Vibrational modes of water predict spectral niches for photosynthesis in lakes and oceans.

Stretching and bending vibrations of water molecules absorb photons of specific wavelengths, a phenomenon that constrains light energy available for aquatic photosynthesis. Previous work suggested that these absorption properties of water create a series of spectral niches but the theory was still too simplified to enable prediction of the spectral niches in real aquatic ecosystems. Here, we show with a state-of-the-art radiative transfer model that the vibrational modes of the water molecule delineate five spectral niches, in the violet, blue, green, orange and red parts of the spectrum. These five niches are effectively captured by chlorophylls and phycobilin pigments of cyanobacteria and their eukaryotic descendants. Global distributions of the spectral niches are predicted by satellite remote sensing and validated with observed large-scale distribution patterns of cyanobacterial pigment types. Our findings provide an elegant explanation for the biogeographical distributions of photosynthetic pigments across the lakes and oceans of our planet.

Stable coexistence of equivalent nutrient competitors through niche differentiation in the light spectrum.

Niche-based theories and the neutral theory of biodiversity differ in their predictions of how the species composition of natural communities will respond to changes in nutrient availability. This is an issue of major environmental relevance, as many ecosystems have experienced changes in nitrogen (N) and phosphorus (P) due to anthropogenic manipulation of nutrient loading. To understand how changes in N and P limitation may impact community structure, we conducted laboratory competition experiments using a multispecies phytoplankton community sampled from the North Sea. Results showed that picocyanobacteria (Cyanobium sp.) won the competition under N limitation, while picocyanobacteria and nonmotile nanophytoplankton (Nannochloropsis sp.) coexisted at equal abundances under P limitation. Additional experiments using isolated monocultures confirmed that Cyanobium sp. depleted N to lower levels than Nannochloropsis sp., but that both species had nearly identical P requirements, suggesting a potential for neutral coexistence under P-limited conditions. Pairwise competition experiments with the two isolates seemed to support the consistency of these results, but P limitation resulted in stable species coexistence irrespective of the initial conditions rather than the random drift of species abundances predicted by neutral theory. Comparison of the light absorption spectra indicates that coexistence of the two species was stabilized through differential use of the underwater light spectrum. Our results provide an interesting experimental example of modern coexistence theory, where species were equal competitors in one niche dimension but their competitive traits differed in other niche dimensions, thus enabling stable species coexistence on a single limiting nutrient through niche differentiation in the light spectrum.

Competition for nutrients and light: testing advances in resource competition with a natural phytoplankton community.

A key challenge in ecology is to understand how nutrients and light affect the biodiversity and community structure of phytoplankton and plant communities. According to resource competition models, ratios of limiting nutrients are major determinants of species composition. At high nutrient levels, however, species interactions may shift to competition for light, which might make nutrient ratios less relevant. The "nutrient-load hypothesis" merges these two perspectives, by extending the classic model of competition for two nutrients to include competition for light. Here, we test five key predictions of the nutrient-load hypothesis using multispecies competition experiments. A marine phytoplankton community sampled from the North Sea was inoculated in laboratory chemostats provided with different nitrogen (N) and phosphorus (P) loads to induce either single resource limitation or co-limitation of N, P, and light. Four of the five predictions were validated by the experiments. In particular, different resource limitations favored the dominance of different species. Increasing nutrient loads caused changes in phytoplankton species composition, even if the N:P ratio of the nutrient loads remained constant, by shifting the species interactions from competition for nutrients to competition for light. In all treatments, small species became dominant whereas larger species were competitively excluded, supporting the common view that small cell size provides a competitive advantage under resource-limited conditions. Contrary to expectation, all treatments led to coexistence of diatoms, cyanobacteria and green algae, resulting in a higher diversity of species than predicted by theory. Because the coexisting species comprised three phyla with different photosynthetic pigments, we speculate that niche differentiation in the light spectrum might play a role. Our results show that mechanistic resource competition models that integrate nutrient-based and light-based approaches provide an important step forward to understand and predict how changing nutrient loads affect community composition.

