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 <i>SOD</i> genes in bivalve <i>Chlamys farreri</i>, an important aquaculture species in China. A total of six <i>Cu/Zn-SOD</i>s (<i>SOD1-6</i>) and two <i>Mn-SOD</i>s (<i>SOD7</i>, <i>SOD8</i>) were identified in <i>C. farreri</i>, with gene expansion being revealed in <i>Cu/Zn-SOD</i>s. In scallops exposed to two different PSTs-producing dinoflagellates, <i>Alexandrium minutum</i> and <i>A. catenella</i>, expression regulation of <i>SOD</i> 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 <i>Cu/Zn-SOD</i>s showed significant alterations after <i>A. minutum</i> exposure, with <i>SOD1</i>, <i>2</i>, <i>3</i>, <i>5</i>, and <i>6</i> being up-regulated, and <i>SOD4</i> being down-regulated, while no significant change was detected in <i>Mn-SOD</i>s. After <i>A. catenella</i> exposure, up-regulation was observed in <i>SOD2</i>, <i>4</i>, <i>6</i>, and <i>8</i>, and <i>SOD7</i> was down-regulated. In the kidney, where PSTs transformation occurs, <i>SOD4</i>, <i>5</i>, <i>6</i>, and <i>8</i> were up-regulated, and <i>SOD7</i> was down-regulated in response to <i>A. minutum</i> feeding. After <i>A. catenella</i> exposure, all the <i>Cu/Zn-SOD</i>s except <i>SOD1</i> were up-regulated, and <i>SOD7</i> was down-regulated in kidney. Overall, in scallops after ingesting different toxic algae, <i>SOD</i> up-regulation mainly occurred in the expanded <i>Cu/Zn-SOD</i> group, and <i>SOD6</i> was the only member being up-regulated in both toxic organs, which also showed the highest fold change among all the <i>SOD</i>s, implying the importance of <i>SOD6</i> in protecting scallops from the stress of PSTs. Our results suggest the diverse function of scallop <i>SOD</i>s in response to the PST-producing algae challenge, and the expansion of <i>Cu/Zn-SOD</i>s might be implicated in the adaptive evolution of scallops or bivalves with respect to antioxidant defense against the ingested toxic algae.