Uneven response of phytoplankton-bacteria coupling under Saharan dust pulse and ultraviolet radiation in the south-western Mediterranean Sea.

The microbial carbon (C) flux in the ocean is a key functional process governed by the excretion of organic carbon by phytoplankton (EOC) and heterotrophic bacterial carbon demand (BCD). Ultraviolet radiation (UVR) levels in upper mixed layers and increasing atmospheric dust deposition from arid regions may alter the degree of coupling in the phytoplankton-bacteria relationship (measured as BCD:EOC ratio) with consequences for the C-flux through these compartments in marine oligotrophic ecosystem. Firstly, we performed a field study across the south-western (SW) Mediterranean Sea to assess the degree of coupling (BCD:EOC) and how it may be related to metabolic balance (total primary production: community respiration; PPT:CR). Secondly, we conducted a microcosm experiment in two contrasting areas (heterotrophic nearshore and autotrophic open sea) to test the impact of UVR and dust interaction on microbial C flux. In the field study, we found that BCD was not satisfied by EOC (i.e., BCD:EOC >1; uncoupled phytoplankton-bacteria relationship). BCD:EOC ratio was negatively related to PPT:CR ratio across the SW Mediterranean Sea. A spatial pattern emerged, i.e. in autotrophic open sea stations uncoupling was less severe (BCD:EOC ranged 1-2), whereas heterotrophic nearshore stations uncoupling was more severe (BCD:EOC > 2). In the experimental study, in the seawater both enriched with dust and under UVR, BCD:EOC ratio decreased by stimulating autotrophic processes (particulate primary production (PPP) and EOC) in the heterotrophic nearshore area, whereas BCD:EOC increased by stimulating heterotrophic processes [heterotrophic bacterial production (HBP), bacterial growth efficiency (BGE), bacterial respiration (BR)] in the autotrophic open sea. Our results show that this spatial pattern could be reversed under future UVR × Dust scenario. Overall, the impact of greater dust deposition and higher UVR levels will alter the phytoplankton-bacteria C-flux with consequences for the productivity of both communities, their standing stocks, and ultimately, the ecosystem's metabolic balance at the sea surface.

Inclusion of ionizing radiation in a mathematical model for photosynthesis.

Ionizing radiation of astrophysical origin might have played an important role in biological evolution during the long course of Earth's evolution. Several phenomena might have induced intense fluctuations in background ionizing radiation, such as highly energetic stellar explosions. There might also be anthropogenic causes for environmental radiation fluctuations, resulting from nuclear industry activities. The inclusion of these effects in a mathematical model for photosynthesis provides a useful tool to account for the damages of the above-mentioned phenomena in vegetal life. Mathematical models for photosynthesis typically only consider ultraviolet radiation and photosynthetically active radiation, as they have been a ubiquitous physical factor in the settlement of vegetal life. In this work a mathematical model for aquatic photosynthesis is modified, from first principles, to include the action of particulate ionizing radiation on the photosynthetic process. After assuming an ansatz allowing to separate damage/repair kinetics of ultraviolet and ionizing radiations, a treatable mathematical expression of the model is obtained. This generalized model is presented as a function of radiometric and photometric magnitudes, making it prone to calibration and useful to apply to aquatic ecosystems under radiational stress due to gamma-ray bursts, cosmic ray bursts, solar storms, or other sources of ionizing radiations.

Morphological bases of phytoplankton energy management and physiological responses unveiled by 3D subcellular imaging.

Eukaryotic phytoplankton have a small global biomass but play major roles in primary production and climate. Despite improved understanding of phytoplankton diversity and evolution, we largely ignore the cellular bases of their environmental plasticity. By comparative 3D morphometric analysis across seven distant phytoplankton taxa, we observe constant volume occupancy by the main organelles and preserved volumetric ratios between plastids and mitochondria. We hypothesise that phytoplankton subcellular topology is modulated by energy-management constraints. Consistent with this, shifting the diatom Phaeodactylum from low to high light enhances photosynthesis and respiration, increases cell-volume occupancy by mitochondria and the plastid CO2-fixing pyrenoid, and boosts plastid-mitochondria contacts. Changes in organelle architectures and interactions also accompany Nannochloropsis acclimation to different trophic lifestyles, along with respiratory and photosynthetic responses. By revealing evolutionarily-conserved topologies of energy-managing organelles, and their role in phytoplankton acclimation, this work deciphers phytoplankton responses at subcellular scales.