From Ecological Stoichiometry to Biochemical Composition: Variation in N and P Supply Alters Key Biosynthetic Rates in Marine Phytoplankton.

One of the major challenges in ecological stoichiometry is to establish how environmental changes in resource availability may affect both the biochemical composition of organisms and the species composition of communities. This is a pressing issue in many coastal waters, where anthropogenic activities have caused large changes in riverine nutrient inputs. Here we investigate variation in the biochemical composition and synthesis of amino acids, fatty acids (FA), and carbohydrates in mixed phytoplankton communities sampled from the North Sea. The communities were cultured in chemostats supplied with different concentrations of dissolved inorganic nitrogen (DIN) and phosphorus (DIP) to establish four different types of resource limitations. Diatoms dominated under N-limited, N+P limited and P-limited conditions. Cyanobacteria became dominant in one of the N-limited chemostats and green algae dominated in the one P-limited chemostat and under light-limited conditions. Changes in nutrient availability directly affected amino acid content, which was lowest under N and N+P limitation, higher under P-limitation and highest when light was the limiting factor. Storage carbohydrate content showed the opposite trend and storage FA content seemed to be co-dependent on community composition. The synthesis of essential amino acids was affected under N and N+P limitation, as the transformation from non-essential to essential amino acids decreased at DIN:DIP ≤ 6. The simple community structure and clearly identifiable nutrient limitations confirm and clarify previous field findings in the North Sea. Our results show that different phytoplankton groups are capable of adapting their key biosynthetic rates and hence their biochemical composition to different degrees when experiencing shifts in nutrient availability. This will have implications for phytoplankton growth, community structure, and the nutritional quality of phytoplankton as food for higher trophic levels.

Competition between cyanobacteria and green algae at low versus elevated CO2: who will win, and why?

Traditionally, it has often been hypothesized that cyanobacteria are superior competitors at low CO2 and high pH in comparison with eukaryotic algae, owing to their effective CO2-concentrating mechanism (CCM). However, recent work indicates that green algae can also have a sophisticated CCM tuned to low CO2 levels. Conversely, cyanobacteria with the high-flux bicarbonate uptake system BicA appear well adapted to high inorganic carbon concentrations. To investigate these ideas we studied competition between three species of green algae and a bicA strain of the harmful cyanobacterium Microcystis aeruginosa at low (100 ppm) and high (2000 ppm) CO2. Two of the green algae were competitively superior to the cyanobacterium at low CO2, whereas the cyanobacterium increased its competitive ability with respect to the green algae at high CO2. The experiments were supported by a resource competition model linking the population dynamics of the phytoplankton species with dynamic changes in carbon speciation, pH and light. Our results show (i) that competition between phytoplankton species at different CO2 levels can be predicted from species traits in monoculture, (ii) that green algae can be strong competitors under CO2-depleted conditions, and (iii) that bloom-forming cyanobacteria with high-flux bicarbonate uptake systems will benefit from elevated CO2 concentrations.

Competition and facilitation between the marine nitrogen-fixing cyanobacterium Cyanothece and its associated bacterial community.

N2-fixing cyanobacteria represent a major source of new nitrogen and carbon for marine microbial communities, but little is known about their ecological interactions with associated microbiota. In this study we investigated the interactions between the unicellular N2-fixing cyanobacterium Cyanothece sp. Miami BG043511 and its associated free-living chemotrophic bacteria at different concentrations of nitrate and dissolved organic carbon and different temperatures. High temperature strongly stimulated the growth of Cyanothece, but had less effect on the growth and community composition of the chemotrophic bacteria. Conversely, nitrate and carbon addition did not significantly increase the abundance of Cyanothece, but strongly affected the abundance and species composition of the associated chemotrophic bacteria. In nitrate-free medium the associated bacterial community was co-dominated by the putative diazotroph Mesorhizobium and the putative aerobic anoxygenic phototroph Erythrobacter and after addition of organic carbon also by the Flavobacterium Muricauda. Addition of nitrate shifted the composition toward co-dominance by Erythrobacter and the Gammaproteobacterium Marinobacter. Our results indicate that Cyanothece modified the species composition of its associated bacteria through a combination of competition and facilitation. Furthermore, within the bacterial community, niche differentiation appeared to play an important role, contributing to the coexistence of a variety of different functional groups. An important implication of these findings is that changes in nitrogen and carbon availability due to, e.g., eutrophication and climate change are likely to have a major impact on the species composition of the bacterial community associated with N2-fixing cyanobacteria.

