Nutritional response of a coccolithophore to changing pH and temperature

Unidad de excelencia María de Maeztu CEX2019-000940-MAcord transformatiu CRUE-CSICCoccolithophores are a calcifying unicellular phytoplankton group that are at the base of the marine food web, and their lipid content provides a source of energy to consumers. Coccolithophores are vulnerable to ocean acidification and warming, therefore it is critical to establish the effects of climate change on these significant marine primary producers, and determine potential consequences that these changes can have on their consumers. Here, we quantified the impact of changes in pH and temperature on the nutritional condition (lipid content, particulate organic carbon/nitrogen), growth rate, and morphology of the most abundant living coccolithophore species, Emiliania huxleyi. We used a regression type approach with nine pH levels (ranging from 7.66 to 8.44) and two temperatures (15°C and 20°C). Lipid production was greater under reduced pH, and growth rates were distinctly lower at 15°C than at 20°C. The production potential of lipids, which estimates the availability of lipids to consumers, increased under 20°C, but decreased under low pH. The results indicate that, while consumers will benefit energetically under ocean warming, this benefit will be mitigated by ocean acidification. The carbon to nitrogen ratio was higher at 20°C and low pH, indicating that the nutritional quality of coccolithophores for consumers will decline under climate change. The impact of low pH on the structural integrity of the coccosphere may also mean that coccolithophores are easier to digest for consumers. Many responses suggest cellular stress, indicating that increases in temperature and reductions in pH may have a negative impact on the ecophysiology of coccolithophores

The Zooxanthellate Jellyfish Holobiont Cassiopea andromeda, a Source of Soluble Bioactive Compounds

Cassiopea andromeda (Forsskål, 1775), commonly found across the Indo-Pacific Ocean, the Red Sea, and now also in the warmest areas of the Mediterranean Sea, is a scyphozoan jellyfish that hosts autotrophic dinoflagellate symbionts (family Symbiodiniaceae). Besides supplying photosynthates to their host, these microalgae are known to produce bioactive compounds as long- chain unsaturated fay acids, polyphenols, and pigments, including carotenoids, with antioxidant properties and other beneficial biological activities. By the present study, a fractionation method was applied on the hydroalcoholic extract from two main body parts (oral arms and umbrella) of the jellyfish holobiont to obtain an improved biochemical characterization of the obtained fractions from the two body parts. The composition of each fraction (i.e., proteins, phenols, fay acids, and pigments) as well as the associated antioxidant activity were analyzed. The oral arms proved richer in zooxanthellae and pigments than the umbrella. The applied fractionation method was effective in separating pigments and fay acids into a lipophilic fraction from proteins and pigment–protein complexes. Therefore, the C. andromeda–dinoflagellate holobiont might be considered as a promising natural source of multiple bioactive compounds produced through mixotrophic metabolism, which are of interest for a wide range of biotechnological applications

Understanding Cassiopea andromeda (Scyphozoa) Invasiveness in Different Habitats: A Multiple Biomarker Comparison

A dual nutrition mode (i.e., mixotrophy) can be advantageous for alien species in a new environment. In Ceara (Brazil), the symbiotic jellyfish Cassiopea andromeda is rapidly spreading under diverse environmental conditions across natural and human-altered coastal habitats, such as mangroves and shrimp farms. Here we report on the trophic ecology of the alien upside-down jellyfish sampled in these two contrasting coastal habitats during the dry (July-October) and rainy (January-April) seasons, investigated by means of organic biomarkers (lipids, carbohydrates) and bulk tissue stable isotope (& delta;N-15 and & delta;C-13) analyses. Total lipid content of jellyfish gonads was generally higher in shrimp farms, whereas no significant difference in carbohydrate concentration was found in jellyfish tissues from the two different habitats. Similarly, there were no significant differences in the & delta;N-15 values of jellyfish tissues from the two contrasting habitats, whereas the & delta;C-13 values were higher in jellyfish from shrimp farms. Overall, the higher carbon-enriched value in aquaculture ponds supports the hypothesis of differences of available food sources compared to the natural mangrove habitats, where food availability exhibits a stronger seasonality. In fact, aquaculture ponds are characterized by human-driven regular food supply, leading to more stable trophic conditions and to enhanced growth, lipid production, and gonadal output of C. andromeda jellyfish. This investigation may contribute to predicting how Cassiopea mixotrophy may contribute to explaining its differential success in different habitats

Brooding strategy of the Arctic cold seep polychaete Oligobrachia haakonmosbiensis

