Comparative transcriptomics across populations offers new insights into the evolution of thermal resistance in marine snails

Wang, Wei; Hui, Jerome H. L.; Williams, Gray A.; Cartwright, Stephen Robert; Tsang, Ling Ming; Chu, Ka Hou

doi:10.1007/s00227-016-2873-3

Cited by 7 publications

(8 citation statements)

References 60 publications

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“…Comparative transcriptomics has proven to be a powerful tool for examining organism-environment interactions in non-model species [ 1 ]. This approach has been applied in both laboratory and field settings, and has become a common method with which to assess physiological responses in marine taxa [ 2 – 5 ]. The advantages of comparative transcriptomics are particularly valuable in marine systems, where differential gene expression analysis has been used to explore how organisms respond to their abiotic environment.…”

Section: Introductionmentioning

confidence: 99%

“…The advantages of comparative transcriptomics are particularly valuable in marine systems, where differential gene expression analysis has been used to explore how organisms respond to their abiotic environment. Examples include studies on adaptations to thermal stress [ 2 , 3 ], population-level variation in tolerance [ 4 , 5 ], and increasingly, studies conducted in a global change context [ 1 , 6 , 7 ]. In this study, we use the analysis of differential gene expression to examine the resistance of a key member of the zooplankton in the Southern Ocean, the shelled pteropod Limacina helicina antarctica , to the impacts of an advancing anthropogenic stress, ocean acidification.…”

Section: Introductionmentioning

confidence: 99%

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Transcriptomic response of the Antarctic pteropod Limacina helicina antarctica to ocean acidification

Johnson

Hofmann

2017

BMC Genomics

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BackgroundOcean acidification (OA), a change in ocean chemistry due to the absorption of atmospheric CO2 into surface oceans, challenges biogenic calcification in many marine organisms. Ocean acidification is expected to rapidly progress in polar seas, with regions of the Southern Ocean expected to experience severe OA within decades. Biologically, the consequences of OA challenge calcification processes and impose an energetic cost.ResultsIn order to better characterize the response of a polar calcifier to conditions of OA, we assessed differential gene expression in the Antarctic pteropod, Limacina helicina antarctica. Experimental levels of pCO2 were chosen to create both contemporary pH conditions, and to mimic future pH expected in OA scenarios. Significant changes in the transcriptome were observed when juvenile L. h. antarctica were acclimated for 21 days to low-pH (7.71), mid-pH (7.9) or high-pH (8.13) conditions. Differential gene expression analysis of individuals maintained in the low-pH treatment identified down-regulation of genes involved in cytoskeletal structure, lipid transport, and metabolism. High pH exposure led to increased expression and enrichment for genes involved in shell formation, calcium ion binding, and DNA binding. Significant differential gene expression was observed in four major cellular and physiological processes: shell formation, the cellular stress response, metabolism, and neural function. Across these functional groups, exposure to conditions that mimic ocean acidification led to rapid suppression of gene expression.ConclusionsResults of this study demonstrated that the transcriptome of the juvenile pteropod, L. h. antarctica, was dynamic and changed in response to different levels of pCO2. In a global change context, exposure of L. h. antarctica to the low pH, high pCO2 OA conditions resulted in a suppression of transcripts for genes involved in key physiological processes: calcification, metabolism, and the cellular stress response. The transcriptomic response at both acute and longer-term acclimation time frames indicated that contemporary L. h. antarctica may not have the physiological plasticity necessary for adaptation to OA conditions expected in future decades. Lastly, the differential gene expression results further support the role of shelled pteropods such as L. h. antarctica as sentinel organisms for the impacts of ocean acidification.Electronic supplementary materialThe online version of this article (10.1186/s12864-017-4161-0) contains supplementary material, which is available to authorized users.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Transcriptomic response of the Antarctic pteropod Limacina helicina antarctica to ocean acidification

Johnson

Hofmann

2017

BMC Genomics

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“…They experience prolonged emersion periods during neap tides, as well as extreme environmental temperatures over 50°C in the case of Echinolittorina species (Williams and Morritt, 1995;Uglow and Williams, 2001;Marshall et al, 2010). Snails of the genus Echinolittorina are distributed widely on the high intertidal shore and exhibit high upper thermal limits (>55°C) and a series of behavioral, morphological, physiological and biochemical responses to cope with thermal stresses Wang et al, 2016;Li, 2012;Wong, 2013). Echinolittorina malaccana is a common species in the splash zone and high intertidal zone in southern China and Southeast Asia, reaching higher tidal levels than any other sympatric congeners (Reid et al, 2006;Marshall and Chua, 2012).…”

