Simultaneous ocean acidification and warming do not alter the lipid-associated biochemistry but induce enzyme activities in an asterinid starfish.

Ocean acidification and warming affect marine ecosystems from the molecular scale in organismal physiology to broad alterations of ecosystem functions. However, knowledge of their combined effects on tropical-subtropical intertidal species remains limited. Pushing the environmental range of marine species away from the optimum initiates stress impacting biochemical metabolic characteristics, with consequences on lipid-associated and enzyme biochemistry. This study investigates lipid-associated fatty acids (FAs) and enzyme activities involved in biomineralization of the tropical-subtropical starfish Aquilonastra yairi in response to projected near-future global change. The starfish were acclimatized to two temperature levels (27 °C, 32 °C) crossed with three pCO2 concentrations (455 µatm, 1052 µatm, 2066 µatm). Total lipid (ΣLC) and FAs composition were unaffected by combined elevated temperature and pCO2, but at elevated temperature, there was an increase in ΣLC, SFAs (saturated FAs) and PUFAs (polyunsaturated FAs), and a decrease in MUFAs (monounsaturated FAs). However, temperature was the sole factor to significantly alter SFAs composition. Positive parabolic responses of Ca-ATPase and Mg-ATPase enzyme activities were detected at 27 °C with elevated pCO2, while stable enzyme activities were observed at 32 °C with elevated pCO2. Our results indicate that the lipid-associated biochemistry of A. yairi is resilient and capable of coping with near-future ocean acidification and warming. However, the calcification-related enzymes Ca-ATPase and Mg-ATPase activity appear to be more sensitive to pCO2/pH changes, leading to vulnerability concerning the skeletal structure.

Nanoplastic incorporation into an organismal skeleton.

Studies on the effects of global marine plastic pollution have largely focused on physiological responses of few organism groups (e.g., corals, fishes). Here, we report the first observation of polymer nanoparticles being incorporated into the calcite skeleton of a large benthic foraminifera (LBF), a significant contributor to global carbonate production. While previous work on LBF has documented selectivity in feeding behaviour and a high degree of specialization regarding skeletal formation, in this study, abundant cases of nanoplastic encrustation into the calcite tests were observed. Nanoplastic incorporation was associated with formation of new chambers, in conjunction with rapid nanoplastic ingestion and subsequent incomplete egestion. Microalgae presence in nanoplastic treatments significantly increased the initial feeding response after 1 day, but regardless of microalgae presence, nanoplastic ingestion was similar after 6 weeks of chronic exposure. While ~ 40% of ingesting LBF expelled all nanoplastics from their cytoplasm, nanoplastics were still attached to the test surface and subsequently encrusted by calcite. These findings highlight the need for further investigation regarding plastic pollution impacts on calcifying organisms, e.g., the function of LBF as potential plastic sinks and alterations in structural integrity of LBF tests that will likely have larger ecosystem-level impacts on sediment production.

Ecosystem design as an avenue for improving services provided by carbonate producing marine ecosystems.

Ecosystem Design (ED) is an approach for constructing habitats that places human needs for ecosystem services at the center of intervention, with the overarching goal of establishing self-sustaining habitats which require limited management. This concept was originally developed for use in mangrove ecosystems, and is understandably controversial, as it markedly diverges from other protection approaches that assign human use a minor priority or exclude it. However, the advantage of ED lies within the considered implementation of these designed ecosystems, thus preserving human benefits from potential later disturbances. Here, we outline the concept of ED in tropical carbonate depositional systems and discuss potential applications to aid ecosystem services such as beach nourishment and protection of coastlines and reef islands at risk from environmental and climate change, CO2 sequestration, food production, and tourism. Biological carbonate sediment production is a crucial source of stability of reef islands and reef-rimmed coastlines. Careful implementation of designed carbonate depositional ecosystems could help counterbalance sea-level rise and manage documented erosion effects of coastal constructions. Importantly, adhering to the core ethos of ED, careful dynamic assessments which provide a balanced approach to maximizing ecosystem services (e.g., carbonate production), should identify and avoid any potential damages to existing functioning ecosystems.

Diversity and flexibility of algal symbiont community in globally distributed larger benthic foraminifera of the genus Amphistegina.

BACKGROUND: Understanding the specificity and flexibility of the algal symbiosis-host association is fundamental for predicting how species occupy a diverse range of habitats. Here we assessed the algal symbiosis diversity of three species of larger benthic foraminifera from the genus Amphistegina and investigated the role of habitat and species identity in shaping the associated algal community. RESULTS: We used next-generation sequencing to identify the associated algal community, and DNA barcoding to identify the diatom endosymbionts associated with species of A. lobifera, A. lessonii, and A. radiata, collected from shallow habitats (< 15 m) in 16 sites, ranging from the Mediterranean Sea to French Polynesia. Next-generation sequencing results showed the consistent presence of Ochrophyta as the main algal phylum associated with all species and sites analysed. A significant proportion of phylotypes were classified as Chlorophyta and Myzozoa. We uncovered unprecedented diversity of algal phylotypes found in low abundance, especially of the class Bacillariophyta (i.e., diatoms). We found a significant influence of sites rather than host identity in shaping algal communities in all species. DNA barcoding revealed the consistent presence of phylotypes classified within the order Fragilariales as the diatoms associated with A. lobifera and A. lessonii, while A. radiata specimens host predominately diatoms of the order Triceratiales. CONCLUSIONS: We show that local habitat is the main factor influencing the overall composition of the algal symbiont community. However, host identity and the phylogenetic relationship among hosts is relevant in shaping the specific endosymbiont diatom community, suggesting that the relationship between diatom endosymbiont and hosts plays a crucial role in the evolutionary history of the genus Amphistegina. The capacity of Amphistegina species to associate with a diverse array of diatoms, and possibly other algal groups, likely underpins the ecological success of these crucial calcifying organisms across their extensive geographic range.

