Anthropogenic CO2 emissions are altering marine ecosystems through two interconnected processes: climate change and ocean acidification, both of which are particularly affecting the Southern Ocean. However, the molecular responses of cold-water corals to these stressors remain poorly understood. In this study, we investigated the transcriptomic response of the Antarctic coral Malacobelemnon daytoni exposed to ocean acidification (pH ~7.7; LpH) and elevated temperatures (+2°C and +4°C above ambient; T1 and T2, respectively) under controlled laboratory conditions. Using high-throughput RNA sequencing (RNA-Seq), we compared gene expression profiles across six treatments, including a control (pH ~8.1, CpH; 0–1°C; CT), acidification, warming, and their combinations. Principal component analysis revealed treatment-specific clustering and greater transcriptomic dispersion under LpH conditions. Differential expression analysis identified between 475 and 767 differentially expressed genes (DEGs), with the strongest transcriptional responses observed under combined stress conditions (LpH + T1 and LpH + T2). Combined exposure to ocean acidification and warming elicited the largest gene expression response, suggesting enhanced, potentially non-additive effects of multiple stressors. Functional enrichment analyses revealed differential regulation of genes associated with protein folding, signal transduction, energy metabolism, oxidative stress, and regulation of cell death. Our findings demonstrate that Malacobelemnon daytoni exhibits complex, treatment-dependent gene expression responses to environmental stressors. These results highlight the capacity of this Antarctic octocoral to mount molecular responses to projected future ocean conditions while also emphasizing its potential vulnerability to the interacting effects of ocean warming and acidification.
Regulation of gene expression is a pivotal adaptive mechanism of organisms facing environmental variation. We studied the in situ gene expression of the shallow-water bivalve Aequiyoldia eightsii in Potter Cove (King George Island, Antarctica) occupying different habitats in front of a melting glacier on a local scale (1 km). The expression of nuclear genes was determined by (1) variation of the nuclear genome itself (nuclear SNPs) and equally strongly by (2) different environmental conditions characterizing the three locations and (3) the composition of the mitochondrial genotype (mitochondrial SNPs). Mitochondrial SNPs divided Antarctic animals into two groups, each composed of organisms featuring mitochondrial homoplasmy and heteroplasmy. We validated our results by contrasting the observed magnitudes of differentially expressed genes (DEGs) with magnitudes expected by stochasticity in randomized group comparisons. Habitat comparison revealed further differences in DEGs at local scale suggesting a high evolutionary adaptive potential to the specific microenvironments. Interestingly, differential expression analysis between mitotypes resulted in a higher number of DEGs than the obtained in the comparison by stations, distinguishing heteroplasmic from homoplasmic organisms. Our results suggest that the mitochondrial genome and possibly heteroplasmy may play a role in the regulation of nuclear gene expression with adaptive implications.
Benthic suspension feeders like corals and sponges are important bioengineers in many marine habitats, from the shallow tropics to the depth of polar oceans. While they are generally considered opportunistic, little is known about their actual in situ diet. To tackle this limitation, fatty acid trophic markers (FATMs) have been employed to gain insights into the composition of their diet. Yet, these in situ studies have not been combined with physiological investigations to understand how physiological limitations may modulate the biochemistry of these organisms.Here, we used the cold-water coral (CWC) Desmophyllum dianthus in its natural habitat in Comau Fjord (Northern Patagonia, Chile) as our model species to assess the trophic ecology in response to contrasting physico-chemical conditions (variable vs. stable) and ecological drivers (food availability) at three shallow sites and one deep site. We took advantage of the expression of two distinct phenotypes with contrasting performance (growth, biomass, respiration) coinciding with the differences in sampling depth. We analysed the corals' fatty acid composition to evaluate the utility of FATM profiles to gain dietary insights and assess how performance trade-offs potentially modulate an organism's FATM composition. We found that 20:1(n-9) zooplankton markers dominated the deep high-performance phenotype, while 20:5(n-3) and 22:6(n-3) diatom and flagellate markers, respectively, are more prominent in shallow low-performance phenotype. Surprisingly, both energy stores and performance were higher in