Impact of Growth Phase, Pigment Adaptation, and Climate Change Conditions on the Cellular Pigment and Carbon Content of Fifty-One Phytoplankton Isolates.

Owing to their importance in aquatic ecosystems, the demand for models that estimate phytoplankton biomass and community composition in the global ocean has increased over the last decade. Moreover, the impacts of climate change, including elevated carbon dioxide (CO2 ), increased stratification, and warmer sea surface temperatures, will likely shape phytoplankton community composition in the global ocean. Chemotaxonomic methods are useful for modeling phytoplankton community composition from marker pigments normalized to chlorophyll a (Chl a). However, photosynthetic pigments, particularly Chl a, are sensitive to nutrient and light conditions. Cellular carbon is less sensitive, so using carbon biomass instead may provide an alternative approach. To this end, cellular pigment and carbon concentrations were measured in 51 strains of globally relevant, cultured phytoplankton. Pigment-to-Chl a and pigment-to-carbon ratios were computed for each strain. For 25 strains, measurements were taken during two growth phases. While some differences between growth phases were observed, they did not exceed within-class differences. Multiple strains of Amphidinium carterae, Ditylum brightwellii and Heterosigma akashiwo were measured to determine whether time in culture influenced pigment and carbon composition. No appreciable trends in cellular pigment or carbon content were observed. Lastly, the potential impact of climate change conditions on the pigment ratios was assessed using a multistressor experiment that included increased mean light, temperature, and elevated pCO2 on three species: Thalassiosira oceanica, Ostreococcus lucimarinus, and Synechococcus. The largest differences were observed in the pigment-to-carbon ratios, while the marker pigments largely covaried with Chl a. The implications of these observations to chemotaxonomic applications are discussed.

Radiometric approach for the detection of picophytoplankton assemblages across oceanic fronts.

Cell abundances of Prochlorococcus, Synechococcus, and autotrophic picoeukaryotes were estimated in surface waters using principal component analysis (PCA) of hyperspectral and multispectral remote-sensing reflectance data. This involved the development of models that employed multilinear correlations between cell abundances across the Atlantic Ocean and a combination of PCA scores and sea surface temperatures. The models retrieve high Prochlorococcus abundances in the Equatorial Convergence Zone and show their numerical dominance in oceanic gyres, with decreases in Prochlorococcus abundances towards temperate waters where Synechococcus flourishes, and an emergence of picoeukaryotes in temperate waters. Fine-scale in-situ sampling across ocean fronts provided a large dynamic range of measurements for the training dataset, which resulted in the successful detection of fine-scale Synechococcus patches. Satellite implementation of the models showed good performance (R2 > 0.50) when validated against in-situ data from six Atlantic Meridional Transect cruises. The improved relative performance of the hyperspectral models highlights the importance of future high spectral resolution satellite instruments, such as the NASA PACE mission's Ocean Color Instrument, to extend our spatiotemporal knowledge about ecologically relevant phytoplankton assemblages.

Stoichiometry of Prochlorococcus, Synechococcus, and small eukaryotic populations in the western North Atlantic Ocean.

In the North Atlantic Ocean, we found that natural populations of Prochlorococcus adhered to Redfield ratio dimensions when comparing cell quotas of carbon to nitrogen, but had flexible composition under nutrient and light stress, allowing for a broad range of cellular carbon- and nitrogen-to-phosphorus ratios. Synechococcus populations also exhibited a wide range of elemental stoichiometry, including carbon-to-nitrogen ratios and increased their carbon-to-phosphorus ratios in response to low dissolved phosphorus availability. Small eukaryotic populations tended to have lower carbon-to-phosphorus ratios than single cell cyanobacterial groups, with the exception of one group of samples, which highlights the importance of community composition when determining how biological diversity influences bulk particle stoichiometry. The ratio of dissolved nitrogen:phosphorus fluxes into the euphotic zone was not correlated to nitrogen:phosphorus cellular quotas. The lack of a homeostatic relationship implies that other mechanisms, such as species-specific adaptation to oligotrophic phosphorus concentrations, control elemental particle ratios.

