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

Abstract

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.

Tissue-Biased and Species-Specific Regulation of Glutathione Peroxidase (GPx) Genes in Scallops Exposed to Toxic Dinoflagellates

“…In scallop embryos and larvae, CfGPx1-1 , CfGPx3-1 , CfGPx3-3b , and CfGPx4 in C. farreri , and PyGPx1 , PyGPx3-1 , PyGPx3-5 , and PyGPx4 in P. yessoensis exhibited relatively higher expression level than other GPx s, suggesting the importance of these GPx s in scallop development ( Figure 3 a). During the entire developmental process, high expression of GPx genes ( CfGPx3-1 , CfGPx3-3b , PyGPx1 , PyGPx3-1 ) was mainly present at the larval stages, especially after the D stage veliger, and in the following umbo larvae and juvenile stages ( Figure 3 a), implying the involvement of these GPx s in antioxidation or detoxification in scallop metamorphosis and post-larval development, which may be due to the elevation of oxygen consumption to meet high demands of energy reserve utilization during organ initiation and structural re-modelling [ 32 ]. Moreover, both CfGPx4 and PyGPx4 were expressed from the very beginning of fertilization and multicellular stages to the larvae and juvenile stages, indicating their maternal origin to play protective roles and to maintain a redox balance during development.…”

“…The activity of antioxidant enzymes, such as SOD, CAT, GST, and GPx, could be enhanced and contributed to the removal of excessive ROS. For example, scallop SOD [ 32 ] and GST [ 33 ] genes were both induced after Alexandrium exposure; The CAT and GPx enzymes could be oxidative stress biomarkers [ 34 ] and were involved in detoxification in responding to PST accumulation in bivalve tissues [ 35 ], and the high enzymatic activity also mirrored the gene expression results [ 36 ]. Moreover, different organisms may present varied levels of tolerance to PSTs, and the activities of antioxidant enzymes could respond specifically with cell types [ 37 ], which indicate that the antioxidant system may be responsible for varied sensitivity to PST exposure.…”

Proteome Response of Meretrix Bivalves Hepatopancreas Exposed to Paralytic Shellfish Toxins Producing Dinoflagellate Gymnodinium catenatum

“…Many organisms are known to produce antioxidative enzymes to scavenge excess ROS, prevent the accumulation of ROS and minimise oxidative damage to the cells. In the presnt study, TP5 (catalase, CAT) is an important enzyme that catalyzes the dismutation reaction of hydrogen peroxide to water and oxygen, while TP8 (Mn-superoxide dismutase, SOD) is involved in the dismutation of superoxide radical into either hydrogen peroxide or oxygen [71,72]. The overexpression of these two enzymes (TP5 and TP8) indicated the potential detoxication of PSTs in M. meretrix.…”

Chemical Defense in Marine Organisms

“…Bivalves are filter-feeding animals, mainly ingesting microalgae that can accumulate paralytic shellfish toxins (PSTs) produced by harmful algae. In this Special Issue, Lian and co-workers [ 46 ] performed the first systematic analysis of SOD genes in the 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.…”