the deep phenotype, in spite of measured lower zooplankton availability.Essential FA concentrations were conserved across sites, likely reflecting required levels for coral functioning and survival. While the deep high-performance phenotype met with these requirements, the low-performance phenotype appeared to need more energy to maintain functionality in its highly variable environment, potentially causing intrinsic re-allocations of energy and enrichment in certain essential markers (20:5(n-3), 22:6(n-3)).Our analysis highlights the biological and ecological insights that can be gained from FATM profiles in CWCs, but also cautions the reliability of FATM as diet tracers under limiting environmental conditions that may also be applicable to other marine organisms.Read the free Plain Language Summary for this article on the Journal blog. Read the free Plain Language Summary for this article on the Journal blog.image
IntroductionHyperiid amphipods of the genus Themisto are a key polar zooplankton group in terms of biomass and play an important role as prey for higher trophic levels. They are prone to undergo changes in abundance and distribution in the course of the ongoing environmental changes. In the Southern Ocean, Themisto gaudichaudii is predicted to expand its distribution poleward. In the Arctic, the boreal-Atlantic T. abyssorum increases in abundance, resulting in an increased competition with a genuine polar congener. It is not known, however, whether T. gaudichaudii and T. abyssorum have the potential to efficiently adapt to changing water temperatures at their current distribution range or whether they will be shifting their ranges poleward.MethodsWe exposed the two Themisto species from different geographic populations to temperature-change experiments, a cold treatment and a heat-shock treatment. After that, we carried out transcriptome sequencing to compare gene expression patterns in the different treatments and species.ResultsWe show that under similar heat conditions, T. gaudichaudii differentially expressed more genes (26-fold change) than T. abyssorum. Furthermore, we observed qualitative differences between genetic clusters in T. gaudichaudii.DiscussionThe differences observed between genetic clusters in T. gaudichaudii suggest that evolutionary divergence can be linked to changes in the regulatory pathways involved in temperature stress. These could influence the capacity of each genetic cluster to cope differently with temperature changes. In contrast to its congeneric species, T. abyssorum showed a pronounced adaptive flexibility to thermal stress; it appears to have the ability to continue its poleward expansion but may also cope with increasing temperatures in its current environments. Our findings contribute to understand the response of two range-shifting Themisto species to thermal stress in view of the environmental gradients they encounter throughout their current or future distribution ranges.
The South Georgia region of the Southern Ocean represents the northernmost range edge for Antarctic krill. Of concern is the extent to which rapid warming of surface water temperatures and reduced oxygen contents around this region might challenge the physiological tolerance of krill, particularly the later maturity stages. Hypoxia is generally considered to be less than 30 to 20
Southern Ocean organisms are thought to be particularly vulnerable to ocean acidification (OA), as they inhabit cold waters where calcite-aragonite saturation states are naturally low. It is also generally assumed that calcifying animals would be more affected by OA than non-calcifying animals. In this context, we aimed to study the impact of reduced pH on both types of species: the ascidian Cnemidocarpa verrucosa sp. A, and the bivalve Aequiyoldia eightsii, from an Antarctic fjord. We used gene expression profiling and enzyme activity to study the responses of these two Antarctic benthic species to OA. We report the results of an experiment lasting 66 days, comparing the molecular mechanisms underlying responses under two pCO2 treatments (ambient and elevated pCO2). We observed 224 upregulated genes and 111 downregulated genes (FC ≥ 2; p value ≤ 0.05) in the ascidian. In particular, the decrease in pH caused an upregulation of genes involved in the immune system and antioxidant response. While fewer differentially expressed (DE) genes were observed in the infaunal bivalve, 34 genes were upregulated and 69 genes were downregulated (FC ≥ 2; p value ≤ 0.05) in response to OA. We found downregulated genes involved in the oxidoreductase pathway (such as glucose dehydrogenase and trimethyl lysine dioxygenase), while the heat shock protein 70 was upregulated. This work addresses the effect of OA in two common, widely distributed Antarctic species, showing, surprisingly, that the non-calcifying species had a more pronounced response.