Accumulation of ambient phosphate into the periplasm of marine bacteria is proton motive force dependent.

Bacteria acquire phosphate (Pi) by maintaining a periplasmic concentration below environmental levels. We recently described an extracellular Pi buffer which appears to counteract the gradient required for Pi diffusion. Here, we demonstrate that various treatments to outer membrane (OM) constituents do not affect the buffered Pi because bacteria accumulate Pi in the periplasm, from which it can be removed hypo-osmotically. The periplasmic Pi can be gradually imported into the cytoplasm by ATP-powered transport, however, the proton motive force (PMF) is not required to keep Pi in the periplasm. In contrast, the accumulation of Pi into the periplasm across the OM is PMF-dependent and can be enhanced by light energy. Because the conventional mechanism of Pi-specific transport cannot explain Pi accumulation in the periplasm we propose that periplasmic Pi anions pair with chemiosmotic cations of the PMF and millions of accumulated Pi pairs could influence the periplasmic osmolarity of marine bacteria.

Uncoupled phytoplankton-bacterioplankton relationship by multiple drivers interacting at different temporal scales in a high-mountain Mediterranean lake.

Global-change stressors act under different timing, implying complexity and uncertainty in the study of interactive effects of multiple factors on planktonic communities. We manipulated three types of stressors acting in different time frames in an in situ experiment: ultraviolet radiation (UVR); phosphorus (P) concentration; temperature (T) in an oligotrophic Mediterranean high-mountain lake. The aim was to examine how the sensitivity of phytoplankton and bacterioplankton to UVR and their trophic relationship change under nutrient acclimation and abrupt temperature shifts. Phytoplankton and bacteria showed a common pattern of metabolic response to UVR × P addition interaction, with an increase in their production rates, although evidencing an inhibitory UVR effect on primary production (PP) but stimulatory on bacterial production (HBP). An abrupt T shift in plankton acclimated to UVR and P addition decreased the values of PP, evidencing an inhibitory UVR effect, whereas warming increased HBP and eliminated the UVR effect. The weakening of commensalistic and predatory relationship between phyto- and bacterioplankton under all experimental conditions denotes the negative effects of present and future global-change conditions on planktonic food webs towards impairing C flux within the microbial loop.

Rapid Colonization of Uranium Mining-Impacted Waters, the Biodiversity of Successful Lineages of Phytoplankton Extremophiles.

Anthropogenic extreme environments are emphasized as interesting sites for the study of evolutionary pathways, biodiversity, and extremophile bioprospection. Organisms that grow under these conditions are usually regarded as extremophiles; however, the extreme novelty of these environments may have favor adaptive radiations of facultative extremophiles. At the Iberian Peninsula, uranium mining operations have rendered highly polluted extreme environments in multiple locations. In this study, we examined the phytoplankton diversity, community structure, and possible determining factors in separate uranium mining-impacted waters. Some of these human-induced extreme environments may be able to sustain indigenous facultative extremophile phytoplankton species, as well as alleged obligate extremophiles. Therefore, we investigated the adaptation capacity of three laboratory strains, two Chlamydomonas reinhardtii and a Dictyosphaerium chlorelloides, to uranium-polluted waters. The biodiversity among the sampled waters was very low, and despite presenting unique taxonomic records, ecological patterns can be identified. The microalgae adaptation experiments indicated a gradient of ecological novelty and different phenomena of adaptation, from acclimation in some waters to non-adaptation in the harshest anthropogenic environment. Certainly, phytoplankton extremophiles might have been often overlooked, and the ability to flourish in extreme environments might be a functional feature in some neutrophilic species. Evolutionary biology and microbial biodiversity can benefit the study of recently evolved systems such as uranium-polluted waters. Moreover, anthropogenic extremophiles can be harnessed for industrial applications.

Direct Effects of Temperature on Growth of Different Tropical Phytoplankton Species.

