Gelatinous larvacean zooplankton can enhance trophic transfer and carbon sequestration.

Larvaceans are gelatinous zooplankton abundant throughout the ocean. Larvaceans have been overlooked in research because they are difficult to collect and are perceived as being unimportant in biogeochemical cycles and food-webs. We synthesise evidence that their unique biology enables larvaceans to transfer more carbon to higher trophic levels and deeper into the ocean than is commonly appreciated. Larvaceans could become even more important in the Anthropocene because they eat small phytoplankton that are predicted to become more prevalent under climate change, thus moderating projected future declines in ocean productivity and fisheries. We identify critical knowledge gaps and argue that larvaceans should be incorporated into ecosystem assessments and biogeochemical models to improve predictions of the future ocean.

Transcriptional Mechanisms of Thermal Acclimation in Prochlorococcus.

Low temperature limits the growth and the distribution of the key oceanic primary producer Prochlorococcus, which does not proliferate above a latitude of ca. 40°. Yet, the molecular basis of thermal acclimation in this cyanobacterium remains unexplored. We analyzed the transcriptional response of the Prochlorococcus marinus strain MIT9301 in long-term acclimations and in natural Prochlorococcus populations along a temperature range enabling its growth (17 to 30°C). MIT9301 upregulated mechanisms of the global stress response at the temperature minimum (17°C) but maintained the expression levels of genes involved in essential metabolic pathways (e.g., ATP synthesis and carbon fixation) along the whole thermal niche. Notably, the declining growth of MIT9301 from the optimum to the minimum temperature was coincident with a transcriptional suppression of the photosynthetic apparatus and a dampening of its circadian expression patterns, indicating a loss in their regulatory capacity under cold conditions. Under warm conditions, the cellular transcript inventory of MIT9301 was strongly streamlined, which may also induce regulatory imbalances due to stochasticity in gene expression. The daytime transcriptional suppression of photosynthetic genes at low temperature was also observed in metatranscriptomic reads mapping to MIT9301 across the global ocean, implying that this molecular mechanism may be associated with the restricted distribution of Prochlorococcus to temperate zones. IMPORTANCE Prochlorococcus is a major marine primary producer with a global impact on atmospheric CO2 fixation. This cyanobacterium is widely distributed across the temperate ocean, but virtually absent at latitudes above 40° for yet unknown reasons. Temperature has been suggested as a major limiting factor, but the exact mechanisms behind Prochlorococcus thermal growth restriction remain unexplored. This study brings us closer to understanding how Prochlorococcus functions under challenging temperature conditions, by focusing on its transcriptional response after long-term acclimation from its optimum to its thermal thresholds. Our results show that the drop in Prochlorococcus growth rate under cold conditions was paralleled by a transcriptional suppression of the photosynthetic machinery during daytime and a loss in the organism's regulatory capacity to maintain circadian expression patterns. Notably, warm temperature induced a marked shrinkage of the organism's cellular transcript inventory, which may also induce regulatory imbalances in the future functioning of this cyanobacterium.

Temperature Responses of Heterotrophic Bacteria in Co-culture With a Red Sea Synechococcus Strain.

Interactions between autotrophic and heterotrophic bacteria are fundamental for marine biogeochemical cycling. How global warming will affect the dynamics of these essential microbial players is not fully understood. The aims of this study were to identify the major groups of heterotrophic bacteria present in a Synechococcus culture originally isolated from the Red Sea and assess their joint responses to experimental warming within the metabolic ecology framework. A co-culture of Synechococcus sp. RS9907 and their associated heterotrophic bacteria, after determining their taxonomic affiliation by 16S rRNA gene sequencing, was acclimated and maintained in the lab at different temperatures (24-34°C). The abundance and cellular properties of Synechococcus and the three dominant heterotrophic bacterial groups (pertaining to the genera Paracoccus, Marinobacter, and Muricauda) were monitored by flow cytometry. The activation energy of Synechococcus, which grew at 0.94-1.38 d-1, was very similar (0.34 ± 0.02 eV) to the value hypothesized by the metabolic theory of ecology (MTE) for autotrophs (0.32 eV), while the values of the three heterotrophic bacteria ranged from 0.16 to 1.15 eV and were negatively correlated with their corresponding specific growth rates (2.38-24.4 d-1). The corresponding carrying capacities did not always follow the inverse relationship with temperature predicted by MTE, nor did we observe a consistent response of bacterial cell size and temperature. Our results show that the responses to future ocean warming of autotrophic and heterotrophic bacteria in microbial consortia might not be well described by theoretical universal rules.

