Natural Phytoplankton Populations Research Articles

Phytoplankton Dynamics and Biogeochemistry of the Black Sea

The biogeochemistry of waters is an essential regulator of phytoplankton dynamics, determining the level of species bloom and the change in dominants. This paper investigated the seasonal dynamics of phytoplankton and the nutrient concentrations and their ratios in the northeastern Black Sea in 2017–2021. Two taxonomic groups, diatoms and coccolithophores, determine the seasonal dynamics and significantly contribute to the total phytoplankton biomass. Coccolithophores formed blooms in early June annually, except in 2020. Large diatoms dominated in summer with a biomass exceeding 1000 mg m−3 annually, except in 2019. During the blooms of these taxonomic groups, their contribution to the total phytoplankton biomass exceeded 90%. Each group has characteristic biogeochemical niches in the nitrogen and phosphorus concentration coordinates. The position of the seasonal thermocline regulates the biogeochemistry of the water. With a high-lying and sharp gradient thermocline (the average for five years is 6.87 m), low nitrogen concentrations and a nitrogen-to-phosphorus ratio below the Redfield ratio are created in the upper mixed layer. These conditions are optimal for the dominance of coccolithophores. When the thermocline is deepened (the average for five years is 17.96 m), the phosphorus concentration decreases significantly and the ratio of nitrogen to phosphorus is significantly higher than the Redfield ratio, and these conditions lead to the dominance of large diatoms. The results of experimental studies with nitrogen and phosphorus additives in the natural phytoplankton population confirm the above statements. The addition of phosphorus leads to the increased role of coccolithophores in the total phytoplankton biomass, the addition of nitrogen alone contributes to the growth of large diatoms, and the combined addition of phosphorus and nitrogen in a ratio close to the Redfield ratio leads to the dominance of small diatoms.

Effects of cyanate enrichment on growth of natural phytoplankton populations in the subtropical Pacific

Effects of cyanate enrichment on growth of natural phytoplankton populations in the subtropical Pacific

Evolution of Phytoplankton as Estimated from Genetic Diversity

Phytoplankton are photosynthetic, single-celled organisms producing almost half of all oxygen on Earth and play a central role as prey for higher organisms, making them irreplaceable in the marine food web. As Global Change proceeds, imposing rapidly intensifying selection pressures, phytoplankton are forced to undergo evolution, local extinction, or redistribution, with potentially cascading effects throughout the marine ecosystem. Recent results from the field of population genetics display high levels of standing genetic diversity in natural phytoplankton populations, providing ample ‘evolutionary options’ and implying high adaptive potential to changing conditions. This potential for adaptive evolution is realized in several studies of experimental evolution, even though most of these studies investigate the evolution of only single strains. This, however, shows that phytoplankton not only evolve from standing genetic diversity, but also rely on de novo mutations. Recent global sampling campaigns show that the immense intraspecific diversity of phytoplankton in the marine ecosystem has been significantly underestimated, meaning we are only studying a minor portion of the relevant variability in the context of Global Change and evolution. An increased understanding of genomic diversity is primarily hampered by the low number of ecologically representative reference genomes of eukaryotic phytoplankton and the functional annotation of these. However, emerging technologies relying on metagenome and transcriptome data may offer a more realistic understanding of phytoplankton diversity.

The ecological response of natural phytoplankton population and related metabolic rates to future ocean acidification

The ecological response of natural phytoplankton population and related metabolic rates to future ocean acidification

Intraseasonal predictability of natural phytoplankton population dynamics.

