Epipodial Tentacle Gene Expression and Predetermined Resilience to Summer Mortality in the Commercially Important Greenlip Abalone, Haliotis laevigata

Abstract

“Summer mortality” is a phenomenon that occurs during warm water temperature spikes that results in the mass mortality of many ecologically and economically important mollusks such as abalone. This study aimed to determine whether the baseline gene expression of abalone before a laboratory-induced summer mortality event was associated with resilience to summer mortality. Tentacle transcriptomes of 35 greenlip abalone (Haliotis laevigata) were sequenced prior to the animals being exposed to an increase in water temperature—simulating conditions which have previously resulted in summer mortality. Abalone derived from three source locations with different environmental conditions were categorized as susceptible or resistant to summer mortality depending on whether they died or survived after the water temperature was increased. We detected two genes showing significantly higher expression in resilient abalone relative to susceptible abalone prior to the laboratory-induced summer mortality event. One of these genes was annotated through the NCBI non-redundant protein database using BLASTX to an anemone (Exaiptasia pallida) Transposon Ty3-G Gag Pol polyprotein. Distinct gene expression signatures were also found between resilient and susceptible abalone depending on the population origin, which may suggest divergence in local adaptation mechanisms for resilience. Many of these genes have been suggested to be involved in antioxidant and immune-related functions. The identification of these genes and their functional roles have enhanced our understanding of processes that may contribute to summer mortality in abalone. Our study supports the hypothesis that prestress gene expression signatures are indicative of the likelihood of summer mortality.Electronic supplementary materialThe online version of this article (doi:10.1007/s10126-017-9742-z) contains supplementary material, which is available to authorized users.

Population structure, genetic connectivity, and adaptation in the Olympia oyster (Ostrea lurida) along the west coast of North America

“…One mapped to the O. lurida mitochondrial NADH dehydrogenase subunit 5 gene ( nad5 ), which exhibits high variability in oyster species and is commonly used for metazoan phylogenetics (Xiao, Wu, Li, & Yu, ). Annotated genes have potential roles in developmental regulation (glyoxalase 3, DNA N6‐methyl adenine demethylase‐like, transcriptional regulator ERG, and serine/threonine‐protein kinase), sensory information processing (serine/threonine‐protein kinase, sodium‐dependent phosphate transport, and vesicular glutamate transporter), immune or stress response ( nad5 , E3 ubiquitin‐protein ligase, Ty3‐G Gag‐Pol, and helicase domino), energy metabolism (carnitine palmitoyltransferase and glucose dehydrogenase), heavy metal binding (heavy metal‐binding protein HIP), and muscle contraction (myosin heavy chain‐striated muscle, myosin‐XVIIIa) (Table ) (Anderson et al., ; Cheng et al., ; de Lorgeril, Saulnier, Janech, Gueguen, & Bachère, ; Epelboin et al., ; Li, Song, Meng, Li, & Zhang, ; Pan, Marrs, & Ryan, ; Pauletto et al., ; Riviere et al., ; Shiel, Hall, Cooke, Robinson, & Strugnell, ; Szent‐Györgyi, Kalabokis, & Perreault‐Micale, ; Wang et al., ). Twenty‐one additional outlier GBS loci had positive matches to InterPro signatures without any BLASTx hits or gene ontology annotation.…”

“…(Anderson et al, 2015;Cheng et al, 2016;de Lorgeril, Saulnier, Janech, Gueguen, & Bachère, 2005;Epelboin et al, 2016;Li, Song, Meng, Li, & Zhang, 2017;Pan, Marrs, & Ryan, 2015;Pauletto et al, 2017;Riviere et al, 2013;Shiel, Hall, Cooke, Robinson, & Strugnell, 2017;Szent-Györgyi, Kalabokis, & Perreault- Micale, 1999;Wang et al, 2018). Twenty-one additional outlierGBS loci had positive matches to InterPro signatures without any BLASTx hits or gene ontology annotation.…”

Population structure, genetic connectivity, and adaptation in the Olympia oyster (Ostrea lurida) along the west coast of North America

“…One mapped to the O. lurida mitochondrial NADH dehydrogenase subunit 5 gene ( nad5 ), which exhibits high variability in oyster species and is commonly used for metazoan phylogenetics (Xiao et al, 2015). Annotated genes have potential roles in developmental regulation (glyoxalase 3, DNA N6-methyl adenine demethylase-like, transcriptional regulator ERG, serine/threonine-protein kinase), sensory information processing (serine/threonine-protein kinase, sodium-dependent phosphate transport, vesicular glutamate transporter), immune or stress response ( nad5 , E3 ubiquitin-protein ligase, Ty3-G Gag-Pol, helicase domino), energy metabolism (carnitine palmitoyltransferase, glucose dehydrogenase), heavy metal binding (Heavy metal-binding HIP), and muscle contraction (myosin heavy chain-striated muscle, myosin-XVIIIa) (Table 3) Epelboin et al (2016); Szent-Gyö rgyi et al (1999); Li et al (2017); Cheng et al (2016); Anderson et al (2015); Riviere et al (2013); Pauletto et al (2017); Wang et al (2018); Shiel et al (2017); Pan et al (2015); de Lorgeril et al (2005). 21 additional outlier GBS loci had positive matches to InterPro signatures without any BLASTx hits or gene ontology annotation.…”

Seascape genomics reveals adaptive divergence in a connected and commercially important mollusc, the greenlip abalone (Haliotis laevigata), along a longitudinal environmental gradient

“…Differences in optimal temperatures for growth and critical maximum temperature have been reported between greenlip abalone originating from warmer (Stone et al., ) and cooler waters (Gilroy & Edwards, ). Likewise, gene expression profiles in greenlip abalone have been found to be predictors of resilience to summer mortality that occurs in association with raised temperature and lowered oxygen levels (Shiel, Hall, Cooke, Robinson, Stone et al., ; Shiel, Hall, Cooke, Robinson, & Strugnell, ). Our results suggest that such fitness differences reported for greenlip abalone populations are due to genetic adaptations associated with local temperature and oxygen availability occurring at small spatial scales.…”