International audienceThe Arctic polychaete, Oligobrachia haakonmosbiensis (Family Siboglinidae) is the most abundant symbiotic species inhabiting the Haakon Mosby Mud Volcano (Norwegian Sea, depth 1250 m). Different aspects of gametogenesis, fecundity, embryogenesis and larval development were studied using biometric measurements, classical histology and scanning electron microscopy on specimens (n = 15) collected in July 2009 at two sites (72°00.28'N, 14°43.36'E; 72°00.33'N, 14°43.22'E). Several cohorts of oocytes, from oogonia to mature oocytes were observed in brooding females. Embryos with 16-64 cell divisions, trochophore and metatrochophore larvae, were found, in sequence, in female tubes, from just above the tentacles to the anterior end of the tube. Trochophores had both a prototroch and a telotroch; metatrochophores had an additional ciliary band, the neurotroch, but lacked a downstream feeding system. All of female reproductive stages, oocytes, embryos and larvae, were recovered in a single specimen suggesting the release of different batches of oocytes at least on the date of collection, which coincided with the boreal summer. Only one brooding female contained exclusively germ cells in the gonad suggesting a pause in reproduction. Fecundity was low: a maximum of 60 mature oocytes per female was counted, and if all the different stages of oocytes, embryos and larvae were combined, a total fecundity of ~250-300 propagules was found in each female. This study advances knowledge of the reproductive biology of O. haakonmosbiensis and has particular significance for understanding the distribution of this ecologically important deep-sea chemosymbiotic species in the Arctic region. The new data on life-history traits are critical for modeling, and predicting dispersal potential and connectivity among cold seeps in the Arctic, which is an essential component of marine spatial management

Seawater carbonate chemistry and lipid content, particulate organic carbon/nitrogen, growth rate, and morphology of Emiliania huxleyi

Coccolithophores are a calcifying unicellular phytoplankton group that are at the base of the marine food web, and their lipid content provides a source of energy to consumers. Coccolithophores are vulnerable to ocean acidification and warming, therefore it is critical to establish the effects of climate change on these significant marine primary producers, and determine potential consequences that these changes can have on their consumers. Here, we quantified the impact of changes in pH and temperature on the nutritional condition (lipid content, particulate organic carbon/nitrogen), growth rate, and morphology of the most abundant living coccolithophore species, Emiliania huxleyi. We used a regression type approach with nine pH levels (ranging from 7.66 to 8.44) and two temperatures (15°C and 20°C). Lipid production was greater under reduced pH, and growth rates were distinctly lower at 15°C than at 20°C. The production potential of lipids, which estimates the availability of lipids to consumers, increased under 20°C, but decreased under low pH. The results indicate that, while consumers will benefit energetically under ocean warming, this benefit will be mitigated by ocean acidification. The carbon to nitrogen ratio was higher at 20°C and low pH, indicating that the nutritional quality of coccolithophores for consumers will decline under climate change. The impact of low pH on the structural integrity of the coccosphere may also mean that coccolithophores are easier to digest for consumers. Many responses suggest cellular stress, indicating that increases in temperature and reductions in pH may have a negative impact on the ecophysiology of coccolithophores

High photosynthetic plasticity may reinforce invasiveness of upside-down zooxanthellate jellyfish in Mediterranean coastal waters

Ecological profiling of non-native species is essential to predict their dispersal and invasiveness potential across different areas of the world. Cassiopea is a monophyletic taxonomic group of scyphozoan mixotrophic jellyfish including C. andromeda, a recent colonizer of sheltered, shallow-water habitats of the Mediterranean Sea, such as harbors and other light-limited, eutrophic coastal habitats. To assess the ecophysiological plasticity of Cassiopea jellyfish and their potential to spread across the Mare Nostrum by secondary introductions, we investigated rapid photosynthetic responses of jellyfish to irradiance transitions-from reduced to increased irradiance conditions (as paradigm of transition from harbors to coastal, meso/oligotrophic habitats). Laboratory incubation experiments were carried out to compare oxygen fluxes and photobiological variables in Cassiopea sp. immature specimens pre-acclimated to low irradiance (PAR = 200 mumol photons m-2 s-1) and specimens rapidly exposed to higher irradiance levels (PAR = 500 mumol photons m-2 s-1). Comparable photosynthetic potential and high photosynthetic rates were measured at both irradiance values, as also shown by the rapid light curves. No significant differences were observed in terms of symbiont abundance between control and treated specimens. However, jellyfish kept at the low irradiance showed a higher content in chlorophyll a and c (0.76±0.51SD vs 0.46±0.13SD mg g-1 AFDW) and a higher Ci (amount of chlorophyll per cell) compared to jellyfish exposed to higher irradiance levels. The ratio between gross photosynthesis and respiration (P:R) was >1, indicating a significant input from the autotrophic metabolism. Cassiopea sp. specimens showed high photosynthetic performances, at both low and high irradiance, demonstrating high potential to adapt to sudden changes in light exposure. Such photosynthetic plasticity, combined with Cassiopea eurythermal tolerance and mixotrophic behavior, jointly suggest the upside-down jellyfish as a potentially successful invader in the scenario of a warming Mediterranean Sea

High photosynthetic plasticity may reinforce invasiveness of upside-down zooxanthellate jellyfish in Mediterranean coastal waters.

