Why do coccolithophores calcify? Does the calcium carbonate shell serve as protection against viral infection and predation?

Coccolithophores are an important group of marine phytoplankton that are characterized by their ability to precipitate calcium carbonate. The single cells form small calcite plates (coccoliths), which are arranged on the cell surface in form of a spherical coating, called coccosphere. Coccolithophores account for a significant proportion of the marine primary production and are among the most important calcifying organisms in the ocean, thus having a significant impact on the marine carbon cycle. However, it is not known in what way their ability to calcify contributes to their ecological success, as the question of why coccolithophores calcify remains unanswered. Probably the most obvious theory is that the coccosphere provides protection against natural predators, the most relevant of which are viruses, microzooplankton (unicellular protists), and mesozooplankton (metazoan predators). By means of laboratory experiments, this work investigated whether the coccosphere of certain species provides protection against infection with a virus, a phagotrophic protozoan, and a copepod. The results show that the coccosphere does not prevent infection with the specific virus and reveal complex infection dynamics in the investigated host-virus system. It is further shown that the coccosphere does not protect against grazing by a certain copepod species. Experiments with a phagotrophic protozoan showed that the coccosphere affects food uptake and growth of the predator, but does not cause the grazer to avoid ingesting coccolithophores and to select non-calcified cells that were offered at the same time. The results raise the questions whether other microzooplankton predators that naturally co-occur with coccolithophores are able to select against calcifying cells, and whether the effect of calcification on the growth of nonselective protozoa provides a benefit for coccolithophores

Why do coccolithophores calcify? Does the calcium carbonate shell serve as protection against viral infection and predation?

Coccolithophores are an important group of marine phytoplankton that are characterized by their ability to precipitate calcium carbonate. The single cells form small calcite plates (coccoliths), which are arranged on the cell surface in form of a spherical coating, called coccosphere. Coccolithophores account for a significant proportion of the marine primary production and are among the most important calcifying organisms in the ocean, thus having a significant impact on the marine carbon cycle. However, it is not known in what way their ability to calcify contributes to their ecological success, as the question of why coccolithophores calcify remains unanswered. Probably the most obvious theory is that the coccosphere provides protection against natural predators, the most relevant of which are viruses, microzooplankton (unicellular protists), and mesozooplankton (metazoan predators). By means of laboratory experiments, this work investigated whether the coccosphere of certain species provides protection against infection with a virus, a phagotrophic protozoan, and a copepod. The results show that the coccosphere does not prevent infection with the specific virus and reveal complex infection dynamics in the investigated host-virus system. It is further shown that the coccosphere does not protect against grazing by a certain copepod species. Experiments with a phagotrophic protozoan showed that the coccosphere affects food uptake and growth of the predator, but does not cause the grazer to avoid ingesting coccolithophores and to select non-calcified cells that were offered at the same time. The results raise the questions whether other microzooplankton predators that naturally co-occur with coccolithophores are able to select against calcifying cells, and whether the effect of calcification on the growth of nonselective protozoa provides a benefit for coccolithophores

The Calcium Carbonate Shell of Emiliania huxleyi Provides Limited Protection Against Viral Infection

Coccolithophores are an important group of marine phytoplankton which cover themselves with the coccosphere – a shell composed of numerous calcium carbonate (CaCO3) platelets. Despite more than a century of coccolithophore research, it remains speculative why coccolithophores calcify. Resolving this question is essential to assess the competitive fitness of coccolithophores in the future ocean where changes in calcification are expected. Here, we used the Emiliania huxleyi – Emiliania huxleyi Virus 86 host-virus model system to test the hypothesis that the coccosphere serves as a physical barrier reducing viral infection. Therefore, we removed the coccosphere from living E. huxleyi cells and compared the infection progress relative to calcified cells in a series of 6 experiments under different growth conditions. We found that the coccosphere does not constitute an effective physical barrier against viral penetration, since non-growing calcified cells were susceptible to viral infection and lysis (growth stopped by light limitation). However, we also found that protection against the virus may depend on the daily growth cycle. E. huxleyi reached higher peak abundances when decalcified cells were allowed to rebuild their coccosphere before entering cell division phase and being exposed to the virus, thereby suggesting that rates of viral infection could be reduced by the coccosphere during the critical phase in the cell cycle. However, the benefit of this potential protection is arguably of limited ecological significance since the concentrations of both, calcified and decalcified E. huxleyi approached similar values until the end of the bloom. We conclude that the coccosphere provides at best a limited protection against infection with the EhV86