Changes in Population Age-Structure Obscure the Temperature-Size Rule in Marine Cyanobacteria.

The temperature-size Rule (TSR) states that there is a negative relationship between ambient temperature and body size. This rule has been independently evaluated for different phases of the life cycle in multicellular eukaryotes, but mostly for the average population in unicellular organisms. We acclimated two model marine cyanobacterial strains (Prochlorococcus marinus MIT9301 and Synechococcus sp. RS9907) to a gradient of temperatures and measured the changes in population age-structure and cell size along their division cycle. Both strains displayed temperature-dependent diel changes in cell size, and as a result, the relationship between temperature and average cell size varied along the day. We computed the mean cell size of new-born cells in order to test the prediction of the TSR on a single-growth stage. Our work reconciles previous inconsistent results when testing the TSR on unicellular organisms, and shows that when a single-growth stage is considered the predicted negative response to temperature is revealed.

Types and Distribution of Bioactive Polyunsaturated Aldehydes in a Gradient from Mesotrophic to Oligotrophic Waters in the Alborán Sea (Western Mediterranean).

Polyunsaturated aldehydes (PUAs) are bioactive molecules suggested as chemical defenses and infochemicals. In marine coastal habitats, diatoms reach high PUA production levels during bloom episodes. Two fractions of PUA can usually be analyzed: pPUA obtained via artificial breakage of collected phytoplankton cells and dissolved PUA already released to the environment (dPUA). In nature, resource supply arises as a main environmental controlling factor of PUA production. In this work, we monitored the vertical distribution and daily variation of pPUA associated with large-size phytoplankton and dPUA, at three sites located in the Alborán Sea from mesotrophic to oligotrophic waters. The results corroborate the presence of large-size PUA producers in oligotrophic and mesotrophic waters with a significant (58%-85%) diatom biomass. In addition to diatoms, significant correlations between pPUA production and dinoflagellate and silicoflagellate abundance were observed. 2E,4E/Z-Heptadienal was the most abundant aldehyde at the three sites with higher values (17.1 fg·cell-1) at the most oligotrophic site. 2E,4E/Z-Decadienal was the least abundant aldehyde, decreasing toward the oligotrophic site. For the first time, we describe the daily fluctuation of pPUA attributable to cellular physiological state and not exclusively to taxonomical composition. Our results demonstrate the persistence of threshold levels of dPUA deep in the water column, as well as the different chromatographic profiles of dPUA compared with pPUA. We propose different isomerization processes that alter the chemical structure of the released PUAs with unknown effects on their stability, biological function, and potential bioactivity.

In Vivo Single-Cell Fluorescence and Size Scaling of Phytoplankton Chlorophyll Content.

In unicellular phytoplankton, the size scaling exponent of chlorophyll content per cell decreases with increasing light limitation. Empirical studies have explored this allometry by combining data from several species, using average values of pigment content and cell size for each species. The resulting allometry thus includes phylogenetic and size scaling effects. The possibility of measuring single-cell fluorescence with imaging-in-flow cytometry devices allows the study of the size scaling of chlorophyll content at both the inter- and intraspecific levels. In this work, the changing allometry of chlorophyll content was estimated for the first time for single phytoplankton populations by using data from a series of incubations with monocultures exposed to different light levels. Interspecifically, our experiments confirm previous modeling and experimental results of increasing size scaling exponents with increasing irradiance. A similar pattern was observed intraspecifically but with a larger variability in size scaling exponents. Our results show that size-based processes and geometrical approaches explain variations in chlorophyll content. We also show that the single-cell fluorescence measurements provided by imaging-in-flow devices can be applied to field samples to understand the changes in the size dependence of chlorophyll content in response to environmental variables affecting primary production.IMPORTANCE The chlorophyll concentrations in phytoplankton register physiological adjustments in cellular pigmentation arising mainly from changes in light conditions. The extent of these adjustments is constrained by the size of the phytoplankton cells, even within single populations. Hence, variations in community chlorophyll derived from photoacclimation are also dependent on the phytoplankton size distribution.

