Dalin Shi

Effect of ocean acidification on iron availability to marine phytoplankton.

Ironed Out In large regions of the ocean, low levels of the essential nutrient, iron, limits primary productivity. Irons chemistry and bioavailability are highly dependent on pH. Rising concentrations of atmospheric CO2 is leading to the acidification of the ocean. Shi et al. (p. 676, published online 14 January; see the Perspective by Sunda) show that the bioavailable fraction of iron dissolved in the ocean may decline as a result of the decrease in ocean pH, which affects the rate of iron uptake by diatoms and coccolithophores. Unless iron input to the oceans increases, these changes may lead to an increase in the iron stress of phytoplankton. Ocean acidification caused by anthropogenic carbon dioxide is changing the chemistry and bioavailability of iron in seawater. The acidification caused by the dissolution of anthropogenic carbon dioxide (CO2) in the ocean changes the chemistry and hence the bioavailability of iron (Fe), a limiting nutrient in large oceanic regions. Here, we show that the bioavailability of dissolved Fe may decline because of ocean acidification. Acidification of media containing various Fe compounds decreases the Fe uptake rate of diatoms and coccolithophores to an extent predicted by the changes in Fe chemistry. A slower Fe uptake by a model diatom with decreasing pH is also seen in experiments with Atlantic surface water. The Fe requirement of model phytoplankton remains unchanged with increasing CO2. The ongoing acidification of seawater is likely to increase the Fe stress of phytoplankton populations in some areas of the ocean.

Ocean acidification slows nitrogen fixation and growth in the dominant diazotroph Trichodesmium under low-iron conditions

Dissolution of anthropogenic CO2 increases the partial pressure of CO2 (pCO2) and decreases the pH of seawater. The rate of Fe uptake by the dominant N2-fixing cyanobacterium Trichodesmium declines as pH decreases in metal-buffered medium. The slower Fe-uptake rate at low pH results from changes in Fe chemistry and not from a physiological response of the organism. Contrary to previous observations in nutrient-replete media, increasing pCO2/decreasing pH causes a decrease in the rates of N2 fixation and growth in Trichodesmium under low-Fe conditions. This result was obtained even though the bioavailability of Fe was maintained at a constant level by increasing the total Fe concentration at low pH. Short-term experiments in which pCO2 and pH were varied independently showed that the decrease in N2 fixation is caused by decreasing pH rather than by increasing pCO2 and corresponds to a lower efficiency of the nitrogenase enzyme. To compensate partially for the loss of N2 fixation efficiency at low pH, Trichodesmium synthesizes additional nitrogenase. This increase comes partly at the cost of down-regulation of Fe-containing photosynthetic proteins. Our results show that although increasing pCO2 often is beneficial to photosynthetic marine organisms, the concurrent decreasing pH can affect primary producers negatively. Such negative effects can occur both through chemical mechanisms, such as the bioavailability of key nutrients like Fe, and through biological mechanisms, as shown by the decrease in N2 fixation in Fe-limited Trichodesmium.

Mechanisms of hexabromocyclododecanes induced developmental toxicity in marine medaka (Oryzias melastigma) embryos

Hexabromocyclododecanes (HBCDs) are widely used as additive brominated flame retardants, and are now ubiquitous contaminants in the environmental media and biota, including the marine environment and marine organisms. However, the impacts of HBCDs on marine fish are not well known. In this study the embryos of marine medaka (Oryzias melastigma) were used to assess the developmental toxicity of HBCDs. Freshly fertilized marine medaka embryos were exposed to various concentrations of technical HBCD (tHBCD, 0, 5, 20 and 50μg/L) until the first fry stage, and hatch success, morphology and cardiac function were examined. In all the exposure groups (5, 20 and 50μg/L) tHBCD significantly increased the embryo heart beats. The measurement of sinus venosus-bulbus arteriosus (SV-BA) distance indicated that tHBCD significantly enlarged the SV-BA distance at exposure concentrations of 20 and 50μg/L. The malformation rate at the first fry stage was also induced by tHBCD in a dose dependent manner, with the formation of pericardial edema and yolk sac edema as the most frequently observed malformation. In addition, the concentrations of total HBCD isomers (ΣHBCDs) in embryos in the current study were comparative with environmental levels and increased with increasing exposure duration. Furthermore, exposure to tHBCD also induced the level of 8-oxodG, a representative oxidative DNA damage. The mechanisms of HBCD-induced developmental toxicity were further explored by TUNEL assay, gel-based quantitative proteomic approach and measurement of the expression of several stress responsive genes, such as p53, TNF-α, IL-1β, CYP1A, COX-1 and COX-2, together with the activities of caspases. The results suggested that HBCDs exposure at environmentally realistic concentrations induced oxidative stress and apoptosis, and suppressed nucleotide and protein synthesis, which all together resulted in developmental toxicity, particularly in the cardiovascular system, in the embryos of O. melastigma.