Influence of ocean acidification on plankton community structure during a winter-to-summer succession: An imaging approach indicates that copepods can benefit from elevated CO2 via indirect food web effects

Plankton communities play a key role in the marine food web and are expected to be highly sensitive to ongoing environmental change. Oceanic uptake of anthropogenic carbon dioxide (CO2) causes pronounced shifts in marine carbonate chemistry and a decrease in seawater pH. These changes–summarized by the term ocean acidification (OA)–can significantly affect the physiology of planktonic organisms. However, studies on the response of entire plankton communities to OA, which also include indirect effects via food-web interactions, are still relatively rare. Thus, it is presently unclear how OA could affect the functioning of entire ecosystems and biogeochemical element cycles. In this study, we report from a long-term in situ mesocosm experiment, where we investigated the response of natural plankton communities in temperate waters (Gullmarfjord, Sweden) to elevated CO2 concentrations and OA as expected for the end of the century (~760 μatm pCO2). Based on a plankton-imaging approach, we examined size structure, community composition and food web characteristics of the whole plankton assemblage, ranging from picoplankton to mesozooplankton, during an entire winter-to-summer succession. The plankton imaging system revealed pronounced temporal changes in the size structure of the copepod community over the course of the plankton bloom. The observed shift towards smaller individuals resulted in an overall decrease of copepod biomass by 25%, despite increasing numerical abundances. Furthermore, we observed distinct effects of elevated CO2 on biomass and size structure of the entire plankton community. Notably, the biomass of copepods, dominated by Pseudocalanus acuspes, displayed a tendency towards elevated biomass by up to 30–40% under simulated ocean acidification. This effect was significant for certain copepod size classes and was most likely driven by CO2-stimulated responses of primary producers and a complex interplay of trophic interactions that allowed this CO2 effect to propagate up the food web. Such OA-induced shifts in plankton community structure could have far-reaching consequences for food-web interactions, biomass transfer to higher trophic levels and biogeochemical cycling of marine ecosystems

No observed effect of ocean acidification on nitrogen biogeochemistry in a summer Baltic Sea plankton community

Nitrogen fixation by filamentous cyanobacteria supplies significant amounts of new nitrogen (N) to the Baltic Sea. This balances N loss processes such as denitrification and anammox, and forms an important N source supporting primary and secondary production in N-limited post-spring bloom plankton communities. Laboratory studies suggest that filamentous diazotrophic cyanobacteria growth and N2-fixation rates are sensitive to ocean acidification, with potential implications for new N supply to the Baltic Sea. In this study, our aim was to assess the effect of ocean acidification on diazotroph growth and activity as well as the contribution of diazotrophically fixed N to N supply in a natural plankton assemblage. We enclosed a natural plankton community in a summer season in the Baltic Sea near the entrance to the Gulf of Finland in six large-scale mesocosms (volume ??55?m3) and manipulated fCO2 over a range relevant for projected ocean acidification by the end of this century (average treatment fCO2: 365–1231?µatm). The direct response of diazotroph growth and activity was followed in the mesocosms over a 47 day study period during N-limited growth in the summer plankton community. Diazotrophic filamentous cyanobacteria abundance throughout the study period and N2-fixation rates (determined only until day 21 due to subsequent use of contaminated commercial 15N-N2 gas stocks) remained low. Thus estimated new N inputs from diazotrophy were too low to relieve N limitation and stimulate a summer phytoplankton bloom. Instead, regeneration of organic N sources likely sustained growth in the plankton community. We could not detect significant CO2-related differences in neither inorganic nor organic N pool sizes, or particulate matter N?:?P stoichiometry. Additionally, no significant effect of elevated CO2 on diazotroph activity was observed. Therefore, ocean acidification had no observable impact on N cycling or biogeochemistry in this N-limited, post-spring bloom plankton assemblage in the Baltic Sea