Temperature increase may influence competition among phytoplankton species, potentially intensifying cyanobacteria blooms that can be favored by direct and indirect effects of temperature. In this study, we aimed to clarify how cyanobacteria can be favored by the direct effects of increased temperature compared to diatoms and chlorophytes. Strains of the most representative species of a eutrophic coastal lagoon (Microcystis aeruginosa, Planktothrix agardhii, Desmodesmus communis, and Cyclotella meneghiniana) were used to test the hypothesis that cyanobacteria would be favored by the direct effect of temperature increase. First, we evaluated the effect of temperature increase on growth in monocultures (batch and chemostats) at 25 and 30 °C and after in mixed cultures (chemostats). In batch monocultures, the cyanobacteria showed higher growth rates in 30 °C than in 25 °C. However, in continuous culture experiments (chemostats), growth rates of M. aeruginosa and P. agardhii were not affected by temperature, but the strains showed higher biovolume in steady-state with the temperature increase. In continuous mixed cultures, M. aeruginosa was always dominant and C. meneghiniana was excluded, regardless of temperature tested. D. communis was able to coexist with lower biomass. This study shows that rising temperatures can be detrimental to diatoms, even for a tropical strain. Although some studies indicate that the dominance of cyanobacteria in warmer climates may be due to the indirect effect of warming that will promote physical conditions in the environment more favorable to cyanobacteria, the outcomes of mixed cultures demonstrate that the direct effect of temperature can also favor the dominance of cyanobacteria.

Incubation in light versus dark affects the vitality of UV-irradiated Tetraselmis suecica differently: A flow cytometric study.

In this study, we used flow cytometry to examine how incubation in dark versus light affects the vitality and viability of UV-irradiated Tetraselmis suecica. High UV doses (300 and 400 mJ/cm2) affected the esterase activity, membrane permeability, and chlorophyll content more when the subsequent incubation took place in light. For non- or low UV dose (100 and 200 mJ/cm2)-treated cells, incubation in light resulted in cell regrowth as compared to incubation in dark. Damaged cells (enzymatically active but with permeable membranes) did not recover when incubated under light or dark conditions. Exposure to light reduces the evaluation time of any given ballast water treatment, as viable cells will be detected at an earlier stage and the vitality is more affected. When evaluating the performance of UV-based ballast water treatment systems (BWTS), these results can be useful for type approval using T. suecica as a test organism in the test regime.

Estimation of Kd(PAR) in inland waters across China in relation to the light absorption of optically active components.

The comprehensive analysis of the relationships between the attenuation of photosynthetic active radiation (Kd(PAR)) and light absorption is an imperative requirement to retrieve Kd(PAR) from remote sensing data for aquatic environments. The spatial distributions of the Kd(PAR) and light absorption of optically active components (aOACs) were routinely estimated in China lakes and reservoirs. Spatial Kd(PAR) was relatively dependent on the inorganic particles (average relative contribution of 57.95%). The aOACs could explain 70-87% of Kd(PAR) variations. A linear model is used to predict Kd(PAR), as a function of light absorption coefficient of phytoplankton (aphy), colored dissolved organic matter (aCDOM), and inorganic particles (aNAP): Kd(PAR) = 0.41 + 0.57 × aCDOM + 0.96 × aNAP + 0.57 × aphy (R2 = 0.87, n = 741, p < 0.001). In the lakes with low TSM concentration and non-eutrophic lakes with high TSM, aCDOM was the most powerful predicting factor on Kd(PAR). In eutrophic lakes with high TSM, aNAP had the most significant impact on Kd(PAR). This study allowed Kd(PAR) to be predicted from aOACs values in the inland waters.

Diel transcriptional response of a California Current plankton microbiome to light, low iron, and enduring viral infection.