Section: Introductionmentioning

confidence: 99%

“…In studies of wholeorganism and cardiac thermal tolerance, no mortality was observed after 24 h exposure at temperatures between 42 and 46°C for E. malaccana, and the values of Arrhenius breakpoint temperature for heart rate of E. malaccana and E. radiata were 46.5-48.2°C Li, 2012). For E. malaccana, the temperature at which 50% of a population died (LT 50 ) was 56.3-57.1°C (Wang et al, 2016); E. radiata showed a slightly lower upper thermal limit of 55.5°C (Li, 2012).…”

Section: Introductionmentioning

confidence: 99%

Heat-resistant cytosolic malate dehydrogenases (cMDHs) of thermophilic intertidal snails (genus Echinolittorina): protein underpinnings of tolerance to body temperatures reaching 55°C

Liao

Zhang

et al. 2017

Journal of Experimental Biology

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Snails of the genus Echinolittorina are among the most heat-tolerant animals; they experience average body temperatures near 41-44°C in summer and withstand temperatures up to at least 55°C. Here, we demonstrate that heat stability of function (indexed by the MichaelisMenten constant of the cofactor NADH, K M NADH ) and structure (indexed by rate of denaturation) of cytosolic malate dehydrogenases (cMDHs) of two congeners (E. malaccana and E. radiata) exceeds values previously found for orthologs of this protein from less thermophilic species. The ortholog of E. malaccana is more heat stable than that of E. radiata, in keeping with the congeners' thermal environments. Only two inter-congener differences in amino acid sequence in these 332 residue proteins were identified. In both cases ( positions 48 and 114), a glycine in the E. malaccana ortholog is replaced by a serine in the E. radiata protein. To explore the relationship between structure and function and to characterize how amino acid substitutions alter stability of different regions of the enzyme, we used molecular dynamics simulation methods. These computational methods allow determination of thermal effects on finescale movements of protein components, for example, by estimating the root mean square deviation in atom position over time and the root mean square fluctuation for individual residues. The minor changes in amino acid sequence favor temperature-adaptive change in flexibility of regions in and around the active sites. Interspecific differences in effects of temperature on fine-scale protein movements are consistent with the differences in thermal effects on binding and rates of heat denaturation.

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“…Third, thermal stress can impact organisms at different life-history stages, from embryos to adults. However, many previous studies have focused on the effect of thermal stress on postembryonic lifehistory stages rather than on embryos (e.g., Esperk et al, 2016;Sentis, Hemptinne, & Brodeur, 2017;Wang et al 2016), despite of the fact that embryos are often more sensitive and vulnerable to temperature variation than later life-history stages. Most reptile embryos are restricted to small spaces and have limited thermoregulatory opportunities (Deeming, 2004; but see Du, Zhao, Chen, & Shine, 2011).…”

Section: Introductionmentioning

confidence: 99%

The vulnerability of developing embryos to simulated climate warming differs between sympatric desert lizards

Sun

et al. 2018

J Exp Zool Pt A

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The vulnerability of species to climate warming varies along latitudinal and elevational clines, but how sympatric species vary in vulnerability to climate warming remains largely unknown. We experimentally simulated nest temperatures of two sympatric lizards with divergent microhabitat preferences (Phrynocephalus przewalskii and Eremias argus), under climate warming senarios, to determine the response of embryos to increased mean temperatures and heat waves. Our study demonstrated that simulated climate warming reduced hatching success and hatchling size and growth in E. argus (that prefers closed microhabitats), but had less effect in P. przewalskii (that occupies open microhabitats). The reduced growth rate of E. argus hatchlings was associated with a decrease in metabolic rate, which was more evident in hatchling E. argus than in P. przewalskii. Our results suggest lizards that prefer closed microhabitats may be more vulnerable to climate warming than those that prefer open microhabitats; further studies are needed to test this hypothesis. More generally, the divergent responses of sympatric species to climate warming highlights the importance of distinguishing the thermal sensitivity of behavior and physiology for each species of a community, in order to make predictions about the impacts of climate warming at regional scales.

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Comparative transcriptomics across populations offers new insights into the evolution of thermal resistance in marine snails

Cited by 7 publications

References 60 publications

Transcriptomic response of the Antarctic pteropod Limacina helicina antarctica to ocean acidification

Transcriptomic response of the Antarctic pteropod Limacina helicina antarctica to ocean acidification

Heat-resistant cytosolic malate dehydrogenases (cMDHs) of thermophilic intertidal snails (genus Echinolittorina): protein underpinnings of tolerance to body temperatures reaching 55°C

The vulnerability of developing embryos to simulated climate warming differs between sympatric desert lizards

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