No observed effect of ocean acidification on nitrogen biogeochemistry in a summer Baltic Sea plankton community

Nitrogen fixation by filamentous cyanobacteria supplies significant amounts of new nitrogen (N) to the Baltic Sea. This balances N loss processes such as denitrification and anammox and forms an important N source supporting primary and secondary production in N-limited post-spring bloom plankton communities. Laboratory studies suggest that filamentous diazotrophic cyanobacteria growth and N2-fixation rates are sensitive to ocean acidification with potential implications for new N supply to the Baltic Sea. In this study, our aim was to assess the effect of ocean acidification on diazotroph growth and activity as well as the contribution of diazotrophically-fixed N to N supply in a natural plankton assemblage. We enclosed a natural plankton community in a summer season in the Baltic Sea near the entrance to the Gulf of Finland in six large-scale mesocosms (volume ~ 55 m3) and manipulated fCO2 over a range relevant for projected ocean acidification by the end of this century (average treatment fCO2: 365–1231 μatm). The direct response of diazotroph growth and activity was followed in the mesocosms over a 47 day study period during N-limited growth in the summer plankton community. Diazotrophic filamentous cyanobacteria abundance throughout the study period and N2-fixation rates (determined only until day 21 due to subsequent use of contaminated commercial 15N-N2 gas stocks) remained low. Thus estimated new N inputs from diazotrophy were too low to relieve N limitation and stimulate a summer phytoplankton bloom. Instead regeneration of organic N sources likely sustained growth in the plankton community. We could not detect significant CO2-related differences in inorganic or organic N pools sizes, or particulate matter N : P stoichiometry. Additionally, no significant effect of elevated CO2 on diazotroph activity was observed. Therefore, ocean acidification had no observable impact on N cycling or biogeochemistry in this N-limited, post-spring bloom plankton assemblage in the Baltic Sea

Enhanced transfer of organic matter to higher trophic levels caused by ocean acidification and its implications for export production : A mass balance approach

Ongoing acidification of the ocean through uptake of anthropogenic CO2 is known to affect marine biota and ecosystems with largely unknown consequences for marine food webs. Changes in food web structure have the potential to alter trophic transfer, partitioning, and biogeochemical cycling of elements in the ocean. Here we investigated the impact of realistic end-of-the-century CO2 concentrations on the development and partitioning of the carbon, nitrogen, phosphorus, and silica pools in a coastal pelagic ecosystem (Gullmar Fjord, Sweden). We covered the entire winter-to-summer plankton succession (100 days) in two sets of five pelagic mesocosms, with one set being CO2 enriched (similar to 760 mu atm pCO(2)) and the other one left at ambient CO2 concentrations. Elemental mass balances were calculated and we highlight important challenges and uncertainties we have faced in the closed mesocosm system. Our key observations under high CO2 were: (1) A significantly amplified transfer of carbon, nitrogen, and phosphorus from primary producers to higher trophic levels, during times of regenerated primary production. (2) A prolonged retention of all three elements in the pelagic food web that significantly reduced nitrogen and phosphorus sedimentation by about 11 and 9%, respectively. (3) A positive trend in carbon fixation (relative to nitrogen) that appeared in the particulate matter pool as well as the downward particle flux. This excess carbon counteracted a potential reduction in carbon sedimentation that could have been expected from patterns of nitrogen and phosphorus fluxes. Our findings highlight the potential for ocean acidification to alter partitioning and cycling of carbon and nutrients in the surface ocean but also show that impacts are temporarily variable and likely depending upon the structure of the plankton food web.Peer reviewe

Factors controlling plankton community production, export flux, and particulate matter stoichiometry in the coastal upwelling system off Peru