It is difficult to make skillful predictions about the future dynamics of marine phytoplankton populations. Here, we use a 22‐year time series of monthly average abundances for 198 phytoplankton taxa from Station L4 in the Western English Channel (1992–2014) to test whether and how aggregating phytoplankton into multi‐species assemblages can improve predictability of their temporal dynamics. Using a non‐parametric framework to assess predictability, we demonstrate that the prediction skill is significantly affected by how species data are grouped into assemblages, the presence of noise, and stochastic behavior within species. Overall, we find that predictability one month into the future increases when species are aggregated together into assemblages with more species, compared with the predictability of individual taxa. However, predictability within dinoflagellates and larger phytoplankton (>12 μm cell radius) is low overall and does not increase by aggregating similar species together. High variability in the data, due to observational error (noise) or stochasticity in population growth rates, reduces the predictability of individual species more than the predictability of assemblages. These findings show that there is greater potential for univariate prediction of species assemblages or whole‐community metrics, such as total chlorophyll or biomass, than for the individual dynamics of phytoplankton species.

Phytoplankton community structuring and succession in a competition-neutral resource landscape

Phytoplankton community composition and succession affect aquatic food webs and biogeochemistry. Resource competition is commonly viewed as an important governing factor for community structuring and this perception is imbedded in modern ecosystem models. Quantitative consideration of the physical spacing between phytoplankton cells, however, suggests that direct competition for growth-limiting resources is uncommon. Here we describe how phytoplankton size distributions and temporal successions are compatible with a competition-neutral resource landscape. Consideration of phytoplankton-herbivore interactions with proportional feeding size ranges yields small-cell dominated size distributions consistent with observations for stable aquatic environments, whereas predator–prey temporal lags and blooming physiologies shift this distribution to larger mean cell sizes in temporally dynamic environments. We propose a conceptual mandala for understanding phytoplankton community composition where species successional series are initiated by environmental disturbance, guided by the magnitude of these disturbances and nutrient stoichiometry, and terminated with the return toward a ‘stable solution’. Our conceptual mandala provides a framework for interpreting and modeling the environmental structuring of natural phytoplankton populations.

Hydrocarbon-Degrading Bacteria Found Tightly Associated with the 50–70 μm Cell-Size Population of Eukaryotic Phytoplankton in Surface Waters of a Northeast Atlantic Region

The surface of marine eukaryotic phytoplankton can harbour communities of hydrocarbon-degrading bacteria; however, this algal–bacterial association has, hitherto, been only examined with non-axenic laboratory cultures of micro-algae. In this study, we isolated an operationally-defined community of phytoplankton, of cell size 50–70 μm, from a natural community in sea surface waters of a subarctic region in the northeast Atlantic. Using MiSeq 16S rRNA sequencing, we identified several recognized (Alcanivorax, Marinobacter, Oleispira, Porticoccus, Thalassospira) and putative hydrocarbon degraders (Colwelliaceae, Vibrionaceae) tightly associated with the phytoplankton population. We combined fluorescence in situ hybridisation with flow-cytometry (FISH-Flow) to examine the association of Marinobacter with this natural eukaryotic phytoplankton population. About 1.5% of the phytoplankton population contained tightly associated Marinobacter. The remaining Marinobacter population were loosely associated with either eukaryotic phytoplankton cells or non-chlorophyll particulate material. This work is the first to show the presence of obligate, generalist and putative hydrocarbonoclastic bacteria associated with natural populations of eukaryotic phytoplankton directly from sea surface water samples. It also highlights the suitability of FISH-Flow for future studies to examine the spatial and temporal structure and dynamics of these and other algal–bacterial associations in natural seawater samples.

Nutrient Patchiness, Phytoplankton Surge-Uptake, and Turbulent History: A Theoretical Approach and Its Experimental Validation

