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

Shanshan Lian,Xiaogang Xun,Xu Li,Liang Zhao,Jiarun Lou,Zhenmin Bao,Xiaoli Hu,Moli Li,Lingling Zhang,Shi Wang

doi:10.3390/md17120700

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.

Highlights

Reactive oxygen species (ROS) are the active partially excited forms of oxygen that are usually unavoidably generated as by-products of aerobic metabolism and can damage multiple cellular components [1]
Genes in oyster C. gigas, snail Biomphalaria glabrata, and sea urchin Strongylocentrotus purpuratus, and our results showed that more than six Superoxide dismutase (SOD) members were present in these species
Among Cu/Zn-SODs, SOD2, and SOD3 were found to be located on the same chromosome in C

Summary

Introduction

Reactive oxygen species (ROS) are the active partially excited forms of oxygen that are usually unavoidably generated as by-products of aerobic metabolism and can damage multiple cellular components [1]. Superoxide dismutase (SOD) (EC 1.15.1.1) is the only eukaryotic metalloenzyme capable of detoxifying superoxide, one type of ROS, principally acting as the first and most important line of antioxidant defense among all eukaryotic organisms [1,2]. Based on distinct catalytic metal cofactors, superoxide dismutases have been classified as copper/zinc SODs and manganese SODs in eukaryotic animals [3]. Mn-SODs are considered as an early evolutionary form of SODs, since they were found mainly in mitochondria, the organelle which is thought have originally been independent organisms and were symbiotically fused into eukaryotes one billion years ago [4]. Multiple lines of evidence have shown that SOD genes are sensitive to stress [2,6], and altered

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