The allometry of the smallest: superlinear scaling of microbial metabolic rates in the Atlantic Ocean.

Prokaryotic planktonic organisms are small in size but largely relevant in marine biogeochemical cycles. Due to their reduced size range (0.2 to 1 µm in diameter), the effects of cell size on their metabolism have been hardly considered and are usually not examined in field studies. Here, we show the results of size-fractionated experiments of marine microbial respiration rate along a latitudinal transect in the Atlantic Ocean. The scaling exponents obtained from the power relationship between respiration rate and size were significantly higher than one. This superlinearity was ubiquitous across the latitudinal transect but its value was not universal revealing a strong albeit heterogeneous effect of cell size on microbial metabolism. Our results suggest that the latitudinal differences observed are the combined result of changes in cell size and composition between functional groups within prokaryotes. Communities where the largest size fraction was dominated by prokaryotic cyanobacteria, especially Prochlorococcus, have lower allometric exponents. We hypothesize that these larger, more complex prokaryotes fall close to the evolutionary transition between prokaryotes and protists, in a range where surface area starts to constrain metabolism and, hence, are expected to follow a scaling closer to linearity.

Seasonality in molecular and cytometric diversity of marine bacterioplankton: the re-shuffling of bacterial taxa by vertical mixing.

The 'cytometric diversity' of phytoplankton communities has been studied based on single-cell properties, but the applicability of this method to characterize bacterioplankton has been unexplored. Here, we analysed seasonal changes in cytometric diversity of marine bacterioplankton along a decadal time-series at three coastal stations in the Southern Bay of Biscay. Shannon-Weaver diversity estimates and Bray-Curtis similarities obtained by cytometric and molecular (16S rRNA tag sequencing) methods were significantly correlated in samples from a 3.5 year monthly time-series. Both methods showed a consistent cyclical pattern in the diversity of surface bacterial communities with maximal values in winter. The analysis of the highly resolved flow cytometry time-series across the vertical profile showed that water column mixing was a key factor explaining the seasonal changes in bacterial composition and the winter increase in bacterial diversity in coastal surface waters. Due to its low cost and short processing time as compared with genetic methods, the cytometric diversity approach represents a useful complementary tool in the macroecology of aquatic microbes.

More, smaller bacteria in response to ocean's warming?

Heterotrophic bacteria play a major role in organic matter cycling in the ocean. Although the high abundances and relatively fast growth rates of coastal surface bacterioplankton make them suitable sentinels of global change, past analyses have largely overlooked this functional group. Here, time series analysis of a decade of monthly observations in temperate Atlantic coastal waters revealed strong seasonal patterns in the abundance, size and biomass of the ubiquitous flow-cytometric groups of low (LNA) and high nucleic acid (HNA) content bacteria. Over this relatively short period, we also found that bacterioplankton cells were significantly smaller, a trend that is consistent with the hypothesized temperature-driven decrease in body size. Although decadal cell shrinking was observed for both groups, it was only LNA cells that were strongly coherent, with ecological theories linking temperature, abundance and individual size on both the seasonal and interannual scale. We explain this finding because, relative to their HNA counterparts, marine LNA bacteria are less diverse, dominated by members of the SAR11 clade. Temperature manipulation experiments in 2012 confirmed a direct effect of warming on bacterial size. Concurrent with rising temperatures in spring, significant decadal trends of increasing standing stocks (3% per year) accompanied by decreasing mean cell size (-1% per year) suggest a major shift in community structure, with a larger contribution of LNA bacteria to total biomass. The increasing prevalence of these typically oligotrophic taxa may severely impact marine food webs and carbon fluxes by an overall decrease in the efficiency of the biological pump.

Multiclass support vector machines with example-dependent costs applied to plankton biomass estimation.