Nutrient History Affects the Response and Resilience of the Tropical Seagrass Halophila stipulacea to Further Enrichment in Its Native Habitat.

Eutrophication is one of the main threats to seagrass meadows, but there is limited knowledge on the interactive effects of nutrients under a changing climate, particularly for tropical seagrass species. This study aimed to detect the onset of stress in the tropical seagrass, Halophila stipulacea, by investigating the effect of in situ nutrient addition during an unusually warm summer over a 6-month period. We measured a suite of different morphological and biochemical community metrics and individual plant traits from two different sites with contrasting levels of eutrophication history before and after in situ fertilization in the Gulf of Aqaba. Nutrient stress combined with summer temperatures that surpassed the threshold for optimal growth negatively affected seagrass plants from South Beach (SB), an oligotrophic marine protected area, while H. stipulacea populations from North Beach (NB), a eutrophic and anthropogenically impacted area, benefited from the additional nutrient input. Lower aboveground (AG) and belowground (BG) biomass, reduced Leaf Area Index (LAI), smaller internodal distances, high sexual reproductive effort and the increasing occurrence of apical shoots in seagrasses from SB sites indicated that the plants were under stress and not growing under optimal conditions. Moreover, AG and BG biomass and internodal distances decreased further with the addition of fertilizer in SB sites. Results presented here highlight the fact that H. stipulacea is one of the most tolerant and plastic seagrass species. Our study further demonstrates that the effects of fertilization differ significantly between meadows that are growing exposed to different levels of anthropogenic pressures. Thus, the meadow's "history" affects it resilience and response to further stress. Our results suggest that monitoring efforts on H. stipulacea populations in its native range should focus especially on carbohydrate reserves in leaves and rhizomes, LAI, internodal length and percentage of apical shoots as suitable warning indicators for nutrient stress in this seagrass species to minimize future impacts on these valuable ecosystems.

High dispersal capacity and biogeographic breaks shape the genetic diversity of a globally distributed reef-dwelling calcifier.

Understanding the role of dispersal and adaptation in the evolutionary history of marine species is essential for predicting their response to changing conditions. We analyzed patterns of genetic differentiation in the key tropical calcifying species of large benthic foraminifera Amphistegina lobifera to reveal the evolutionary processes responsible for its biogeographic distribution. We collected specimens from 16 sites encompassing the entire range of the species and analyzed hypervariable fragments of the 18S SSU rDNA marker. We identified six hierarchically organized genotypes with mutually exclusive distribution organized along a longitudinal gradient. The distribution is consistent with diversification occurring in the Indo-West Pacific (IWP) followed by dispersal toward the periphery. This pattern can be explained by: (a) high dispersal capacity of the species, (b) habitat heterogeneity driving more recent differentiation in the IWP, and (c) ecological-scale processes such as niche incumbency reinforcing patterns of genotype mutual exclusion. The dispersal potential of this species drives the ongoing range expansion into the Mediterranean Sea, indicating that A. lobifera is able to expand its distribution by tracking increases in temperature. The genetic structure reveals recent diversification and high rate of extinction in the evolutionary history of the clade suggesting a high turnover rate of the diversity at the cryptic level. This diversification dynamic combined with high dispersal potential, allowed the species to maintain a widespread distribution over periods of geological and climatic upheaval. These characteristics are likely to allow the species to modify its geographic range in response to ongoing global warming without requiring genetic differentiation.

Putative sponge biomarkers in unicellular Rhizaria question an early rise of animals.

The dawn of animals remains one of the most mysterious milestones in the evolution of life. The fossil lipids 24-isopropylcholestane and 26-methylstigmastane are considered diagnostic for demosponges-arguably the oldest group of living animals. The widespread occurrence and high relative abundance of these biomarkers in Ediacaran sediments from 635-541 million years (Myr) ago have been viewed as evidence for the rise of animals to ecological importance approximately 100 Myr before their rapid Cambrian radiation. Here we show that the biosynthesis of 24-isopropylcholestane and 26-methylstigmastane precursors is common among early-branching unicellular Rhizaria-heterotrophic protists that play an important role in trophic cycling and carbon export in the modern ocean. Negating these hydrocarbons as sponge biomarkers, our study places the oldest evidence for animals closer to the Cambrian Explosion. Cambrian silica hexactine spicules that are approximately 535 Myr old now represent the oldest diagnostic sponge remains, whereas approximately 558-Myr-old Dickinsonia and Kimberella (Ediacara biota) provide the most reliable evidence for the emergence of animals. The proliferation of predatory protists may have been responsible for much of the ecological changes during the late Neoproterozoic, including the rise of algae, the establishment of complex trophic relationships and the oxygenation of shallow-water habitats required for the subsequent ascent of macroscopic animals.

