Dataset Information

Combined stress of ocean acidification and warming influence survival and drives differential gene expression patterns in the Antarctic pteropod, Limacina helicina antarctica.

ABSTRACT: The ecologically important thecosome pteropods in the Limacina spp. complex have recently been the focus of studies examining the impacts global change factors - e.g., ocean acidification (OA) and ocean warming (OW) - on their performance and physiology. This focus is driven by conservation concerns where the health of pteropod populations is threatened by the high susceptibility of their shells to dissolution in low aragonite saturation states associated with OA and how coupling of these stressors may push pteropods past the limits of physiological plasticity. In this manipulation experiment, we describe changes in the transcriptome of the Antarctic pteropod, Limacina helicina antarctica, to these combined stressors. The conditions used in the laboratory treatments met or exceeded those projected for the Southern Ocean by the year 2100. We made two general observations regarding the outcome of the data: (1) Temperature was more influential than pH in terms of changing patterns of gene expression, and (2) these Antarctic pteropods appeared to have a significant degree of transcriptomic plasticity to respond to acute abiotic stress in the laboratory. In general, differential gene expression was observed amongst the treatments; here, for example, transcripts associated with maintaining protein structure and cell proliferation were up-regulated. To disentangle the effects of OA and OW, we used a weighted gene co-expression network analysis to explore patterns of change in the transcriptome. This approach identified gene networks associated with OW that were enriched for transcripts proposed to be involved in increasing membrane fluidity at warmer temperatures. Together these data provide evidence that L.h.antarctica has a limited capacity to acclimate to the combined conditions of OA and OW used in this study. This reduced scope of acclimation argues for continued study of how adaptation to polar aquatic environments may limit the plasticity of present-day populations in responding to future environmental change.

SUBMITTER: Johnson KM

PROVIDER: S-EPMC7098371 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Combined stress of ocean acidification and warming influence survival and drives differential gene expression patterns in the Antarctic pteropod, <i>Limacina helicina antarctica</i>.

Johnson Kevin M KM Hofmann Gretchen E GE

Conservation physiology 20200326 1

The ecologically important thecosome pteropods in the <i>Limacina spp.</i> complex have recently been the focus of studies examining the impacts global change factors - e.g., ocean acidification (OA) and ocean warming (OW) - on their performance and physiology. This focus is driven by conservation concerns where the health of pteropod populations is threatened by the high susceptibility of their shells to dissolution in low aragonite saturation states associated with OA and how coupling of these ...[more]

PMID: 32257214

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Project description: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.

Project description:Anthropogenic CO2 is rapidly causing oceans to become warmer and more acidic, challenging marine ectotherms to respond to simultaneous changes in their environment. While recent work has highlighted that marine fishes, particularly during early development, can be vulnerable to ocean acidification, we lack an understanding of how life-history strategies, ecosystems and concurrent ocean warming interplay with interspecific susceptibility. To address the effects of multiple ocean changes on cold-adapted, slowly developing fishes, we investigated the interactive effects of elevated partial pressure of carbon dioxide (pCO2) and temperature on the embryonic physiology of an Antarctic dragonfish (Gymnodraco acuticeps), with protracted embryogenesis (∼10 months). Using an integrative, experimental approach, our research examined the impacts of near-future warming [-1 (ambient) and 2°C (+3°C)] and ocean acidification [420 (ambient), 650 (moderate) and 1000 μatm pCO2 (high)] on survival, development and metabolic processes over the course of 3 weeks in early development. In the presence of increased pCO2 alone, embryonic mortality did not increase, with greatest overall survival at the highest pCO2. Furthermore, embryos were significantly more likely to be at a later developmental stage at high pCO2 by 3 weeks relative to ambient pCO2. However, in combined warming and ocean acidification scenarios, dragonfish embryos experienced a dose-dependent, synergistic decrease in survival and developed more slowly. We also found significant interactions between temperature, pCO2 and time in aerobic enzyme activity (citrate synthase). Increased temperature alone increased whole-organism metabolic rate (O2 consumption) and developmental rate and slightly decreased osmolality at the cost of increased mortality. Our findings suggest that developing dragonfish are more sensitive to ocean warming and may experience negative physiological effects of ocean acidification only in the presence of an increased temperature. In addition to reduced hatching success, alterations in development and metabolism due to ocean warming and acidification could have negative ecological consequences owing to changes in phenology (i.e. early hatching) in the highly seasonal Antarctic ecosystem.

Project description:Rising seawater temperature and ocean acidification threaten the survival of coral reefs. The relationship between coral physiology and its microbiome may reveal why some corals are more resilient to these global change conditions. Here, we conducted the first experiment to simultaneously investigate changes in the coral microbiome and coral physiology in response to the dual stress of elevated seawater temperature and ocean acidification expected by the end of this century. Two species of corals, Acropora millepora containing the thermally sensitive endosymbiont C21a and Turbinaria reniformis containing the thermally tolerant endosymbiont Symbiodinium trenchi, were exposed to control (26.5°C and pCO2 of 364 μatm) and treatment (29.0°C and pCO2 of 750 μatm) conditions for 24 days, after which we measured the microbial community composition. These microbial findings were interpreted within the context of previously published physiological measurements from the exact same corals in this study (calcification, organic carbon flux, ratio of photosynthesis to respiration, photosystem II maximal efficiency, total lipids, soluble animal protein, soluble animal carbohydrates, soluble algal protein, soluble algal carbohydrate, biomass, endosymbiotic algal density, and chlorophyll a). Overall, dually stressed A. millepora had reduced microbial diversity, experienced large changes in microbial community composition, and experienced dramatic physiological declines in calcification, photosystem II maximal efficiency, and algal carbohydrates. In contrast, the dually stressed coral T. reniformis experienced a stable and more diverse microbiome community with minimal physiological decline, coupled with very high total energy reserves and particulate organic carbon release rates. Thus, the microbiome changed and microbial diversity decreased in the physiologically sensitive coral with the thermally sensitive endosymbiotic algae but not in the physiologically tolerant coral with the thermally tolerant endosymbiont. Our results confirm recent findings that temperature-stress tolerant corals have a more stable microbiome, and demonstrate for the first time that this is also the case under the dual stresses of ocean warming and acidification. We propose that coral with a stable microbiome are also more physiologically resilient and thus more likely to persist in the future, and shape the coral species diversity of future reef ecosystems.

Dataset Information

Combined stress of ocean acidification and warming influence survival and drives differential gene expression patterns in the Antarctic pteropod, Limacina helicina antarctica.

Publications

Combined stress of ocean acidification and warming influence survival and drives differential gene expression patterns in the Antarctic pteropod, <i>Limacina helicina antarctica</i>.

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