The complex effects of ocean acidification on the prominent N2-fixing cyanobacterium Trichodesmium

A future, more acidic ocean could be less productive, despite the fertilizing effects of elevated CO2. Reconciling pH and future productivity The differential effects of reduced seawater pH and increased carbon dioxide on marine phytoplankton productivity have not been resolved. Hong et al. found that previous experimentation did not account for variable metal concentrations or for ammonia contamination. After controlling for these variables, experimentation, protein expression analysis, and field data showed that low pH, coupled with the low ambient iron availability in the open ocean, inhibits nitrogen fixation, whereas elevated CO2 is fertilizing. Overall, the deleterious effects of decreased pH trump the beneficial effects of increased CO2. Thus, it seems that in a future, more acidic ocean, phytoplankton productivity is likely to be suppressed. Science, this issue p. 527 Acidification of seawater caused by anthropogenic carbon dioxide (CO2) is anticipated to influence the growth of dinitrogen (N2)–fixing phytoplankton, which contribute a large fraction of primary production in the tropical and subtropical ocean. We found that growth and N2-fixation of the ubiquitous cyanobacterium Trichodesmium decreased under acidified conditions, notwithstanding a beneficial effect of high CO2. Acidification resulted in low cytosolic pH and reduced N2-fixation rates despite elevated nitrogenase concentrations. Low cytosolic pH required increased proton pumping across the thylakoid membrane and elevated adenosine triphosphate production. These requirements were not satisfied under field or experimental iron-limiting conditions, which greatly amplified the negative effect of acidification.

Developmental toxicity of three hexabromocyclododecane diastereoisomers in embryos of the marine medaka Oryzias melastigma.

The composition of major hexabromocyclododecane (HBCD) diastereoisomers, i.e. α-, β-, and γ-HBCDs, in marine biota is different from that of the commercially available form (technical HBCD), which is used extensively for toxicological studies. To properly evaluate the impact of HBCDs, the embryos of Oryzias melastigma were used to examine the developmental toxicity of the individual diastereoisomers. Results showed that HBCD diastereoisomers at the environmentally realistic concentrations in the embryos induced malformation rate and heartbeat, and caused the appearance of apoptotic heart. In addition, α-, β-, and γ-HBCDs had similar potency to stimulate the generation of reactive oxygen species, consequently leading to apoptosis in O. melastigma embryos. The order of the developmental toxicity of α-, β-, and γ-HBCDs in O. melastigma embryos was different from that in zebrafish embryos studied previously, which highlighted the importance of using species from both fresh and salt water for toxicity assessment.

Toxicity and bioaccumulation of three hexabromocyclododecane diastereoisomers in the marine copepod Tigriopus japonicas

The three major hexabromocyclododecane (HBCD) diastereoisomers, i.e. α-, β- and γ-HBCD, have distinct physical and chemical properties that may potentially result in different levels of bioaccumulation and toxicity in aquatic organisms. To assess the impact of diastereomeric variation in HBCDs, the marine copepod Tigriopus japonicus was exposed to α-, β- and γ-HBCD in isolation. Results showed that all the three diastereoisomers had a similar potency to cause growth delay in T. japonicas. Variation was observed in the overall survival rate with exposure to α- and β-HBCD, and this resulted in significantly higher lethal toxicity in T. japonicas than that with exposure to γ-HBCD. Exposure to α-, β- and γ-HBCD led to the generation of ROS in T. japonicas, a possibly toxic mechanism. Both α- and β-HBCD showed a higher potential to induce oxidative stress, which may be a factor in the higher lethal toxicity observed with α- and β-HBCD exposure. It is of note that T. japonicus was found to be more sensitive to all three diastereoisomers in the F1 generation than in the F0 generation. The bioconcentration potential of HBCD diastereoisomers can be ranked in the order α-HBCD>γ-HBCD>β-HBCD and was found to be higher in T. japonicus than has been reported for fish species.