Impact of ocean phytoplankton diversity on phosphate uptake.

We have a limited understanding of the consequences of variations in microbial biodiversity on ocean ecosystem functioning and global biogeochemical cycles. A core process is macronutrient uptake by microorganisms, as the uptake of nutrients controls ocean CO2 fixation rates in many regions. Here, we ask whether variations in ocean phytoplankton biodiversity lead to novel functional relationships between environmental variability and phosphate (Pi) uptake. We analyzed Pi uptake capabilities and cellular allocations among phytoplankton groups and the whole community throughout the extremely Pi-depleted western North Atlantic Ocean. Pi uptake capabilities of individual populations were well described by a classic uptake function but displayed adaptive differences in uptake capabilities that depend on cell size and nutrient availability. Using an eco-evolutionary model as well as observations of in situ uptake across the region, we confirmed that differences among populations lead to previously uncharacterized relationships between ambient Pi concentrations and uptake. Supported by novel theory, this work provides a robust empirical basis for describing and understanding assimilation of limiting nutrients in the oceans. Thus, it demonstrates that microbial biodiversity, beyond cell size, is important for understanding the global cycling of nutrients.

Accumulation and enhanced cycling of polyphosphate by Sargasso Sea plankton in response to low phosphorus.

Phytoplankton alter their biochemical composition according to nutrient availability, such that their bulk elemental composition varies across oceanic provinces. However, the links between plankton biochemical composition and variation in biogeochemical cycling of nutrients remain largely unknown. In a survey of phytoplankton phosphorus stress in the western North Atlantic, we found that phytoplankton in the phosphorus-depleted subtropical Sargasso Sea were enriched in the biochemical polyphosphate (polyP) compared with nutrient-rich temperate waters, contradicting the canonical oceanographic view of polyP as a luxury phosphorus storage molecule. The enrichment in polyP coincided with enhanced alkaline phosphatase activity and substitution of sulfolipids for phospholipids, which are both indicators of phosphorus stress. Further, polyP appeared to be liberated preferentially over bulk phosphorus from sinking particles in the Sargasso Sea, thereby retaining phosphorus in shallow waters. Thus, polyP cycling may form a feedback loop that attenuates the export of phosphorus when it becomes scarce, contributes bioavailable P for primary production, and supports the export of carbon and nitrogen via sinking particles.

Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus.

The Cyanobacteria Prochlorococcus and Synechococcus account for a substantial fraction of marine primary production. Here, we present quantitative niche models for these lineages that assess present and future global abundances and distributions. These niche models are the result of neural network, nonparametric, and parametric analyses, and they rely on >35,000 discrete observations from all major ocean regions. The models assess cell abundance based on temperature and photosynthetically active radiation, but the individual responses to these environmental variables differ for each lineage. The models estimate global biogeographic patterns and seasonal variability of cell abundance, with maxima in the warm oligotrophic gyres of the Indian and the western Pacific Oceans and minima at higher latitudes. The annual mean global abundances of Prochlorococcus and Synechococcus are 2.9 ± 0.1 × 10(27) and 7.0 ± 0.3 × 10(26) cells, respectively. Using projections of sea surface temperature as a result of increased concentration of greenhouse gases at the end of the 21st century, our niche models projected increases in cell numbers of 29% and 14% for Prochlorococcus and Synechococcus, respectively. The changes are geographically uneven but include an increase in area. Thus, our global niche models suggest that oceanic microbial communities will experience complex changes as a result of projected future climate conditions. Because of the high abundances and contributions to primary production of Prochlorococcus and Synechococcus, these changes may have large impacts on ocean ecosystems and biogeochemical cycles.

Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity.