Termination of a toxic Alexandrium bloom with hydrogen peroxide.

The dinoflagellate Alexandrium ostenfeldii is a well-known harmful algal species that can potentially cause paralytic shellfish poisoning (PSP). Usually A. ostenfeldii occurs in low background concentrations only, but in August of 2012 an exceptionally dense bloom of more than 1millioncellsL-1 occurred in the brackish Ouwerkerkse Kreek in The Netherlands. The A. ostenfeldii bloom produced both saxitoxins and spirolides, and is held responsible for the death of a dog with a high saxitoxin stomach content. The Ouwerkerkse Kreek routinely discharges its water into the adjacent Oosterschelde estuary, and an immediate reduction of the bloom was required to avoid contamination of extensive shellfish grounds. Previously, treatment of infected waters with hydrogen peroxide (H2O2) successfully suppressed cyanobacterial blooms in lakes. Therefore, we adapted this treatment to eradicate the Alexandrium bloom using a three-step approach. First, we investigated the required H2O2 dosage in laboratory experiments with A. ostenfeldii. Second, we tested the method in a small, isolated canal adjacent to the Ouwerkerkse Kreek. Finally, we brought 50mgL-1 of H2O2 into the entire creek system with a special device, called a water harrow, for optimal dispersal of the added H2O2. Concentrations of both vegetative cells and pellicle cysts declined by 99.8% within 48h, and PSP toxin concentrations in the water were reduced below local regulatory levels of 15µgL-1. Zooplankton were strongly affected by the H2O2 treatment, but impacts on macroinvertebrates and fish were minimal. A key advantage of this method is that the added H2O2 decays to water and oxygen within a few days, which enables rapid recovery of the system after the treatment. This is the first successful field application of H2O2 to suppress a marine harmful algal bloom, although Alexandrium spp. reoccurred at lower concentrations in the following year. The results show that H2O2 treatment provides an effective emergency management option to mitigate toxic Alexandrium blooms, especially when immediate action is required.

Low temperature delays timing and enhances the cost of nitrogen fixation in the unicellular cyanobacterium Cyanothece.

Marine nitrogen-fixing cyanobacteria are largely confined to the tropical and subtropical ocean. It has been argued that their global biogeographical distribution reflects the physiologically feasible temperature range at which they can perform nitrogen fixation. In this study we refine this line of argumentation for the globally important group of unicellular diazotrophic cyanobacteria, and pose the following two hypotheses: (i) nitrogen fixation is limited by nitrogenase activity at low temperature and by oxygen diffusion at high temperature, which is manifested by a shift from strong to weak temperature dependence of nitrogenase activity, and (ii) high respiration rates are required to maintain very low levels of oxygen for nitrogenase, which results in enhanced respiratory cost per molecule of fixed nitrogen at low temperature. We tested these hypotheses in laboratory experiments with the unicellular cyanobacterium Cyanothece sp. BG043511. In line with the first hypothesis, the specific growth rate increased strongly with temperature from 18 to 30 °C, but leveled off at higher temperature under nitrogen-fixing conditions. As predicted by the second hypothesis, the respiratory cost of nitrogen fixation and also the cellular C:N ratio rose sharply at temperatures below 21 °C. In addition, we found that low temperature caused a strong delay in the onset of the nocturnal nitrogenase activity, which shortened the remaining nighttime available for nitrogen fixation. Together, these results point at a lower temperature limit for unicellular nitrogen-fixing cyanobacteria, which offers an explanation for their (sub)tropical distribution and suggests expansion of their biogeographical range by global warming.