When an organism makes a long-distance transition to a new habitat, the associated environmental change is often marked and requires physiological plasticity of larvae, juveniles, or other migrant stages. Exposing shallow-water marine bivalves (Aequiyoldia cf. eightsii) from southern South America (SSA) and the West Antarctic Peninsula (WAP) to changes in temperature and oxygen availability, we investigated changes in gene expression in a simulated colonization experiment of the shores of a new continent after crossing of the Drake Passage, and in a warming scenario in the WAP. Bivalves from SSA were cooled from 7°C (in situ) to 4°C and 2°C (future warmed WAP conditions), WAP bivalves were warmed from 1.5°C (current summer in situ) to 4°C (warmed WAP), gene expression patterns in response to thermal stress by itself and in combination with hypoxia were measured after 10 days. Our results confirm that molecular plasticity may play a vital role for local adaptation. Hypoxia had a greater effect on the transcriptome than temperature alone. The effect was further amplified when hypoxia and temperature acted as combined stressors. The WAP bivalves showed a remarkable ability to cope with short-term exposure to hypoxia by switching to a metabolic rate depression strategy and activating the alternative oxidation pathway, whilst the SSA population showed no comparable response. In SSA, the high prevalence of apoptosis-related differentially expressed genes especially under combined higher temperatures and hypoxia indicated that the SSA Aequiyoldia are operating near their physiological limits already. While the effect of temperature per se may not represent the single most effective barrier to Antarctic colonization by South American bivalves, the current distribution patterns as well as their resilience to future conditions can be better understood by looking at the synergistic effects of temperature in conjunction with short-term exposure to hypoxia.
Polar ecosystems are experiencing amongst the most rapid rates of regional warming on Earth. Here, we discuss ‘omics’ approaches to investigate polar biodiversity, including the current state of the art, future perspectives and recommendations. We propose a community road map to generate and more fully exploit multi-omics data from polar organisms. These data are needed for the comprehensive evaluation of polar biodiversity and to reveal how life evolved and adapted to permanently cold environments with extreme seasonality. We argue that concerted action is required to mitigate the impact of warming on polar ecosystems via conservation efforts, to sustainably manage these unique habitats and their ecosystem services, and for the sustainable bioprospecting of novel genes and compounds for societal gain.
Pocillopora damicornis (Linnaeus, 1758), a species complex, consists of several genetic lineages, some of which likely represent reproductively isolated species, including the species Pocillopora acuta Lamarck, 1816. Pocillopora acuta can exhibit similar morphological characteristics as P. damicornis, thus making it difficult to identify species-level taxonomic units. To determine whether the P. damicornis-like colonies on the reefs in the Andaman Sea (previously often identified as P. damicornis) consist of different species, we sampled individual colonies at five sites along a 50 km coastal stretch at Phuket Island and four island sites towards Krabi Province, Thailand. We sequenced 210 coral samples for the mitochondrial open reading frame and identified six distinct haplotypes, all belonging to P. acuta according to the literature. Recently, P. acuta was observed to efficiently recolonize heat-damaged reefs in Thailand as well as globally, making it a potentially important coral species in future reefs. Specifically in the light of global change, this study underscores the importance of high-resolution molecular species recognition, since taxonomic units are important factors for population genetic studies, and the latter are crucial for management and conservation efforts.
The species delimitation of the marine bivalve species complex Aequiyoldia eightsii in South America and Antarctica is complicated by mitochondrial heteroplasmy and amplification bias in molecular barcoding. In this study, we compare different data sources (mitochondrial cytochrome c oxidase subunit I (COI) sequences; nuclear and mitochondrial SNPs). Whilst all the data suggest that populations on either side of the Drake Passage belong to different species, the picture is less clear within Antarctic populations, which harbor three distinct mitochondrial lineages (p-dist ≈ 6%) that coexist in populations and in a subset of individuals with heteroplasmy. Standard barcoding procedures lead to amplification bias favoring either haplotype unpredictably and thus overestimate the species richness with high confidence. However, nuclear SNPs show no differentiation akin to the trans-Drake comparison, suggesting that the Antarctic populations represent a single species. Their distinct haplotypes likely evolved during periods of temporary allopatry, whereas recombination eroded similar differentiation patterns in the nuclear genome after secondary contact. Our study highlights the importance of using multiple data sources and careful quality control measures to avoid bias and increase the accuracy of molecular species delimitation. We recommend an active search for mitochondrial heteroplasmy and haplotype-specific primers for amplification in DNA-barcoding studies.
