their roles in PST response in bivalves are less understood. Herein, a total of six and six ACOXs were identified in the Chlamys farreri and Patinopecten yessoensis genome, respectively, and the expansion of ACOX1s was observed. Gene expression analysis revealed an organ/tissue-specific expression pattern in both scallops, with all ACOXs being predominantly expressed in the two most toxic organs, digestive glands and kidneys. The regulation patterns of scallop ACOXs after exposure to different PST-producing algaes Alexandrium catenella (ACDH) and A. minutum (AM-1) were revealed. After ACDH exposure, more differentially expressed genes (DEGs) were identified in C. farreri digestive glands (three) and kidneys (five) than that in P. yessoensis (two), but the up-regulated DEGs showed similar expression patterns in both species. In C. farreri, three DEGs were found in both digestive glands and kidneys after AM-1 exposure, with two same CfACOX1s being acutely and chronically induced, respectively. Notably, these two CfACOX1s also showed different expression patterns in kidneys between ACDH (acute response) and AM-1 (chronic response) exposure. Moreover, inductive expression of CfACOXs after AM-1 exposure was observed in gills and mantles, and all DEGs in both tissues were up-regulated and their common DEGs exhibited both acute and chronic induction. These results indicate the involvement of scallop ACOXs in PST response, and their plasticity expression patterns between scallop species, among tissues, and between the exposure of different PST analogs.

show abstract

Toxin- and species-dependent regulation of ATP-binding cassette (ABC) transporters in scallops after exposure to paralytic shellfish toxin-producing dinoflagellates

Cited by 22 publications

References 50 publications

The Caspase Homologues in Scallop Chlamys farreri and Their Expression Responses to Toxic Dinoflagellates Exposure

The Caspase Homologues in Scallop Chlamys farreri and Their Expression Responses to Toxic Dinoflagellates Exposure

Transcriptome and Network Analyses Reveal the Gene Set Involved in PST Accumulation and Responses to Toxic Alexandrium minutum Exposure in the Gills of Chlamys farreri

Expression Plasticity of Peroxisomal Acyl-Coenzyme A Oxidase Genes Implies Their Involvement in Redox Regulation in Scallops Exposed to PST-Producing Alexandrium

Contact Info

Product

Resources

About