Ecological profiling of non-native species is essential to predict their dispersal and invasiveness potential across different areas of the world. Cassiopea is a monophyletic taxonomic group of scyphozoan mixotrophic jellyfish including C. andromeda, a recent colonizer of sheltered, shallow-water habitats of the Mediterranean Sea, such as harbors and other light-limited, eutrophic coastal habitats. To assess the ecophysiological plasticity of Cassiopea jellyfish and their potential to spread across the Mare Nostrum by secondary introductions, we investigated rapid photosynthetic responses of jellyfish to irradiance transitions-from reduced to increased irradiance conditions (as paradigm of transition from harbors to coastal, meso/oligotrophic habitats). Laboratory incubation experiments were carried out to compare oxygen fluxes and photobiological variables in Cassiopea sp. immature specimens pre-acclimated to low irradiance (PAR = 200 μmol photons m-2 s-1) and specimens rapidly exposed to higher irradiance levels (PAR = 500 μmol photons m-2 s-1). Comparable photosynthetic potential and high photosynthetic rates were measured at both irradiance values, as also shown by the rapid light curves. No significant differences were observed in terms of symbiont abundance between control and treated specimens. However, jellyfish kept at the low irradiance showed a higher content in chlorophyll a and c (0.76±0.51SD vs 0.46±0.13SD mg g-1 AFDW) and a higher Ci (amount of chlorophyll per cell) compared to jellyfish exposed to higher irradiance levels. The ratio between gross photosynthesis and respiration (P:R) was >1, indicating a significant input from the autotrophic metabolism. Cassiopea sp. specimens showed high photosynthetic performances, at both low and high irradiance, demonstrating high potential to adapt to sudden changes in light exposure. Such photosynthetic plasticity, combined with Cassiopea eurythermal tolerance and mixotrophic behavior, jointly suggest the upside-down jellyfish as a potentially successful invader in the scenario of a warming Mediterranean Sea

Host–symbiont plasticity in the upside-down jellyfish Cassiopea xamachana: strobilation across symbiont genera

IntroductionIn the upside-down jellyfish, Cassiopea xamachana (Cnidaria: Scyphozoa), the establishment of photosymbiosis with dinoflagellates (family Symbiodiniaceae) is necessary for the sessile polyp to undergo metamorphosis (strobilation) into a free-swimming adult. C. xamachana has the capacity to associate with a wide variety of dinoflagellate species and representatives of divergent genera. While some studies have looked at the successful induction of symbiosis, none to date have examined the lasting effect of diverse symbiont taxa on host survivorship and development, which is needed to assess the fitness costs of such symbioses.MethodsOur study exposes C. xamachana polyps to 22 different cultured Symbiodinaceae strains representing 13 species from 5 genera. We analyzed the time to strobilation, the number of ephyra (juvenile medusa) produced, and the proportion of ephyra that died prematurely.ResultsHere we show that C. xamachana strobilation can be induced by nearly each symbiodinacean strain we tested, with the exception of free-living species (i.e., unknown to establish symbiosis with any other marine host). Additionally, ephyrae did not display morphological variation or survivorship differences with varying symbionts. However, we observed intraspecific variation in time to induce strobilation with different cultured dinoflagellate strains.DiscussionThis work expands the known symbiont species that can form stable mutualisms with C. xamachana, primarily in the genera Symbiodinium and Breviolum. Additionally, we provide evidence of differences in ability of cultured symbiodiniaceans to establish symbiosis with a host, which suggests population-level differences in dinoflagellate cultures impact their symbiosis success. By utilizing an animal like C. xamachana with flexible symbiont uptake, we are able to explore how symbiont diversity can influence the timing and success of symbiosis-driven development

Reproductive cycle and gonadal output of the Lessepsian jellyfish Cassiopea andromeda in NW Sicily (Central Mediterranean Sea).

Knowledge of the reproductive strategy is a key prerequisite to predict population dynamics and potential invasiveness of both native and non-indigenous outbreak-forming species. In 2014 the Lessepsian upside-down jellyfish Cassiopea andromeda reached the harbor of Palermo (NW Sicily, Thyrrenian Sea), to date its established westernmost outpost in the Mediterranean Sea. To predict C. andromeda reproductive success in its novel habitat, gonad histology was carried out to record the number and size of mature and immature oocytes. Both male and female simultaneously presented gametes at all stages of development suggesting an asynchronous, yet apparently continuous, reproduction strategy. Indeed, oogenesis was observed throughout the year from pre-vitellogenic, vitellogenetic, and late-vitellogenetic to mature oocytes suggesting multiple reproductive events, as known in other Mediterranean Rhizostomeae. Oocytes were found from May to December, with two seasonal peaks of abundance (late spring = 392 and autumn = 272), suggesting imminent spawning events. Further, jellyfish size varied significantly throughout the year, with maximum diameter (up to 24 cm) in summer, and minimum diameter (6 cm) in winter. Small-sized jellyfish in winter belong to the new cohort, most probably arising from intense summer strobilation of polyps. Late spring fertilization, planula development, and metamorphosis, followed by polyp strobilation in the summer months, may explain the late appearance of a new jellyfish cohort, likely coincident with that recorded throughout winter