Phytoplankton and associated microbial communities provide organic carbon to oceanic food webs and drive ecosystem dynamics. However, capturing those dynamics is challenging. Here, an in situ, semi-Lagrangian, robotic sampler profiled pelagic microbes at 4 h intervals over ~2.6 days in North Pacific high-nutrient, low-chlorophyll waters. We report on the community structure and transcriptional dynamics of microbes in an operationally large size class (>5 µm) predominantly populated by dinoflagellates, ciliates, haptophytes, pelagophytes, diatoms, cyanobacteria (chiefly Synechococcus), prasinophytes (chiefly Ostreococcus), fungi, archaea, and proteobacteria. Apart from fungi and archaea, all groups exhibited 24-h periodicity in some transcripts, but larger portions of the transcriptome oscillated in phototrophs. Periodic photosynthesis-related transcripts exhibited a temporal cascade across the morning hours, conserved across diverse phototrophic lineages. Pronounced silica:nitrate drawdown, a high flavodoxin to ferredoxin transcript ratio, and elevated expression of other Fe-stress markers indicated Fe-limitation. Fe-stress markers peaked during a photoperiodically adaptive time window that could modulate phytoplankton response to seasonal Fe-limitation. Remarkably, we observed viruses that infect the majority of abundant taxa, often with total transcriptional activity synchronized with putative hosts. Taken together, these data reveal a microbial plankton community that is shaped by recycled production and tightly controlled by Fe-limitation and viral activity.

Light limitation increases multidimensional trait evenness in phytoplankton populations.

Individual-level variation arising from responses to environmental gradients influences population and community dynamics. How such responses empirically relate to the mechanisms that govern species coexistence is, however, poorly understood. Previous results from l ake phytoplankton communities suggested that the evenness of organismal traits in multiple dimensions increases with resource limitation, possibly due to resource partitioning at the individual level. Here we experimentally tested the emergence of this pattern by growing two phytoplankton species (Pseudokirchneriella subcapitata and Microcystis aeruginosa) under a gradient of light intensity, in monoculture and jointly. Under low light (resource) conditions, the populations diversified into a wide range of phenotypes, which were evenly distributed in multidimensional trait space (defined by four pigment-related trait dimensions), consistent with the observed field pattern. Our interpretation is that under conditions of light limitation, individual phytoplankton cells alter photosynthetic traits to reduce overlap in light acquisition, acquiring unexploited resources and thereby likely maximising individual success. Our results provide prime experimental evidence that resource limitation increases the evenness of conspecific and heterospecific microbial phenotypes along trait axes, advancing our understanding of trait-based coexistence.

Seasonal dependency of controlling factors on the phytoplankton production in Taihu Lake, China.

In this study, 44 profiles of gross primary productivity (GPP) and sunlight, along with water temperature, Chlorophyll-a (Chla) and nutrients, were observed in Meiliang Bay of Taihu Lake, China, in the spring, summer, and fall seasons. Effects of water temperature, light, and nutrient concentration were examined in relation to the GPP-unit-Chla (GPP of algae per Chla). The results showed that the optimum temperature for the GPP of phytoplankton was 27.9°C, the optimal PNA-unit-Chla (photon number absorbed by phytoplankton per Chla) was 0.25 (mol), and the HSCN-unit-Chla and HSCP-unit-Chla (half-saturation constants of nitrogen and phosphorus of algae per Chla) were 0.005 (mg/L) and 0.0004 (mg/L), respectively. The seasonal dependency of the effect of different factors on the GPP was analyzed. Compared with temperature and nutrients, light was found to be the most important factor affecting the GPP during the three seasons. The effect of temperature and nutrients on the GPP of phytoplankton has obvious seasonal change. In spring, temperature was the secondary factor affecting the GPP of phytoplankton, and the effect of nutrients may be negligible in the eutrophic lake on account of temperature limit, which showed that the GPP of algae was only affected by the physical process. In summer and fall, temperature didn't affect the GPP of algae, and the presence of nutrients was the secondary factor affecting the GPP of phytoplankton. From summer to fall, effect of phosphorus was weakened and effect of nitrogen was enhanced.

Daily changes in phytoplankton lipidomes reveal mechanisms of energy storage in the open ocean.

Sunlight is the dominant control on phytoplankton biosynthetic activity, and darkness deprives them of their primary external energy source. Changes in the biochemical composition of phytoplankton communities over diel light cycles and attendant consequences for carbon and energy flux in environments remain poorly elucidated. Here we use lipidomic data from the North Pacific subtropical gyre to show that biosynthesis of energy-rich triacylglycerols (TAGs) by eukaryotic nanophytoplankton during the day and their subsequent consumption at night drives a large and previously uncharacterized daily carbon cycle. Diel oscillations in TAG concentration comprise 23 ± 11% of primary production by eukaryotic nanophytoplankton representing a global flux of about 2.4 Pg C yr-1. Metatranscriptomic analyses of genes required for TAG biosynthesis indicate that haptophytes and dinoflagellates are active members in TAG production. Estimates suggest that these organisms could contain as much as 40% more calories at sunset than at sunrise due to TAG production.