Phosphorus is an obligate requirement for the growth of all organisms; major biochemical reservoirs of phosphorus in marine plankton include nucleic acids and phospholipids. However, eukaryotic phytoplankton and cyanobacteria (that is, 'phytoplankton' collectively) have the ability to decrease their cellular phosphorus content when phosphorus in their environment is scarce. The biochemical mechanisms that allow phytoplankton to limit their phosphorus demand and still maintain growth are largely unknown. Here we show that phytoplankton, in regions of oligotrophic ocean where phosphate is scarce, reduce their cellular phosphorus requirements by substituting non-phosphorus membrane lipids for phospholipids. In the Sargasso Sea, where phosphate concentrations were less than 10 nmol l-1, we found that only 1.3 +/- 0.6% of phosphate uptake was used for phospholipid synthesis; in contrast, in the South Pacific subtropical gyre, where phosphate was greater than 100 nmol l-1, plankton used 17 6% (ref. 6). Examination of the planktonic membrane lipids at these two locations showed that classes of sulphur- and nitrogen-containing membrane lipids, which are devoid of phosphorus, were more abundant in the Sargasso Sea than in the South Pacific. Furthermore, these non-phosphorus, 'substitute lipids' were dominant in phosphorus-limited cultures of all of the phytoplankton species we examined. In contrast, the marine heterotrophic bacteria we examined contained no substitute lipids and only phospholipids. Thus heterotrophic bacteria, which compete with phytoplankton for nutrients in oligotrophic regions like the Sargasso Sea, appear to have a biochemical phosphorus requirement that phytoplankton avoid by using substitute lipids. Our results suggest that phospholipid substitutions are fundamental biochemical mechanisms that allow phytoplankton to maintain growth in the face of phosphorus limitation.

Development and bias assessment of a method for targeted metagenomic sequencing of marine cyanobacteria.

Prochlorococcus and Synechococcus are the most abundant photosynthetic organisms in oligotrophic waters and responsible for a significant percentage of the earth's primary production. Here we developed a method for metagenomic sequencing of sorted Prochlorococcus and Synechococcus populations using a transposon-based library preparation technique. First, we observed that the cell lysis technique and associated amount of input DNA had an important role in determining the DNA library quality. Second, we found that our transposon-based method provided a more even coverage distribution and matched more sequences of a reference genome than multiple displacement amplification, a commonly used method for metagenomic sequencing. We then demonstrated the method on Prochlorococcus and Synechococcus field populations from the Sargasso Sea and California Current isolated by flow cytometric sorting and found clear environmentally related differences in ecotype distributions and gene abundances. In addition, we saw a significant correspondence between metagenomic libraries sequenced with our technique and regular sequencing of bulk DNA. Our results show that this targeted method is a viable replacement for regular metagenomic approaches and will be useful for identifying the biogeography and genome content of specific marine cyanobacterial populations.

Long-term oscillations in the normalized biomass-size spectrum reveal the impact of oligotrophication on zooplankton trophic structure in the North Atlantic Subtropical Gyre.

Ocean warming of the North Atlantic Subtropical Gyre (NASG) induced oligotrophication and a decrease in integrated net primary production during the 2010s, potentially affecting higher trophic levels. We analyzed long-term records (1994-2019) of daytime and nighttime zooplankton biomass in five size classes from the NASG. Daytime biomass decreased in the three largest size classes during the 2010s, while decrease in nighttime biomass was less evident due to the relative stability in diel vertical migrator biomass. We used the normalized biomass size spectrum (NBSS) to estimate the relative transfer efficiency between trophic levels. The steepness of the NBSS slope at the end of the time series increased by 14% (daytime) and 24% (nighttime) from the maximum observed annual average values (2011 and 2009, respectively). This suggests oligotrophication during the 2010s led to a significant reduction in the transfer of biomass across trophic levels, with negative impacts on the NASG planktonic food web.

Phytoplankton optical fingerprint libraries for development of phytoplankton ocean color satellite products.