Despite ample evidence of micro- and small-scale (i.e., millimeter- to meter-scale) phytoplankton and zooplankton patchiness in the ocean, direct observations of nutrient distributions and the ecological importance of this phenomenon are still relatively scarce. In this context, we first describe a simple procedure to continuously sample nutrients in surface waters, and subsequently provide evidence of the existence of microscale distribution of ammonium in the ocean. We further show that ammonium is never homogeneously distributed, even under very high conditions of turbulence. Instead, turbulence intensity appears to control nutrient patchiness, with a more homogeneous or a more heterogeneous distribution observed under high and low turbulence intensities, respectively, under the same concentration in nutrient. Based on a modelling procedure taking into account the stochastic properties of intermittent nutrient distributions and observations carried out on natural phytoplankton communities, we introduce and verify the hypothesis that under nutrient limitation, the “turbulent history” of phytoplankton cells, i.e., the turbulent conditions they experienced in their natural environments, conditions their efficiency to uptake ephemeral inorganic nitrogen patches of different concentrations. Specifically, phytoplankton cells exposed to high turbulence intensities (i.e., more homogeneous nutrient distribution) were more efficient to uptake high concentration nitrogen pulses (2 µM). In contrast, under low turbulence conditions (i.e., more heterogeneous nutrient distribution), uptake rates were higher for low concentration nitrogen pulses (0.5 µM). These results suggest that under nutrient limitation, natural phytoplankton populations respond to high turbulence intensities through a decrease in affinity for nutrients and an increase in their transport rate, and vice versa.

Characteristics of global port phytoplankton and implications for current ballast water regulations

The International Maritime Organization and U.S. Coast Guard have implemented regulations to reduce introductions of non-indigenous species via ballast water (BW). For phytoplankton, regulations limit discharges to <10 live/viable cells mL−1 (size: 10–50 μm), ignoring other size fractions. Additionally, challenge conditions of 100 (shipboard) and 1000 (land-based) cells mL−1 are required in BW management system certification testing. How these requirements correspond to natural phytoplankton populations is poorly resolved. We analyzed phytoplankton samples from 31 major ports to evaluate: a) how natural communities compare to challenge requirements and b) abundances of unregulated size fractions (i.e., <10 and ≥50 μm). None of the ports met land-based challenge conditions, and only 32% met requirements for shipboard testing. Approximately 71% of organisms ≥50 μm were centric diatoms, also unregulated by current protocols. This study demonstrates that current regulations do not consider natural phytoplankton populations, limiting control efforts for potentially harmful non-indigenous species.

The role of mineral nutrients in regulation of phytoplankton community structure of the North-Eastern part of the Black Sea at the end of May 2019

The effect of nitrogen and phosphorus additives on the species structure of the natural phytoplankton population at the end of May 2019 was studied. An increase in the concentration of nitrogen and phosphorus in seawater led to a rise in the number of coccolithophores, while the relative contribution of phosphorus was higher. The predominance of small-cell diatoms in the community was facilitated by the simultaneous addition of nitrogen and phosphorus. In contrast, the relative contribution of nitrogen was higher than that of phosphorus. An increase in nitrogen concentrations at relatively low phosphorus concentrations intensified the growth of large-cell diatoms.

Changes in phytoplankton production and upwelling intensity off A Coru\xf1a (NW Spain) for the last 28\xa0years

The analysis of a 28-year-long (1989–2016) series of monthly measurements of chlorophyll concentrations and primary production rates at a shelf station off A Coruña (NW Spain) provided evidence of changes at several time scales that were only partly related to upwelling intensity. Chlorophyll determinations were made in acetonic extracts and primary production rates by the measurement of 14C-uptake by natural phytoplankton populations in simulated in situ conditions. Wavelet analysis revealed multiple modes of variation in both series, particularly at high frequencies, but some were only significant for part of the series. For instance, the seasonal cycle was not uniform through the series despite the annual repetition of maxima and minima. At multiannual time scales, both series were divided in three quasi-decadal periods characterized by significant increases in mean values. Fluctuations in chlorophyll and primary production covaried with changes in upwelling intensity at annual scales, but annual means showed low correlation. Changes in dissolved nutrient concentrations from continental sources were the likely drivers of the observed changes in productivity at large time scales. Increases in the decadal mean rates of production and concentrations of chlorophyll were driven by increased intensity of spring blooms associated to increased nutrients and low salinity water in the surface. In contrast, blooms caused by upwelling nutrients remained unchanged along the series. This study illustrates the complexity of interactions in coastal upwelling areas at large time scales, where changes in continental nutrient inputs may affect phytoplankton production more than variations in upwelling intensity.