Abstract Background The widespread Indo-Pacific coral species Pocillopora acuta Lamarck, 1816 displays varying levels of asexual versus sexual reproduction, with strong repercussions on genetic diversity, connectivity and genetic structuring within and among populations. For many geographic regions, baseline information on genetic diversity is still lacking, particularly in the Andaman Sea. The region suffered a massive heat-induced bleaching event in 2010 with high coral cover loss of branching coral species such as P. acuta. A subsequent bleaching in 2016, however, revealed a mild bleaching response in pocilloporids compared to other coral taxa in the region, suggesting that rare, heat tolerant genotypes had been selected by the 2010 bleaching event. In order to test whether this potential ‘evolutionary rescue’ event has led to a low genetic diversity, we conducted a population genetic survey covering a total of nine different P. acuta populations (336 individuals) along a 50 km coastal stretch around Phuket Island, Thailand. We used six microsatellite markers to assess genotypic diversity and to determine the prevalent mode of reproduction (i.e. sexual or asexual recruitment). Results In contrast to other Indian Ocean P. acuta populations, the majority of corals in this study adopted a sexual reproduction mode (75% across all populations). At the same time, substantial regional gene flow was observed around Phuket Island with strong genetic differentiation as indicated by three genetic clusters that were separated by only a few kilometers. Patterns of isolation by distance over 0.7 – 40 km suggest small-scale genetic barriers, such as changing currents throughout each monsoonal season, potentially contributing to locally restricted dispersal of P. acuta larvae. Conclusions The occurrence of distinct genetic clusters within short coastal stretches suggests that the 2010 bleaching event has not led to extreme genetic impoverishment. While more in-depth genomic analyses are necessary to investigate changes in genetic diversity following extreme bleaching events, our results will help guide conservation efforts to maintain genetic diversity of a coral species that likely will be dominant in future, warmer Andaman Sea reefs.
The removal of carbon from the atmosphere for a long period (sequestration) is an increasingly pressing societal need in order to mitigate the negative effects of climate change. Investment and technology solutions are moving in the direction of industrial carbon capture and storage. To date, this technology is inefficient, expensive, and in some cases, not even net carbon zero. Optimistic estimates suggesting huge investment in infrastructure, which requires resources that include land and fresh water, will only marginally contribute toward the reductions in atmospheric CO2 required to minimize the impact of climate change over the next 50 years (Hankin et al., 2019).
Southern Ocean organisms are considered particularly vulnerable to Ocean acidification (OA), as they inhabit cold waters where calcite-aragonite saturation states are naturally low. It is also generally assumed that OA would affect calcifying animals more than non-calcifying animals. In this context, we aimed to study the impact of reduced pH on both types of species: the ascidian Cnemidocarpa verrucosa sp. A, and the bivalve Aequiyoldia eightsii, from an Antarctic fjord. We used gene expression profiling and enzyme activity to study the responses of these two Antarctic benthic species to OA. We report the results of an experiment lasting 66 days, comparing the molecular mechanisms underlying responses under two pCO2 treatments (ambient and elevated pCO2). We observed 224 up-regulated and 111 down-regulated genes (FC ≥ 2; p-value ≤ 0.05) in the ascidian. In particular, the decrease in pH caused an upregulation of genes involved in the immune system and antioxidant response. While fewer differentially expressed (DE) genes were observed in the infaunal bivalve, 34 genes were up-regulated, and 69 genes were downregulated (FC ≥ 2; p-value ≤ 0.05) in response to OA. We found downregulated genes involved in the oxidoreductase pathway (such as glucose dehydrogenase and trimethyl lysine dioxygenase), while the heat shock protein 70 was up-regulated. This work addresses the effect of OA in two common, widely distributed Antarctic species, showing striking results. Our major finding highlights the impact of OA on the non-calcifying species, a result that differ from the general trend, which describes a higher impact on calcifying species. This calls for discussion of potential effects on non-calcifying species, such as ascidians, a diverse and abundant group that form extended three-dimensional clusters in shallow waters and shelf areas in the Southern Ocean.