Phytoplankton respond to physical and hydrographic forcing on time and space scales up to and including those relevant to climate change. Quantifying changes in phytoplankton communities over these scales is essential for predicting ocean food resources, occurrences of harmful algal blooms, and carbon and other elemental cycles, among other predictions. However, one of the best tools for quantifying phytoplankton communities across relevant time and space scales, ocean color sensors, is constrained by its own spectral capabilities and availability of adequately vetted and relevant optical models. To address this later shortcoming, greater than fifty strains of phytoplankton, from a range of taxonomic lineages, geographic locations, and time in culture, alone and in mixtures, were grown to exponential and/or stationary phase for determination of hyperspectral UV-VIS absorption coefficients, multi-angle and multi-spectral backscatter coefficients, volume scattering functions, particle size distributions, pigment content, and fluorescence. The aim of this publication is to share these measurements to expedite their utilization in the development of new optical models for the next generation of ocean color satellites.

Macroalgal deep genomics illuminate multiple paths to aquatic, photosynthetic multicellularity.

Macroalgae are multicellular, aquatic autotrophs that play vital roles in global climate maintenance and have diverse applications in biotechnology and eco-engineering, which are directly linked to their multicellularity phenotypes. However, their genomic diversity and the evolutionary mechanisms underlying multicellularity in these organisms remain uncharacterized. In this study, we sequenced 110 macroalgal genomes from diverse climates and phyla, and identified key genomic features that distinguish them from their microalgal relatives. Genes for cell adhesion, extracellular matrix formation, cell polarity, transport, and cell differentiation distinguish macroalgae from microalgae across all three major phyla, constituting conserved and unique gene sets supporting multicellular processes. Adhesome genes show phylum- and climate-specific expansions that may facilitate niche adaptation. Collectively, our study reveals genetic determinants of convergent and divergent evolutionary trajectories that have shaped morphological diversity in macroalgae and provides genome-wide frameworks to understand photosynthetic multicellular evolution in aquatic environments.

Whales in the carbon cycle: can recovery remove carbon dioxide?

The great whales (baleen and sperm whales), through their massive size and wide distribution, influence ecosystem and carbon dynamics. Whales directly store carbon in their biomass and contribute to carbon export through sinking carcasses. Whale excreta may stimulate phytoplankton growth and capture atmospheric CO2; such indirect pathways represent the greatest potential for whale-carbon sequestration but are poorly understood. We quantify the carbon values of whales while recognizing the numerous ecosystem, cultural, and moral motivations to protect them. We also propose a framework to quantify the economic value of whale carbon as populations change over time. Finally, we suggest research to address key unknowns (e.g., bioavailability of whale-derived nutrients to phytoplankton, species- and region-specific variability in whale carbon contributions).

Enhanced solubility and ecological impact of atmospheric phosphorus deposition upon extended seawater exposure.

Atmospheric P solubility affects the amount of P available for phytoplankton in the surface ocean, yet our understanding of the timing and extent of atmospheric P solubility is based on short-term leaching experiments where conditions may differ substantially from the surface ocean. We conducted longer- term dissolution experiments of atmospheric aerosols in filtered seawater, and found up to 9-fold greater dissolution of P after 72 h compared to instantaneous leaching. Samples rich in anthropogenic materials released dissolved inorganic P (DIP) faster than mineral dust. To gauge the effect of biota on the fate of atmospheric P, we conducted field incubations with aerosol samples collected in the Sargasso Sea and Red Sea. In the Sargasso Sea phytoplankton were not P limited, and biological activity enhanced DIP release from aerosols, and aerosols induced biological mineralization of dissolved organic P in seawater, leading to DIP accumulation. However, in the Red Sea where phytoplankton were colimited by P and N, soluble P was rapidly consumed by phytoplankton following aerosol enrichment. Our results suggest that atmospheric P dissolution could continue over multiple days once reaching the surface ocean, and that previous estimates of atmospheric P deposition may underestimate the contribution from this source.