2H/1H fractionation in microalgal lipids from the North Pacific Ocean: Growth rate and irradiance effects

The hydrogen isotope ratio (2H/1H) of microalgal lipids has become a useful tool for reconstructing hydrologic conditions in the geologic past from marine and lacustrine sediments. Culture studies have shown that, in addition to the 2H/1H ratio of growth water, parameters such as salinity, growth rate, and irradiance, can have a large effect on lipid 2H/1H ratios. But aside from salinity, these effects have not been well studied in the field. In this work, hydrogen isotope fractionation relative to growth water was measured in four algal lipids - C37:3 and C37:2 methyl alkenones, (3β,4α,5α,22E)-4,23-Dimethylergost-22-en-3-ol (dinosterol), and 24-methylcholesta-5,22E-dien-3β-ol (brassicasterol) – in the upper water column of two North Pacific Ocean locations. By comparing lipid 2H/1H variations as a function of depth at tropical Station ALOHA (22°45′N, 158°00′W) and mid-latitude Gyre (41°30′N, 132°00′W in the Transition Zone) it was possible to evaluate the H isotope effects of nutrient limitation and irradiance on natural phytoplankton populations by comparing measured fractionation factors (αlipid) with those derived from laboratory-based empirical relationships. Significant distinctions were observed between the inferred causes of H isotope fractionation in different algal lipids at the two locations. At Station Aloha, 2H/1H fractionation in coccolithophorid-derived alkenones was primarily caused by nutrient-limited growth, while at Gyre it was caused by light limitation. Distinctions were less clear for the two sterols. 2H/1H fractionation in dinosterol was possibly influenced by nutrient-limited growth or light limitation at greater depths at both stations, while 2H/1H fractionation in brassicasterol matched values expected for nutrient-limited growth at both locations. Although systematic trends with depth in αlipid on the order of 10–30‰ were observed for each lipid, inter-day variability was some 3–7‰ depending on the lipid and site, and the magnitude of αlipid changes observed in the field were much less than those expected based on culture studies. This implies that the effects of nutrient and light limitation on natural phytoplankton populations in the ocean may not have a large influence on hydroclimate reconstructions based on 2H/1H ratios of microalgal lipids in marine sediments.

Both phosphorus- and nitrogen limitation constrain viral proliferation in marine phytoplankton

Through cell lysis, viruses shape phytoplankton community composition and stimulatebiogeochemical cycling in the oceans. Earlier studies indicate that reduced phosphorus (P)availability can affect phytoplankton virus proliferation. The effects of nitrogen (N) availability areclaimed to be weaker than those for P, but this has not been thoroughly studied. Here, we investigatedhow N-limiting growth conditions, resulting in altered algal elemental stoichiometry andphysiology, affected virus proliferation in the phytoplankters Micromonas pusilla and Phaeocystisglobosa. Algal cultures were adapted to balanced nutrient-limited growth, i.e. N-, P- and NPcontrolledgrowth, before infection with their respective viruses MpV-08T and PgV-07T. The viralinfection experiments were then performed in batch cultures to allow optimal 1-step virus growthcycles. Compared to the nutrient-replete cultures, infection of nutrient-controlled hosts resulted inelongated latent periods (time until first virus release) and reduced viral burst sizes (viruses lysedhost cell−1) for both MpV and PgV. For MpV, the viral burst size was reduced by 70%, independentof the type of nutrient. The burst size of PgV was most reduced under N-limitation, by as much as92%, compared to 70% under P-limitation. Overall, our results demonstrate that algal virusproduction can be strongly impaired by N-limitation and that the effects are of a similar magnitudeto or even larger than for P. Our study indicates that viral control of natural phytoplanktonpopulations might be strongly driven by both P- and N-availability.

Biodegradability of algal-derived organic matter in a large artificial lake by using stable isotope tracers.