Cold-water corals (CWCs) are considered vulnerable to environmental changes. However, previous studies have focused on adult CWCs and mainly investigated the short-term effects of single stressors. So far, the effects of environmental changes on different CWC life stages are unknown, both for single and multiple stressors and over long time periods. Therefore, we conducted a six-month aquarium experiment with three life stages of Caryophyllia huinayensis to study their physiological response (survival, somatic growth, calcification and respiration) to the interactive effects of aragonite saturation (0.8 and 2.5), temperature (11 and 15 degrees C) and food availability (8 and 87 & mu;g C L-1). The response clearly differed between life stages and measured traits. Elevated temperature and reduced feeding had the greatest effects, pushing the corals to their physiological limits. Highest mortality was observed in adult corals, while calcification rates decreased the most in juveniles. We observed a three-month delay in response, presumably because energy reserves declined, suggesting that short-term experiments overestimate coral resilience. Elevated summer temperatures and reduced food supply are likely to have the greatest impact on live CWCs in the future, leading to reduced coral growth and population shifts due to delayed juvenile maturation and high adult mortality.
Systematic long-term studies on ecosystem dynamics are largely lacking from the East Antarctic Southern Ocean, although it is well recognized that they are indispensable to identify the ecological impacts and risks of environmental change. Here, we present a framework for establishing a long-term cross-disciplinary study on decadal timescales. We argue that the eastern Weddell Sea and the adjacent sea to the east, off Dronning Maud Land, is a particularly well suited area for such a study, since it is based on findings from previous expeditions to this region. Moreover, since climate and environmental change have so far been comparatively muted in this area, as in the eastern Antarctic in general, a systematic long-term study of its environmental and ecological state can provide a baseline of the current situation, which will be important for an assessment of future changes from their very onset, with consistent and comparable time series data underpinning and testing models and their projections. By establishing an Integrated East Antarctic Marine Research (IEAMaR) observatory, long-term changes in ocean dynamics, geochemistry, biodiversity, and ecosystem functions and services will be systematically explored and mapped through regular autonomous and ship-based synoptic surveys. An associated long-term ecological research (LTER) programme, including experimental and modelling work, will allow for studying climate-driven ecosystem changes and interactions with impacts arising from other anthropogenic activities. This integrative approach will provide a level of long-term data availability and ecosystem understanding that are imperative to determine, understand, and project the consequences of climate change and support a sound science-informed management of future conservation efforts in the Southern Ocean.
Rapid regional warming causing glacial retreat and melting of ice caps in Antarctica leads benthic filter-feeders to be exposed to periods of food shortage and high respiratory impairment as a consequence of seasonal sediment discharge in the West Antarctic Peninsula coastal areas. The molecular physiological response and its fine-tuning allow species to survive acute environmental stress and are thus a prerequisite to longer-term adaptation to changing environments. Under experimental conditions, we analyzed here the metabolic response to changes in suspended sediment concentrations, through transcriptome sequencing and enzymatic measurements in a highly abundant Antarctic ascidian. We found that the mechanisms underlying short-term response to sedimentation in Cnemidocarpa verrucosa sp. A involved apoptosis, immune defense, and general metabolic depression. These mechanisms may be understood as an adaptive protection against sedimentation caused by glacial retreat. This process can strongly contribute to the structuring of future benthic filter-feeder communities in the face of climate change.