The Response of Three Southern Ocean Phytoplankton Species to Ocean Acidification and Light Availability: A Transcriptomic Study.

Ocean acidification (OA) and high light was found to negatively affect the Antarctic key species Phaeocystis antarctica, Fragilariopsis kerguelensis and Chaetoceros debilis. To unravel the underlying physiological response at the transcriptomic level, these species were grown under ambient and elevated pCO2 combined with low or high light. RNA sequencing revealed that the haptophyte was much more tolerant towards OA than the two diatoms as only these showed distinct OA-dependent gene regulation patterns. Under ambient pCO2, high light resulted in decreased glycolysis in P. antarctica. Contrastingly, upregulation of genes related to cell division and transcription as well as reduced expression of both cata- and anabolic carbon related pathways were seen in C. debilis. OA in combination with low light led to reduced respiration, but also surprisingly to higher expression of genes involved in light protection, transcription and translation in C. debilis. Though not affecting P. antarctica, OA combined with high light caused also photosensitivity in both diatoms. As additional response reallocation of carbon to lipids was found in C. debilis under these conditions. Overall, we conclude that P. antarctica is better adapted than the two diatoms to OA and high light.

UV-shielding and wavelength conversion by centric diatom nanopatterned frustules.

Diatoms can represent the major component of phytoplankton and contribute massively to global primary production in the oceans. Over tens of millions of years they developed an intricate porous silica shell, the frustule, which ensures mechanical protection, sorting of nutrients from harmful agents, and optimization of light harvesting. Several groups of microalgae evolved different strategies of protection towards ultraviolet radiation (UVR), which is harmful for all living organisms mainly through the formation of dimeric photoproducts between adjacent pyrimidines in DNA. Even in presence of low concentrations of UV-absorbing compounds, several diatoms exhibit significant UVR tolerance. We here investigated the mechanisms involved in UVR screening by diatom silica investments focusing on single frustules of a planktonic centric diatom, Coscinodiscus wailesii, analyzing absorption by the silica matrix, diffraction by frustule ultrastructure and also UV conversion into photosynthetically active radiation exerted by nanostructured silica photoluminescence. We identified the defects and organic residuals incorporated in frustule silica matrix which mainly contribute to absorption; simulated and measured the spatial distribution of UVR transmitted by a single valve, finding that it is confined far away from the diatom valve itself; furthermore, we showed how UV-to-blue radiation conversion (which is particularly significant for photosynthetic productivity) is more efficient than other emission transitions in the visible spectral range.

Effects of climatically-modulated changes in solar radiation and wind speed on spring phytoplankton community dynamics in Lake Taihu, China.

Many studies have focused on the interactive effects of temperature increases due to global warming and nutrient enrichment on phytoplankton communities. Recently, non-temperature effects of climate change (e.g., decreases in wind speed and increases in solar radiation) on large lakes have received increasing attention. To evaluate the relative contributions of both temperature and non-temperature effects on phytoplankton communities in a large eutrophic subtropical shallow lake, we analyzed long-term monitoring data from Lake Taihu, China from 1997 to 2016. Results showed that Lake Taihu's spring phytoplankton biovolume and composition changed dramatically over this time frame, with a change in dominant species. Stepwise multiple linear regression models indicated that spring phytoplankton biovolume was strongly influenced by total phosphorus (TP), light condition, wind speed and total nitrogen (TN) (radj2 = 0.8, p < 0.01). Partial redundancy analysis (pRDA) showed that light condition accounted for the greatest variation of phytoplankton community composition, followed by TP and wind speed, as well as the interactions between TP and wind speed. Our study points to the additional importance of non-temperature effects of climate change on phytoplankton community dynamics in Lake Taihu.

UV fluences required for compliance with ballast water discharge standards using two approved methods for algal viability assessment.