In order to understand the biodegradability of algal-derived organic matter, biodegradation experiments were conducted with (13)C and (15)N-labeled natural phytoplankton and periphytic algal populations in experimental conditions for 60days. Qualitative changes in the dissolved organic matter were also determined using parallel factor analysis and the stable carbon isotopic composition of the hydrophobic dissolved organic matter through the experimental period. Although algal-derived organic matter is considered to be easily biodegradable, the initial amounts of total organic carbon newly produced by phytoplankton and periphytic algae remained approximately 16 and 44% after 60days, respectively, and about 22 and 43% of newly produced particulate nitrogen remained. Further, the dissolved organic carbon derived from both algal populations increased significantly after 60days. Although the dissolved organic matter gradually became refractory, the contributions of the algal-derived organic matter to the dissolved organic matter and hydrophobic dissolved organic matter increased. Our laboratory experimental results suggest that algal-derived organic matter produced by phytoplankton and periphytic algae could contribute significantly to the non-biodegradable organic matter through microbial transformations.

Nutrient induced fluorescence transients (NIFTs) provide a rapid measure of P and C (co-)limitation in a green alga

Nutrient Induced Fluorescence Transients (NIFTs) have been shown to be a possible way of testing for the limiting nutrient in algal populations. In this study we tested the hypothesis that NIFTs can be used to detect a (co-)limitation for inorganic phosphorus (Pi) and CO2 in the green alga Chlamydomonas acidophila and that the magnitude of the NIFTs can be related to cellular P:C ratios. We show a co-limitation response for Pi and CO2 via traditional nutrient enrichment experiments in natural phytoplankton populations dominated by C. acidophila. We measured NIFT responses after a Pi- or a CO2-spike in C. acidophila batch cultures at various stages of Pi and inorganic C limitation. Significant NIFTs were observed in response to spikes in both nutrients. The NIFT response to a Pi-spike showed a strong negative correlation with cellular P:C ratio that was pronounced below 3 mmol P: mol C (equivalent to 0.2 pg P cell–1). Both cellular P and C content influenced the extent of the Pi-NIFT response. The NIFT response to a CO2-spike correlated to low CO2 culturing conditions and also had a negative correlation with cellular P content. A secondary response within the Pi-NIFT response was related to the CO2 concentration and potentially reflected co-limitation. In conclusion, NIFTs provided a quick and reliable method to detect the growth-limiting nutrient in an extremophile green alga, under Pi-, CO2- and Pi/CO2 (co-)limited growth conditions.

A multi‐laser flow cytometry method to measure single cell and population‐level relative fluorescence action spectra for the targeted study and isolation of phytoplankton in complex assemblages

AbstractDiscerning the diversity, abundance, and functional role of distinct phytoplankton groups is essential to ecological study of aquatic systems. Flow cytometry is a widely used method to rapidly identify and quantify individual phytoplankton cells. Here, we present a new flow cytometry method that uses up to five excitation colors to determine the relative fluorescence action spectra of phytoplankton within complex assemblages, thus leveraging the precise and high‐throughput capabilities of flow cytometry and the unique combinations of photosynthetic pigments in phylogenetically related groups of phytoplankton. First, we tested the method on cultivated Synechococcus of known pigment composition and genotype then we applied the method to a natural phytoplankton assemblage where we determined the relative fluorescence action spectra of numerous distinct populations. By coupling multi‐laser flow cytometry to cell sorting we demonstrated that natural phytoplankton populations with similar relative fluorescence action spectra belonged to the same taxonomic classes based on 18S rRNA gene phylogeny. This method will be instrumental in studying the ecology of distinct phytoplankton populations within complex microbial communities through spectral analysis of individual cells, identification of unique populations, and cell sorting for downstream applications such as enrichment for isolation, genome assembly, and linkage of chromatic and genetic information in a predictive fashion.