The nutrient-load hypothesis: patterns of resource limitation and community structure driven by competition for nutrients and light.

Resource competition theory predicts that the outcome of competition for two nutrients depends on the ratio at which these nutrients are supplied. Yet there is considerable debate whether nutrient ratios or absolute nutrient loads determine the species composition of phytoplankton and plant communities. Here we extend the classical resource competition model for two nutrients by including light as additional resource. Our results suggest the nutrient-load hypothesis, which predicts that nutrient ratios determine the species composition in oligotrophic environments, whereas nutrient loads are decisive in eutrophic environments. The underlying mechanism is that nutrient enrichment shifts the species interactions from competition for nutrients to competition for light, which favors the dominance of superior light competitors overshadowing all other species. Intermediate nutrient loads can generate high biodiversity through a fine-grained patchwork of two-species and three-species coexistence equilibria. Depending on the species traits, however, competition for nutrients and light may also produce multiple alternative stable states, suppressing the predictability of the species composition. The nutrient-load hypothesis offers a solution for several discrepancies between classical resource competition theory and field observations, explains why eutrophication often leads to diversity loss, and provides a simple conceptual framework for patterns of biodiversity and community structure observed in nature.

Large-scale biodiversity patterns in freshwater phytoplankton.

Our planet shows striking gradients in the species richness of plants and animals, from high biodiversity in the tropics to low biodiversity in polar and high-mountain regions. Recently, similar patterns have been described for some groups of microorganisms, but the large-scale biogeographical distribution of freshwater phytoplankton diversity is still largely unknown. We examined the species diversity of freshwater phytoplankton sampled from 540 lakes and reservoirs distributed across the continental United States and found strong latitudinal, longitudinal, and altitudinal gradients in phytoplankton biodiversity, demonstrating that microorganisms can show substantial geographic variation in biodiversity. Detailed analysis using structural equation models indicated that these large-scale biodiversity gradients in freshwater phytoplankton diversity were mainly driven by local environmental factors, although there were residual direct effects of latitude, longitude, and altitude as well. Specifically, we found that phytoplankton species richness was an increasing saturating function of lake chlorophyll a concentration, increased with lake surface area and possibly increased with water temperature, resembling effects of productivity, habitat area, and temperature on diversity patterns commonly observed for macroorganisms. In turn, these local environmental factors varied along latitudinal, longitudinal, and altitudinal gradients. These results imply that changes in land use or climate that affect these local environmental factors are likely to have major impacts on large-scale biodiversity patterns of freshwater phytoplankton.

Evolution of nutrient uptake reveals a trade-off in the ecological stoichiometry of plant-herbivore interactions.

Nutrient limitation determines the primary production and species composition of many ecosystems. Here we apply an adaptive dynamics approach to investigate evolution of the ecological stoichiometry of primary producers and its implications for plant-herbivore interactions. The model predicts a trade-off between the competitive ability and grazing susceptibility of primary producers, driven by changes in their nutrient uptake rates. High nutrient uptake rates enhance the competitiveness of primary producers but also increase their nutritional quality for herbivores. This trade-off enables coexistence of nutrient exploiters and grazing avoiders. If herbivores are not selective, evolution favors runaway selection toward high nutrient uptake rates of the primary producers. However, if herbivores select nutritious food, the model predicts an evolutionarily stable strategy with lower nutrient uptake rates. When the model is parameterized for phytoplankton and zooplankton, the evolutionary dynamics result in plant-herbivore oscillations at ecological timescales, especially in environments with high nutrient availability and low selectivity of the herbivores. High herbivore selectivity stabilizes the community dynamics. These model predictions show that evolution permits nonequilibrium dynamics in plant-herbivore communities and shed new light on the evolutionary forces that shape the ecological stoichiometry of primary producers.

The timescale of phenotypic plasticity and its impact on competition in fluctuating environments.

