Terje Berge

Phytoplankton growth after a century of dormancy illuminates past resilience to catastrophic darkness

Photosynthesis evolved in the oceans more than 3 billion years ago and has persisted throughout all major extinction events in Earths history. The most recent of such events is linked to an abrupt collapse of primary production due to darkness following the Chicxulub asteroid impact 65.5 million years ago. Coastal phytoplankton groups (particularly dinoflagellates and diatoms) appear to have been resilient to this biotic crisis, but the reason for their high survival rates is still unknown. Here we show that the growth performance of dinoflagellate cells germinated from resting stages is unaffected by up to a century of dormancy. Our results clearly indicate that phytoplankton resting stages can endure periods of darkness far exceeding those estimated for the Cretaceous-Paleogene extinction and may effectively aid the rapid resurgence of primary production in coastal areas after events of prolonged photosynthesis shut-down.

Marine microalgae attack and feed on metazoans

Free-living microalgae from the dinoflagellate genus Karlodinium are known to form massive blooms in eutrophic coastal waters worldwide and are often associated with fish kills. Natural bloom populations, recently shown to consist of the two mixotrophic and toxic species Karlodinium armiger and Karlodinium veneficum have caused fast paralysis and mortality of finfish and copepods in the laboratory, and have been associated with reduced metazooplankton biomass in-situ. Here we show that a strain of K. armiger (K-0688) immobilises the common marine copepod Acartia tonsa in a density-dependent manner and collectively ingests the grazer to promote its own growth rate. In contrast, four strains of K. veneficum did not attack or affect the motility and survival of the copepods. Copepod immobilisation by the K. armiger strain was fast (within 15 min) and caused by attacks of swarming cells, likely through the transfer and action of a highly potent but uncharacterised neurotoxin. The copepods grazed and reproduced on a diet of K. armiger at densities below 1000, cells ml−1, but above 3500 cells ml−1 the mixotrophic dinoflagellates immobilised, fed on and killed the copepods. Switching the trophic role of the microalgae from prey to predator of copepods couples population growth to reduced grazing pressure, promoting the persistence of blooms at high densities. K. armiger also fed on three other metazoan organisms offered, suggesting that active predation by mixotrophic dinoflagellates may be directly involved in causing mortalities at several trophic levels in the marine food web.

Hundred Years of Environmental Change and Phytoplankton Ecophysiological Variability Archived in Coastal Sediments

Marine protist species have been used for several decades as environmental indicators under the assumption that their ecological requirements have remained more or less stable through time. However, a growing body of evidence suggests that marine protists, including several phytoplankton species, are in fact highly diverse and may quickly respond to changes in the environment. Predicting how future climate will impact phytoplankton populations is important, but this task has been challenged by a lack of time-series of ecophysiological parameters at time-scales relevant for climate studies (i.e. at least decadal). Here, we report on ecophysiological variability in a marine dinoflagellate over a 100-year period of well-documented environmental change, by using the sedimentary archive of living cysts from a Scandinavian fjord (Koljö Fjord, Sweden). During the past century, Koljö Fjord has experienced important changes in salinity linked to the North Atlantic Oscillation (NAO). We revived resting cysts of Pentapharsodinium dalei preserved in the fjord sediments and determined growth rates for 18 strains obtained from 3 sediment core layers at salinity 15 and 30, which represent extreme sea-surface conditions during periods of predominantly negative and positive NAO phases, respectively. Upper pH tolerance limits for growth were also tested. In general, P. dalei grew at a higher rate in salinity 30 than 15 for all layers, but there were significant differences among strains. When accounting for inter-strain variability, cyst age had no effect on growth performance or upper pH tolerance limits for this species, indicating a stable growth response over the 100-year period in spite of environmental fluctuations. Our findings give some support for the use of morphospecies in environmental studies, particularly at decadal to century scales. Furthermore, the high intra-specific variability found down to sediment layers dated as ca. 50 years-old indicates that cyst-beds of P. dalei are repositories of ecophysiological diversity.

Photoregulation in a Kleptochloroplastidic Dinoflagellate, Dinophysis acuta

Some phagotrophic organisms can retain chloroplasts of their photosynthetic prey as so-called kleptochloroplasts and maintain their function for shorter or longer periods of time. Here we show for the first time that the dinoflagellate Dinophysis acuta takes control over “third-hand” chloroplasts obtained from its ciliate prey Mesodinium spp. that originally ingested the cryptophyte chloroplasts. With its kleptochloroplasts, D. acuta can synthesize photosynthetic as well as photoprotective pigments under long-term starvation in the light. Variable chlorophyll fluorescence measurements showed that the kleptochloroplasts were fully functional during 1 month of prey starvation, while the chlorophyll a-specific inorganic carbon uptake decreased within days of prey starvation under an irradiance of 100 μmol photons m-2 s-1. While D. acuta cells can regulate their pigmentation and function of kleptochloroplasts they apparently lose the ability to maintain high inorganic carbon fixation rates.

Modeling succession of key resource-harvesting traits of mixotrophic plankton.

Unicellular eukaryotes make up the base of the ocean food web and exist as a continuum in trophic strategy from pure heterotrophy (phagotrophic zooplankton) to pure photoautotrophy (‘phytoplankton’), with a dominance of mixotrophic organisms combining both strategies. Here we formulate a trait-based model for mixotrophy with three key resource-harvesting traits: photosynthesis, phagotrophy and inorganic nutrient uptake, which predicts the trophic strategy of species throughout the seasonal cycle. Assuming that simple carbohydrates from photosynthesis fuel respiration, and feeding primarily provides building blocks for growth, the model reproduces the observed light-dependent ingestion rates and species-specific growth rates with and without prey from the laboratory. The combination of traits yielding the highest growth rate suggests high investments in photosynthesis, and inorganic nutrient uptake in the spring and increased phagotrophy during the summer, reflecting general seasonal succession patterns of temperate waters. Our trait-based model presents a simple and general approach for the inclusion of mixotrophy, succession and evolution in ecosystem models.

The blue mussel Mytilus edulis is vulnerable to the toxic dinoflagellate Karlodinium armiger—Adult filtration is inhibited and several life stages killed

Blooms of the toxic dinoflagellates Karlodinium armiger and K. veneficum are frequently observed in Alfacs Bay, Spain, causing mass mortality to wild and farmed mussels. An isolate of K. armiger from Alfacs Bay was grown in the laboratory and exposed to adults, embryos and trochophore larvae of the blue mussel, Mytilus edulis. Adult mussels rejected to filter K. armiger at cell concentrations >1.5·103 cells ml-1. Exposure of adult mussels (23–33 mm shell length) to a range of K. armiger cell concentrations led to mussel mortality with LC50 values of 9.4·103 and 6.1·103 cells ml-1 after 24 and 48 h exposure to ~3.6·104 K. armiger cells ml-1, respectively. Karlodinium armiger also affected mussel embryos and trochophore larvae and feeding by K. armiger on both embryos and larvae was observed under the microscope. Embryos exposed to low K. armiger cell concentrations suffered no measurable mortality. However, at higher K. armiger cell concentrations the mortality of the embryos increased significantly with cell concentration and reached 97% at 1.8·103 K. armiger cells ml-1 after 29 h of exposure. Natural K. armiger blooms may not only have serious direct effects on benthic communities, but may also affect the recruitment of mussels in affected areas.