Ecotoxicology of bromoacetic acid on estuarine phytoplankton

Bromoacetic acid is formed when effluent containing chlorine residuals react with humics in natural waters containing bromide. The objective of this research was to quantify the effects of bromoacetic acid on estuarine phytoplankton as a proxy for ecosystem productivity. Bioassays were used to measure the EC50 for growth in cultured species and natural marine communities. Growth inhibition was estimated by changes in chlorophyll a concentrations measured by fluorometry and HPLC. The EC50s for cultured Thalassiosira pseudonana were 194 mg L−1, 240 mg L−1 for Dunaliella tertiolecta and 209 mg L−1 for Rhodomonas salina. Natural phytoplankton communities were more sensitive to contamination with an EC50 of 80 mg L−1. Discriminant analysis suggested that bromoacetic acid additions cause an alteration of phytoplankton community structure with implications for higher trophic levels. A two-fold EC50 decrease in mixed natural phytoplankton populations affirms the importance of field confirmation for establishing water quality criteria.

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.

Comparison of two methods to derive the size-structure of natural populations of phytoplankton

Various methods have been proposed to estimate the size structure of phytoplankton in situ, each exhibiting limitations and advantages. Two common approaches are size-fractionated filtration (SFF) and analysis of pigments derived from High Performance Liquid Chromatography (HPLC), and yet these two techniques have rarely been compared. In this paper, size-fractionated chlorophylls for pico- (<2μm), nano- (2–20μm) and micro-phytoplankton (>20μm) were estimated independently from concurrent measurements of HPLC and SFF data collected along Atlantic Meridional Transect cruises. Three methods for estimating size-fractionated chlorophyll from HPLC data were tested. Size-fractionated chlorophylls estimated from HPLC and SFF data were significantly correlated, with HPLC data explaining between 40 and 88% of the variability in the SFF data. However, there were significant biases between the two methods, with HPLC methods overestimating nanoplankton chlorophyll and underestimating picoplankton chlorophyll when compared with SFF. Uncertainty in both HPLC and SFF data makes it difficult to ascertain which is more reliable. Our results highlight the importance of using multiple methods when determining the size-structure of phytoplankton in situ, to reduce uncertainty and facilitate interpretation of data.

Light and nutrient control of photosynthesis in natural phytoplankton populations from the Chukchi and Beaufort seas, Arctic Ocean

During the 2010–2011 ‘Impacts of Climate Change on the EcoSystems and Chemistry of the Arctic Pacific Environment’ project, we measured photosynthetic parameters in natural Arctic phytoplankton assemblages from the Chukchi and Beaufort seas. Water‐column samples were taken from the near surface (3.1 ± 0.9 m) and subsurface (28 ± 10.3 m) at ∼ 85 stations each year representing a wide range of ecological conditions, including under sea ice (UI) and in open water (OW). The physiological response of phytoplankton to light was used to assess photo‐acclimation, photosynthetic efficiency, and maximum chlorophyll a (Chl a) normalized rates of carbon fixation. Phytoplankton from the subsurface were acclimated to lower irradiance, as evidenced by higher photosynthetic efficiencies (α*), reduced mean absorption spectra (ā*) associated with heavy pigment packaging, higher maximum quantum yields of photosynthesis (Φm), increased Chl a content (Chl a : POC), and higher potential growth rates (μm) than surface samples. In addition, phytoplankton growing in the UI subsurface had higher μm, increased Φm, and higher Chl a content, as well as reduced ā* compared with those found in OW. P*m did not vary between habitats despite vastly different nutrient and light conditions (averaging ∼ 1 mg C mg−1 Chl a h−1), except where nitrate exceeded &gt; 10 mg m−3, in which case P*m averaged 5–6 mg C mg−1 Chl a h−1. Results from a stepwise regression analysis of photosynthetic parameters vs. environmental factors indicate that the concentration of inorganic nitrogen (significant relationships with P*m, α*, Φm, μm, and Chl a : POC) and temperature at sample depth (a strong indicator of habitat type; significant relationship with β*, ā*, Φm, μm, and Chl a : POC) are the best predictors of photosynthetic variables. In addition, the amount of light available at sample depth significantly predicted both Ek and Chl a : POC. Our results suggest that it is the balance between light and nutrient availability in the various environments encountered in the seasonal sea ice zone that result in the pattern of photo‐physiological data presented here. A significant proportion of primary production has now been observed to occur under the sea ice; therefore, our results may be a change from prior conditions in the region.