Ambient nitrate switches the ammonium consumption pathway in the euphotic ocean

Phytoplankton assimilation and microbial oxidation of ammonium are two critical conversion pathways in the marine nitrogen cycle. The underlying regulatory mechanisms of these two competing processes remain unclear. Here we show that ambient nitrate acts as a key variable to bifurcate ammonium flow through assimilation or oxidation, and the depth of the nitracline represents a robust spatial boundary between ammonium assimilators and oxidizers in the stratified ocean. Profiles of ammonium utilization show that phytoplankton assemblages in nitrate-depleted regimes have higher ammonium affinity than nitrifiers. In nitrate replete conditions, by contrast, phytoplankton reduce their ammonium reliance and thus enhance the success of nitrifiers. This finding helps to explain existing discrepancies in the understanding of light inhibition of surface nitrification in the global ocean, and provides further insights into the spatial linkages between oceanic nitrification and new production.The underlying regulatory mechanisms of phytoplankton assimilation and microbial oxidation of ammonium in the surface ocean are unclear. Here, using isotope labeling experiments, the authors show that ambient nitrate is a key variable bifurcating ammonium flow through assimilation or oxidation.

Multigenerational effects of 4-methylbenzylidene camphor (4-MBC) on the survival, development and reproduction of the marine copepod Tigriopus japonicus

One of the most widely used organic UV filters, 4-methylbenzylidene camphor (4-MBC), is present at high concentrations in offshore waters. The marine copepod Tigriopus japonicus was exposed to different concentrations of 4-MBC (i.e., 0, 0.5, 1, 5 and 10μgL-1) for 4 consecutive generations (F0-F3) to evaluate the impact of 4-MBC on marine ecosystems. The results showed that in the F0 generation, 4-MBC caused significant lethal toxicity in T. japonicas at concentrations of 5 and 10μgL-1 and the nauplii were more sensitive to 4-MBC toxicity than the adults. However in the F1-F3 generations, 4-MBC exposure did not affect the survival rate. The hatching rate and the developmental duration from the nauplii to the copepodite (N-C) and from the nauplii to adult (N-A) decreased significantly in the F1-F2 generations and in the F2-F3 generations, respectively, even at the lowest exposure concentration (0.5μgL-1). In the subsequent two generations (i.e., the F4-F5 generations) of recovery exposure in clean seawater, the growth rates of the original 4-MBC exposure groups were still faster than the control in both the N-C and N-A stages, suggesting possible transgenerational genetic and/or epigenetic changes upon chronic 4-MBC exposure. The expression of the ecdysone receptor gene was up-regulated by 4-MBC, which was consistent with the decrease of the N-C/N-A duration. In addition, 4-MBC may induce oxidative stress and trigger apoptosis in T. japonicas, resulting in developmental, reproductive and even lethal toxicity. A preliminary risk assessment suggested that under environmentally realistic concentrations, 4-MBC had significant potential to pose a threat to marine crustaceans and marine ecosystems.

Nitrogen fixation in two coastal upwelling regions of the Taiwan Strait

Recent studies have demonstrated that dinitrogen fixation can be important in nutrient-rich coastal upwelling regions. During a cruise to the Taiwan Strait in summer 2015, we found that the nitrogen fixation rate in surface waters ranged from below detection limits to 7.51 nmol N L−1 d−1. Higher rates accompanied by low N:P ratios (1–10.4:1) associated with low temperatures occurred in the surface water where the Pingtan and the Dongshan upwelling regions met (the NE area). In contrast, insignificant rates were observed in the southwest area of the Dongshan upwelling region (the SW area) with sufficient N and deficient P, and therefore high N:P ratios (e.g., >43 at station C2) due largely to the influence of the Pearl River plume. Diatom-associated symbionts (het-1; 104–106 copies L−1) that are efficient in organic matter export were found to dominate the other diazotrophic groups that were surveyed, which may represent a direct relationship between new nitrogen input and export in the upwelling regions. Our results suggest a hydrographical influence on the diazotroph community and N2 fixation in coastal upwelling regions.

Response to Comment on “The complex effects of ocean acidification on the prominent N2-fixing cyanobacterium Trichodesmium”

Hutchins et al. question the validity of our results showing that under fast growth conditions, the beneficial effect of high CO2 on Trichodesmium is overwhelmed by the deleterious effect of the concomitant decrease in ambient and cellular pH. The positive effect of acidification reported by Hutchins and co-workers is likely caused by culture conditions that support suboptimal growth rates.