Disentangling thermal stress responses in a reef-calcifier and its photosymbionts by shotgun proteomics.

The proliferation of key marine ecological engineers and carbonate producers often relies on their association with photosymbiotic algae. Evaluating stress responses of these organisms is important to predict their fate under future climate projections. Physiological approaches are limited in their ability to resolve the involved molecular mechanisms and attribute stress effects to the host or symbiont, while probing and partitioning of proteins cannot be applied in organisms where the host and symbiont are small and cannot be physically separated. Here we apply a label-free quantitative proteomics approach to detect changes of proteome composition in the diatom-bearing benthic foraminifera Amphistegina gibbosa experimentally exposed to three thermal-stress scenarios. We developed a workflow for protein extraction from less than ten specimens and simultaneously analysed host and symbiont proteomes. Despite little genomic data for the host, 1,618 proteins could be partially assembled and assigned. The proteomes revealed identical pattern of stress response among stress scenarios as that indicated by physiological measurements, but allowed identification of compartment-specific stress reactions. In the symbiont, stress-response and proteolysis-related proteins were up regulated while photosynthesis-related proteins declined. In contrast, host homeostasis was maintained through chaperone up-regulation associated with elevated proteosynthesis and proteolysis, and the host metabolism shifted to heterotrophy.

Reef calcifiers are adapted to episodic heat stress but vulnerable to sustained warming.

Shallow marine ecosystems naturally experience fluctuating physicochemical conditions across spatial and temporal scales. Widespread coral-bleaching events, induced by prolonged heat stress, highlight the importance of how the duration and frequency of thermal stress influence the adaptive physiology of photosymbiotic calcifiers. Large benthic foraminifera harboring algal endosymbionts are major tropical carbonate producers and bioindicators of ecosystem health. Like corals, they are sensitive to thermal stress and bleach at temperatures temporarily occurring in their natural habitat and projected to happen more frequently. However, their thermal tolerance has been studied so far only by chronic exposure, so how they respond under more realistic episodic heat-event scenarios remains unknown. Here, we determined the physiological responses of Amphistegina gibbosa, an abundant western Atlantic foraminifera, to four different treatments--control, single, episodic, and chronic exposure to the same thermal stress (32°C)--in controlled laboratory cultures. Exposure to chronic thermal stress reduced motility and growth, while antioxidant capacity was elevated, and photosymbiont variables (coloration, oxygen-production rates, chlorophyll a concentration) indicated extensive bleaching. In contrast, single- and episodic-stress treatments were associated with higher motility and growth, while photosymbiont variables remained stable. The effects of single and episodic heat events were similar, except for the presumable occurrence of reproduction, which seemed to be suppressed by both episodic and chronic stress. The otherwise different responses between treatments with thermal fluctuations and chronic stress indicate adaptation to thermal peaks, but not to chronic exposure expected to ensue when baseline temperatures are elevated by climate change. This firstly implies that marine habitats with a history of fluctuating thermal stress potentially support resilient physiological mechanisms among photosymbiotic organisms. Secondly, there seem to be temporal constraints related to heat events among coral reef environments and reinforces the importance of temporal fluctuations in stress exposure in global-change studies and projections.

DISMS2: A flexible algorithm for direct proteome- wide distance calculation of LC-MS/MS runs.

BACKGROUND: The classification of samples on a molecular level has manifold applications, from patient classification regarding cancer treatment to phylogenetics for identifying evolutionary relationships between species. Modern methods employ the alignment of DNA or amino acid sequences, mostly not genome-wide but only on selected parts of the genome. Recently proteomics-based approaches have become popular. An established method for the identification of peptides and proteins is liquid chromatography-tandem mass spectrometry (LC-MS/MS). First, protein sequences from MS/MS spectra are identified by means of database searches, given samples with known genome-wide sequence information, then sequence based methods are applied. Alternatively, de novo peptide sequencing algorithms annotate MS/MS spectra and deduce peptide/protein information without a database. A newer approach independent of additional information is to directly compare unidentified tandem mass spectra. The challenge then is to compute the distance between pairwise MS/MS runs consisting of thousands of spectra. METHODS: We present DISMS2, a new algorithm to calculate proteome-wide distances directly from MS/MS data, extending the algorithm compareMS2, an approach that also uses a spectral comparison pipeline. RESULTS: Our new more flexible algorithm, DISMS2, allows for the choice of the spectrum distance measure and includes different spectra preprocessing and filtering steps that can be tailored to specific situations by parameter optimization. CONCLUSIONS: DISMS2 performs well for samples from species with and without database annotation and thus has clear advantages over methods that are purely based on database search.