In many applications, the mistakes made by an automatic classifier are not equal, they have different costs. These problems may be solved using a cost-sensitive learning approach. The main idea is not to minimize the number of errors, but the total cost produced by such mistakes. This brief presents a new multiclass cost-sensitive algorithm, in which each example has attached its corresponding misclassification cost. Our proposal is theoretically well-founded and is designed to optimize cost-sensitive loss functions. This research was motivated by a real-world problem, the biomass estimation of several plankton taxonomic groups. In this particular application, our method improves the performance of traditional multiclass classification approaches that optimize the accuracy.

The offspring-development-time/offspring-number trade-off.

The metabolic theory of ecology (MTE) states that metabolic rate, ruled mainly by individual mass and temperature, determines many other biological rates. This view of ecology as ruled by the laws of physics and thermodynamics contrasts with life-history-optimization (LHO) theories, where traits are shaped by evolutionary processes. Integrating the MTE and LHO can lead, however, to a synthetic theory of ecology. In this work, we link the two theories to show that offspring development time is the result of both maternal investment in offspring and the metabolic constraints on offspring growth. We formulate a model that captures how offspring development time is the consequence of both offspring growth rate, determined by temperature and allometric scaling in accordance with the MTE, and the size reached by offspring at the end of the developmental period, determined mainly by LHO and reproductive strategies. We first extend the trade-off between offspring size and offspring number to ectotherms, showing that increased body temperatures result in increased resources available for reproduction. We then combine this trade-off with the general ontogenetic growth model to show that there is a trade-off between the number of offspring produced and offspring development time. The model predicts a shorter developmental time in organisms producing larger numbers of offspring.

Faking giants: the evolution of high prey clearance rates in jellyfishes.

Jellyfishes have functionally replaced several overexploited commercial stocks of planktivorous fishes. This is paradoxical, because they use a primitive prey capture mechanism requiring direct contact with the prey, whereas fishes use more efficient visual detection. We have compiled published data to show that, in spite of their primitive life-style, jellyfishes exhibit similar instantaneous prey clearance and respiration rates as their fish competitors and similar potential for growth and reproduction. To achieve this production, they have evolved large, water-laden bodies that increase prey contact rates. Although larger bodies are less efficient for swimming, optimization analysis reveals that large collectors are advantageous if they move through the water sufficiently slowly.

Resource limitation of bacterial production distorts the temperature dependence of oceanic carbon cycling.

Our view of the effects of temperature on bacterial carbon fluxes in the ocean has been confounded by the interplay of resource availability. Using an extensive compilation of cell-specific bacterial respiration (BRi) and production (BPi), we show that both physiological rates respond to changing temperature in a similar manner and follow the predictions of the metabolic theory of ecology. Their apparently different temperature dependence under warm, oligotrophic conditions is due to strong resource limitation of BP, but not of BRi. Thus, and despite previous preconception, bacterial growth efficiency (BGE = BPi/[BPi + BRi]) is not directly regulated by temperature, but by the availability of substrates for growth. We develop simple equations that can be used for the estimation of bacterial community metabolism from temperature, chlorophyll concentration, and bacterial abundance. Since bacteria are the greatest living planktonic biomass, our results challenge current understanding of how warming and shifts in ecosystem trophic state will modify oceanic carbon cycle feedbacks to climate change.

Scaling the metabolic balance of the oceans.

Oceanic communities are sources or sinks of CO2, depending on the balance between primary production and community respiration. The prediction of how global climate change will modify this metabolic balance of the oceans is limited by the lack of a comprehensive underlying theory. Here, we show that the balance between production and respiration is profoundly affected by environmental temperature. We extend the general metabolic theory of ecology to the production and respiration of oceanic communities and show that ecosystem rates can be reliably scaled from theoretical knowledge of organism physiology and measurement of population abundance. Our theory predicts that the differential temperature-dependence of respiration and photosynthesis at the organism level determines the response of the metabolic balance of the epipelagic ocean to changes in ambient temperature, a prediction that we support with empirical data over the global ocean. Furthermore, our model predicts that there will be a negative feedback of ocean communities to climate warming because they will capture less CO2 with a future increase in ocean temperature. This feedback of marine biota will further aggravate the anthropogenic effects on global warming.