Eastern boundary upwelling systems (EBUS) are among the most productive marine ecosystems on Earth. The production of organic material is fueled by upwelling of nutrient-rich deep waters and high incident light at the sea surface. However, biotic and abiotic factors can modify surface production and related biogeochemical processes. Determining these factors is important because EBUS are considered hotspots of climate change, and reliable predictions of their future functioning requires understanding of the mechanisms driving the biogeochemical cycles therein. In this field experiment, we used in situ mesocosms as tools to improve our mechanistic understanding of processes controlling organic matter cycling in the coastal Peruvian upwelling system. Eight mesocosms, each with a volume of ∼55 m3, were deployed for 50 d ∼6 km off Callao (12∘ S) during austral summer 2017, coinciding with a coastal El Niño phase. After mesocosm deployment, we collected subsurface waters at two different locations in the regional oxygen minimum zone (OMZ) and injected these into four mesocosms (mixing ratio ≈1.5 : 1 mesocosm: OMZ water). The focus of this paper is on temporal developments of organic matter production, export, and stoichiometry in the individual mesocosms. The mesocosm phytoplankton communities were initially dominated by diatoms but shifted towards a pronounced dominance of the mixotrophic dinoflagellate (Akashiwo sanguinea) when inorganic nitrogen was exhausted in surface layers. The community shift coincided with a short-term increase in production during the A. sanguinea bloom, which left a pronounced imprint on organic matter C : N : P stoichiometry. However, C, N, and P export fluxes did not increase because A. sanguinea persisted in the water column and did not sink out during the experiment. Accordingly, export fluxes during the study were decoupled from surface production and sustained by the remaining plankton community. Overall, biogeochemical pools and fluxes were surprisingly constant for most of the experiment. We explain this constancy by light limitation through self-shading by phytoplankton and by inorganic nitrogen limitation which constrained phytoplankton growth. Thus, gain and loss processes remained balanced and there were few opportunities for blooms, which represents an event where the system becomes unbalanced. Overall, our mesocosm study revealed some key links between ecological and biogeochemical processes for one of the most economically important regions in the oceans

Influence of Ocean Acidification on a Natural Winter-to-Summer Plankton Succession : First Insights from a Long-Term Mesocosm Study Draw Attention to Periods of Low Nutrient Concentrations

Every year, the oceans absorb about 30% of anthropogenic carbon dioxide (CO2) leading to a re-equilibration of the marine carbonate system and decreasing seawater pH. Today, there is increasing awareness that these changes-summarized by the term ocean acidification (OA)-could differentially affect the competitive ability of marine organisms, thereby provoking a restructuring of marine ecosystems and biogeochemical element cycles. In winter 2013, we deployed ten pelagic mesocosms in the Gullmar Fjord at the Swedish west coast in order to study the effect of OA on plankton ecology and biogeochemistry under close to natural conditions. Five of the ten mesocosms were left unperturbed and served as controls (similar to 380 mu atm pCO(2)), whereas the others were enriched with CO2-saturated water to simulate realistic end-of-the-century carbonate chemistry conditions (mu 760 mu atm pCO(2)). We ran the experiment for 113 days which allowed us to study the influence of high CO2 on an entire winter-to-summer plankton succession and to investigate the potential of some plankton organisms for evolutionary adaptation to OA in their natural environment. This paper is the first in a PLOS collection and provides a detailed overview on the experimental design, important events, and the key complexities of such a "long-term mesocosm" approach. Furthermore, we analyzed whether simulated end-of-the-century carbonate chemistry conditions could lead to a significant restructuring of the plankton community in the course of the succession. At the level of detail analyzed in this overview paper we found that CO2-induced differences in plankton community composition were non-detectable during most of the succession except for a period where a phytoplankton bloom was fueled by remineralized nutrients. These results indicate: (1) Long-term studies with pelagic ecosystems are necessary to uncover OA-sensitive stages of succession. (2) Plankton communities fueled by regenerated nutrients may be more responsive to changing carbonate chemistry than those having access to high inorganic nutrient concentrations and may deserve particular attention in future studies.Peer reviewe