Parallel phenotypic divergence is the independent differentiation between phenotypes of the same lineage or species occupying ecologically similar environments in different populations. We tested in the Antarctic limpet Nacella concinna the extent of parallel morphological divergence in littoral and sublittoral ecotypes throughout its distribution range. These ecotypes differ in morphological, behavioural and physiological characteristics. We studied the lateral and dorsal outlines of shells and the genetic variation of the mitochondrial gene Cytochrome Oxidase subunit I from both ecotypes in 17 sample sites along more than 2,000 km. The genetic data indicate that both ecotypes belong to a single evolutionary lineage. The magnitude and direction of phenotypic variation differ between ecotypes across sample sites; completely parallel ecotype-pairs (i.e., they diverge in the same magnitude and in the same direction) were detected in 84.85% of lateral and 65.15% in dorsal view comparisons. Besides, specific traits (relative shell height, position of shell apex, and elliptical/pear-shape outline variation) showed high parallelism. We observed weak morphological covariation between the two shape shell views, indicating that distinct evolutionary forces and environmental pressures could be acting on this limpet shell shape. Our results demonstrate there is a strong parallel morphological divergence pattern in N. concinna along its distribution, making this Antarctic species a suitable model for the study of different evolutionary forces shaping the shell evolution of this limpet.
Metazoans normally possess a single lineage of mitochondria inherited from the mother (♀-type mitochondria) while paternal mitochondria are absent or eliminated in fertilized eggs. In doubly uniparental inheritance (DUI), which is specific to the bivalve clade including the ocean quahog, Arctica islandica , ♂-type mitochondria are retained in male gonads and, in a few species, small proportions of ♂-type mitochondria co-exist with ♀-type in somatic tissues. To the best of our knowledge, we report, for the first time in metazoan, the natural occurrence of male and female individuals with exclusively ♂-type mitochondria in somatic tissues of the bivalve A. islandica . Mitochondrial genomes differ by ~5.5% at DNA sequence level. Exclusive presence of ♂-type mitochondria affects mitochondrial complexes partially encoded by mitochondrial genes and leads to a sharp drop in respiratory capacity. Through a combination of whole mitochondrial genome sequencing and molecular assays (gene presence and expression), we demonstrate that 1) 11% of individuals of an Icelandic population appear homoplasmic for ♂-type mitochondria in somatic tissues, 2) ♂-type mitochondrial genes are transcribed and 3) individuals with ♂-type mitochondria in somatic cells lose 30% of their wild-type respiratory capacity. This mitochondrial pattern in A. islandica is a special case of DUI, highlighted in individuals from both sexes with functional consequences at cellular and conceivably whole animal level.
Benthic organisms of the Southern Ocean are particularly vulnerable to ocean acidification (OA), as they inhabit cold waters where calcite-aragonite saturation states are naturally low. OA most strongly affects animals with calcium carbonate skeletons or shells, such as corals and mollusks. We exposed the abundant cold-water coral Malacobelemnon daytoni from an Antarctic fjord to low pH seawater (LpH) (7.68 +/- 0.17) to test its physiological responses to OA, at the level of gene expression (RT-PCR) and enzyme activity. Corals were exposed in short- (3 days) and long-term (54 days) experiments to two pCO(2) conditions (ambient and elevated pCO(2) equaling RCP 8.5, IPCC 2019, approximately 372.53 and 956.78 mu atm, respectively). Of the eleven genes studied through RT-PCR, six were significantly upregulated compared with control in the short-term in the LpH condition, including the antioxidant enzyme superoxide dismutase (SOD), Heat Shock Protein 70 (HSP70), Toll-like receptor (TLR), galaxin and ferritin. After long-term exposure to low pH conditions, RT-PCR analysis showed seven genes were upregulated. These include the mannose-binding C-Lectin and HSP90. Also, the expression of TLR and galaxin, among others, continued to be upregulated after long-term exposure to LpH. Expression of carbonic anhydrase (CA), a key enzyme involved in calcification, was also significantly upregulated after long-term exposure. Our results indicated that, after two months, M. daytoni is not acclimatized to this experimental LpH condition. Gene expression profiles revealed molecular impacts that were not evident at the enzyme activity level. Consequently, understanding the molecular mechanisms behind the physiological processes in the response of a coral to LpH is critical to understanding the ability of polar species to cope with future environmental changes. Approaches integrating molecular tools into Antarctic ecological and/or conservation research make an essential contribution given the current ongoing OA processes.