Although phenotypic plasticity can be advantageous in fluctuating environments, it may come too late if the environment changes fast. Complementary chromatic adaptation is a colorful form of phenotypic plasticity, where cyanobacteria tune their pigmentation to the prevailing light spectrum. Here, we study the timescale of chromatic adaptation and its impact on competition among phytoplankton species exposed to fluctuating light colors. We parameterized a resource competition model using monoculture experiments with green and red picocyanobacteria and the cyanobacterium Pseudanabaena, which can change its color within approximately 7 days by chromatic adaptation. The model predictions were tested in competition experiments, where the incident light color switched between red and green at different frequencies (slow, intermediate, and fast). Pseudanabaena (the flexible phenotype) competitively excluded the green and red picocyanobacteria in all competition experiments. Strikingly, the rate of competitive exclusion was much faster when the flexible phenotype had sufficient time to fully adjust its pigmentation. Thus, the flexible phenotype benefited from its phenotypic plasticity if fluctuations in light color were relatively slow, corresponding to slow mixing processes or infrequent storms in their natural habitat. This shows that the timescale of phenotypic plasticity plays a key role during species interactions in fluctuating environments.

Widespread distribution of proteorhodopsins in freshwater and brackish ecosystems.

Proteorhodopsins (PRs) are light-driven proton pumps that have been found in a variety of marine environments. The goal of this study was to search for PR presence in different freshwater and brackish environments and to explore the diversity of non-marine PR protein. Here, we show that PRs exist in distinctly different aquatic environments, ranging from clear water lakes to peat lakes and in the Baltic Sea. Some of the PRs observed in this study formed unique clades that were not previously observed in marine environments, whereas others were similar to PRs found in non-marine samples of the Global Ocean Sampling (GOS) expedition. Furthermore, the similarity of several PRs isolated from lakes in different parts of the world suggests that these genes are dispersed globally and that they may encode unique functional capabilities enabling successful competition in a wide range of freshwater environments. Phylogenomic analysis of genes found on these GOS scaffolds suggests that some of the freshwater PRs are found in freshwater Flavobacteria and freshwater SAR11-like bacteria.

Diversity and phylogeny of Baltic Sea picocyanobacteria inferred from their ITS and phycobiliprotein operons.

Picocyanobacteria of the genus Synechococcus span a range of different colours, from red strains rich in phycoerythrin (PE) to green strains rich in phycocyanin (PC). Here, we show that coexistence of red and green picocyanobacteria in the Baltic Sea is widespread. The diversity and phylogeny of red and green picocyanobacteria was analysed using three different genes: 16S rRNA-ITS, the cpeBA operon of the red PE pigment and the cpcBA operon of the green PC pigment. Sequencing of 209 clones showed that Baltic Sea picocyanobacteria exhibit high levels of microdiversity. The partial nucleotide sequences of the cpcBA and cpeBA operons from the clone libraries of the Baltic Sea revealed two distinct phylogenetic clades: one clade containing mainly sequences from cultured PC-rich picocyanobacteria, while the other contains only sequences from cultivated PE-rich strains. A third clade of phycourobilin (PUB) containing strains of PE-rich Synechococcus spp. did not contain sequences from the Baltic Sea clone libraries. These findings differ from previously published phylogenies based on 16S rRNA gene analysis. Our data suggest that, in terms of their pigmentation, Synechococcus spp. represent three different lineages occupying different ecological niches in the underwater light spectrum. Strains from different lineages can coexist in light environments that overlap with their light absorption spectra.

Colorful niches of phototrophic microorganisms shaped by vibrations of the water molecule.

The photosynthetic pigments of phototrophic microorganisms cover different regions of the solar light spectrum. Utilization of the light spectrum can be interpreted in terms of classical niche theory, as the light spectrum offers opportunities for niche differentiation and allows coexistence of species absorbing different colors of light. However, which spectral niches are available for phototrophic microorganisms? Here, we show that the answer is hidden in the vibrations of the water molecule. Water molecules absorb light at specific wavebands that match the energy required for their stretching and bending vibrations. Although light absorption at these specific wavelengths appears only as subtle shoulders in the absorption spectrum of pure water, these subtle shoulders create large gaps in the underwater light spectrum due to the exponential nature of light attenuation. Model calculations show that the wavebands between these gaps define a series of distinct niches in the underwater light spectrum. Strikingly, these distinct spectral niches match the light absorption spectra of the major photosynthetic pigments on our planet. This suggests that vibrations of the water molecule have played a major role in the ecology and evolution of phototrophic microorganisms.