Adaptive carbon export response to warming in the Sargasso Sea.

Ocean ecosystem models predict that warming and increased surface ocean stratification will trigger a series of ecosystem events, reducing the biological export of particulate carbon to the ocean interior. We present a nearly three-decade time series from the open ocean that documents a biological response to ocean warming and nutrient reductions wherein particulate carbon export is maintained, counter to expectations. Carbon export is maintained through a combination of phytoplankton community change to favor cyanobacteria with high cellular carbon-to-phosphorus ratios and enhanced shallow phosphorus recycling leading to increased nutrient use efficiency. These results suggest that surface ocean ecosystems may be more responsive and adapt more rapidly to changes in the hydrographic system than is currently envisioned in earth ecosystem models, with positive consequences for ocean carbon uptake.

Global Ocean Particulate Organic Phosphorus, Carbon, Oxygen for Respiration, and Nitrogen (GO-POPCORN).

Concentrations and elemental stoichiometry of suspended particulate organic carbon, nitrogen, phosphorus, and oxygen demand for respiration (C:N:P:-O2) play a vital role in characterizing and quantifying marine elemental cycles. Here, we present Version 2 of the Global Ocean Particulate Organic Phosphorus, Carbon, Oxygen for Respiration, and Nitrogen (GO-POPCORN) dataset. Version 1 is a previously published dataset of particulate organic matter from 70 different studies between 1971 and 2010, while Version 2 is comprised of data collected from recent cruises between 2011 and 2020. The combined GO-POPCORN dataset contains 2673 paired surface POC/N/P measurements from 70°S to 73°N across all major ocean basins at high spatial resolution. Version 2 also includes 965 measurements of oxygen demand for organic carbon respiration. This new dataset can help validate and calibrate the next generation of global ocean biogeochemical models with flexible elemental stoichiometry. We expect that incorporating variable C:N:P:-O2 into models will help improve our estimates of key ocean biogeochemical fluxes such as carbon export, nitrogen fixation, and organic matter remineralization.

Large-scale genome sequencing reveals the driving forces of viruses in microalgal evolution.

Being integral primary producers in diverse ecosystems, microalgal genomes could be mined for ecological insights, but representative genome sequences are lacking for many phyla. We cultured and sequenced 107 microalgae species from 11 different phyla indigenous to varied geographies and climates. This collection was used to resolve genomic differences between saltwater and freshwater microalgae. Freshwater species showed domain-centric ontology enrichment for nuclear and nuclear membrane functions, while saltwater species were enriched in organellar and cellular membrane functions. Further, marine species contained significantly more viral families in their genomes (p = 8e-4). Sequences from Chlorovirus, Coccolithovirus, Pandoravirus, Marseillevirus, Tupanvirus, and other viruses were found integrated into the genomes of algal from marine environments. These viral-origin sequences were found to be expressed and code for a wide variety of functions. Together, this study comprehensively defines the expanse of protein-coding and viral elements in microalgal genomes and posits a unified adaptive strategy for algal halotolerance.

Abundance and diversity of heterotrophic bacterial cells assimilating phosphate in the subtropical North Atlantic Ocean.

Microorganisms play key roles in the cycles of carbon and nutrients in the ocean, and identifying the extent to which specific taxa contribute to these cycles will establish their ecological function. We examined the use of (33)P-phosphate to identify heterotrophic bacteria actively involved in the cycling of phosphate, an essential inorganic nutrient. Seawater from the sub-tropical North Atlantic Ocean was incubated with (33)P-phosphate and analysed by microautoradiography to determine the proportion and diversity of the bacterial community-assimilating phosphate. Complementary incubations using (3)H-leucine and (3)H-thymidine were also conducted. We found that a higher proportion of total heterotrophic bacterial cells in surface water samples assimilated phosphate compared with leucine or thymidine. Bacteria from all of the phylogenetic groups we identified by CARD-FISH were able to assimilate phosphate, although the abundances of cells within each group did not scale directly with the number found to assimilate phosphate. Furthermore, a significantly higher proportion of Alphaproteobacteria, Gammaproteobacteria and Cytophaga-like cells assimilated phosphate compared with leucine or thymidine. Our results suggest that a greater proportion of bacterial cells in surface waters are actively participating in the biogeochemical cycling of phosphorus, and possibly other elements, than is currently estimated through the use of (3)H-leucine or (3)H-thymidine.