This study investigates the extra UV fluence needed to meet the International Maritime Organisation's ballast water discharge standards for the 10-50 µm size-class using the approved vital stain (VS) method compared to the Most Probable Number (MPN) method for organism viability assessment. Low- and medium pressure UV collimated beam treatments were applied to natural algae collected in temperate and tropical water environments and analysed using both methods. About 10 times higher UV fluence was required to meet discharge standards when using VS compared to MPN. Implementing a dark-hold period after UV treatments decreased algal viability. Length of dark-hold period to meet discharge standards decreased with increasing UV fluence. No significant differences between temperate and tropical samples were observed. The results showed that UV treated algae assessed using the VS method could meet discharge standards by increasing fluence and/or introducing a dark-hold period.

A shady phytoplankton paradox: when phytoplankton increases under low light.

Light is a fundamental driver of ecosystem dynamics, affecting the rate of photosynthesis and primary production. In spite of its importance, less is known about its community-scale effects on aquatic ecosystems compared with those of nutrient loading. Understanding light limitation is also important for ecosystem management, as human activities have been rapidly altering light availability to aquatic ecosystems. Here we show that decreasing light can paradoxically increase phytoplankton abundance in shallow lakes. Our results, based on field manipulation experiments, field observations and models, suggest that, under competition for light and nutrients between phytoplankton and submersed macrophytes, alternative stable states are possible under high-light supply. In a macrophyte-dominated state, as light decreases phytoplankton density increases, because macrophytes (which effectively compete for nutrients released from the sediment) are more severely affected by light reduction. Our results demonstrate how species interactions with spatial heterogeneity can cause an unexpected outcome in complex ecosystems. An implication of our findings is that partial surface shading for controlling harmful algal bloom may, counterintuitively, increase phytoplankton abundance by decreasing macrophytes. Therefore, to predict how shallow lake ecosystems respond to environmental perturbations, it is essential to consider effects of light on the interactions between pelagic and benthic producers.

Photobiological Effects at Earth's Surface Following a 50 pc Supernova.

We investigated the potential biological impacts at Earth's surface of stratospheric O3 depletion caused by nearby supernovae known to have occurred about 2.5 and 8 million years ago at about 50 pc distance. New and previously published atmospheric chemistry modeling results were combined with radiative transfer modeling to determine changes in surface-level solar irradiance and biological responses. We find that UVB irradiance is increased by a factor of 1.1 to 2.8, with large variation in latitude, and seasonally at high-latitude regions. Changes in UVA and PAR (visible light) are much smaller. DNA damage (in vitro) is increased by factors similar to UVB, while other biological impacts (erythema, skin cancer, cataracts, marine phytoplankton photosynthesis inhibition, and plant damage) are increased by smaller amounts. We conclude that biological impacts due to increased UV irradiance in this SN case are not mass-extinction level but might be expected to contribute to changes in species abundances; this result fits well with species turnover observed around the Pliocene-Pleistocene boundary. Key Words: UV radiation-Supernovae-Ozone-Radiative transfer. Astrobiology 18, 481-490.

Vulnerability of mixotrophic algae to nutrient pulses and UVR in an oligotrophic Southern and Northern Hemisphere lake.

Nutrient inputs and ultraviolet radiation (UVR) are global factors affecting the structure and functioning of aquatic ecosystems, particularly clear-water ecosystems. We performed experiments in two model lakes highly exposed to UVR fluxes in order to test the effect that future increases in mineral nutrients transported by dust aerosol might exert on primary producers depending on the likelihood of atmospheric inputs. Lake La Caldera (Northern Hemisphere) has been receiving recurrent dust inputs from the Sahara Desert while lake Los Cántaros (Southern Hemisphere) has been less affected by dust aerosol. UVR × Nutrient synergistically stimulated primary production (PP), chlorophyll a (Chl a), with a smaller increase in phytoplanktonic biomass in La Caldera, but not in Los Cántaros, where nutrient addition unmasked the UVR inhibitory effect on phytoplankton. The proportional decrease of mixotrophic nanoflagellates (MNFs) after the nutrient pulse (in Los Cántaros) and the long-term decline of MNFs in La Caldera associated with the increase in aerosol-dust intrusions from the Sahara during the last 40 years suggest that a future scenario of intensified aerosol events from desert and desertified areas would not only reduce functional diversity with the decline of MNFs, but would ultimately alter the C flux towards the grazing chain in oligotrophic ecosystems.