Colourful coexistence of red and green picocyanobacteria in lakes and seas.

Hutchinson's paradox of the plankton inspired many studies on the mechanisms of species coexistence. Recent laboratory experiments showed that partitioning of white light allows stable coexistence of red and green picocyanobacteria. Here, we investigate to what extent these laboratory findings can be extrapolated to natural waters. We predict from a parameterized competition model that the underwater light colour of lakes and seas provides ample opportunities for coexistence of red and green phytoplankton species. To test this prediction, we sampled picocyanobacteria of 70 aquatic ecosystems, ranging from clear blue oceans to turbid brown peat lakes. As predicted, red picocyanobacteria dominated in clear waters, whereas green picocyanobacteria dominated in turbid waters. We found widespread coexistence of red and green picocyanobacteria in waters of intermediate turbidity. These field data support the hypothesis that niche differentiation along the light spectrum promotes phytoplankton biodiversity, thus providing a colourful solution to the paradox of the plankton.

Animal-plant-microbe interactions: direct and indirect effects of swan foraging behaviour modulate methane cycling in temperate shallow wetlands.

Wetlands are among the most important ecosystems on Earth both in terms of productivity and biodiversity, but also as a source of the greenhouse gas CH(4). Microbial processes catalyzing nutrient recycling and CH(4) production are controlled by sediment physico-chemistry, which is in turn affected by plant activity and the foraging behaviour of herbivores. We performed field and laboratory experiments to evaluate the direct effect of herbivores on soil microbial activity and their indirect effects as the consequence of reduced macrophyte density, using migratory Bewick's swans (Cygnus columbianus bewickii Yarrell) feeding on fennel pondweed (Potamogeton pectinatus L.) tubers as a model system. A controlled foraging experiment using field enclosures indicated that swan bioturbation decreases CH(4) production, through a decrease in the activity of methanogenic Archaea and an increased rate of CH(4) oxidation in the bioturbated sediment. We also found a positive correlation between tuber density (a surrogate of plant density during the previous growth season) and CH(4) production activity. A laboratory experiment showed that sediment sterilization enhances pondweed growth, probably due to elimination of the negative effects of microbial activity on plant growth. In summary, the bioturbation caused by swan grazing modulates CH(4) cycling by means of both direct and indirect (i.e. plant-mediated) effects with potential consequences for CH(4) emission from wetland systems.

Adaptive divergence in pigment composition promotes phytoplankton biodiversity.

The dazzling diversity of the phytoplankton has puzzled biologists for decades. The puzzle has been enlarged rather than solved by the progressive discovery of new phototrophic microorganisms in the oceans, including picocyanobacteria, pico-eukaryotes, and bacteriochlorophyll-based and rhodopsin-based phototrophic bacteria. Physiological and genomic studies suggest that natural selection promotes niche differentiation among these phototrophic microorganisms, particularly with respect to their photosynthetic characteristics. We have analysed competition for light between two closely related picocyanobacteria of the Synechococcus group that we isolated from the Baltic Sea. One of these two has a red colour because it contains the pigment phycoerythrin, whereas the other is blue-green because it contains high contents of the pigment phycocyanin. Here we report theory and competition experiments that reveal stable coexistence of the two picocyanobacteria, owing to partitioning of the light spectrum. Further competition experiments with a third marine cyanobacterium, capable of adapting its pigment composition, show that this species persists by investing in the pigment that absorbs the colour not used by its competitors. These results demonstrate the adaptive significance of divergence in pigment composition of phototrophic microorganisms, which allows an efficient utilization of light energy and favours species coexistence.