Linking regional shifts in microbial genome adaptation with surface ocean biogeochemistry.

Linking 'omics measurements with biogeochemical cycles is a widespread challenge in microbial community ecology. Here, we propose applying genomic adaptation as 'biosensors' for microbial investments to overcome nutrient stress. We then integrate this genomic information with a trait-based model to predict regional shifts in the elemental composition of marine plankton communities. We evaluated this approach using metagenomic and particulate organic matter samples from the Atlantic, Indian and Pacific Oceans. We find that our genome-based trait model significantly improves our prediction of particulate C : P (carbon : phosphorus) across ocean regions. Furthermore, we detect previously unrecognized ocean areas of iron, nitrogen and phosphorus stress. In many ecosystems, it can be very challenging to quantify microbial stress. Thus, a carefully calibrated genomic approach could become a widespread tool for understanding microbial responses to environmental changes and the biogeochemical outcomes. This article is part of the theme issue 'Conceptual challenges in microbial community ecology'.

Machine learning identifies a strong association between warming and reduced primary productivity in an oligotrophic ocean gyre.

Phytoplankton play key roles in the oceans by regulating global biogeochemical cycles and production in marine food webs. Global warming is thought to affect phytoplankton production both directly, by impacting their photosynthetic metabolism, and indirectly by modifying the physical environment in which they grow. In this respect, the Bermuda Atlantic Time-series Study (BATS) in the Sargasso Sea (North Atlantic gyre) provides a unique opportunity to explore effects of warming on phytoplankton production across the vast oligotrophic ocean regions because it is one of the few multidecadal records of measured net primary productivity (NPP). We analysed the time series of phytoplankton primary productivity at BATS site using machine learning techniques (ML) to show that increased water temperature over a 27-year period (1990-2016), and the consequent weakening of vertical mixing in the upper ocean, induced a negative feedback on phytoplankton productivity by reducing the availability of essential resources, nitrogen and light. The unbalanced availability of these resources with warming, coupled with ecological changes at the community level, is expected to intensify the oligotrophic state of open-ocean regions that are far from land-based nutrient sources.

Parallel phylogeography of Prochlorococcus and Synechococcus.

The globally abundant marine Cyanobacteria Prochlorococcus and Synechococcus share many physiological traits but presumably have different evolutionary histories and associated phylogeography. In Prochlorococcus, there is a clear phylogenetic hierarchy of ecotypes, whereas multiple Synechococcus clades have overlapping physiologies and environmental distributions. However, microbial traits are associated with different phylogenetic depths. Using this principle, we reclassified diversity at different phylogenetic levels and compared the phylogeography. We sequenced the genetic diversity of Prochlorococcus and Synechococcus from 339 samples across the tropical Pacific Ocean and North Atlantic Ocean using a highly variable phylogenetic marker gene (rpoC1). We observed clear parallel niche distributions of ecotypes leading to high Pianka's Index values driven by distinct shifts at two transition points. The first transition point at 6°N distinguished ecotypes adapted to warm waters but separated by macronutrient content. At 39°N, ecotypes adapted to warm, low macronutrient vs. colder, high macronutrient waters shifted. Finally, we detected parallel vertical and regional single-nucleotide polymorphism microdiversity within clades from both Prochlorococcus and Synechococcus, suggesting uniquely adapted populations at very specific depths, as well as between the Atlantic and Pacific Oceans. Overall, this study demonstrates that Prochlorococcus and Synechococcus have shared phylogenetic organization of traits and associated phylogeography.