Organic and inorganic nutrients modulate taxonomic diversity and trophic strategies of small eukaryotes in oligotrophic oceans.

As the oligotrophic gyres expand due to global warming, exacerbating resource limitation impacts on primary producers, predicting changes to microbial assemblages and productivity requires knowledge of the community response to nutrient availability. This study examines how organic and inorganic nutrients influence the taxonomic and trophic composition (18S metabarcoding) of small eukaryotic plankton communities (< 200 µm) within the euphotic zone of the oligotrophic Sargasso Sea. The study was conducted by means of field sampling of natural microbial communities and laboratory incubation of these communities under different nutrient regimes. Dissimilarity in community composition increased along a depth gradient, with a homogeneous protist community within the mixed layer and distinct microbial assemblages at different depths below the deep chlorophyll maximum. A nutrient enrichment assay revealed the potential of natural microbial communities to rapidly shift in composition in response to nutrient addition. Results highlighted the importance of inorganic phosphorus availability, largely understudied compared to nitrogen, in constraining microbial diversity. Dissolved organic matter addition led to a loss of diversity, benefiting a limited number of phagotrophic and mixotrophic taxa. Nutrient history of the community sets the physiological responsiveness of the eukaryotic community to changing nutrient regimes and needs to be considered in future studies.

Allometry of carbon and nitrogen content and growth rate in a diverse range of coccolithophores.

As both photoautotrophs and calcifiers, coccolithophores play important roles in ecosystems and biogeochemical cycles. Though some species form blooms in high-latitude waters, low-latitude communities exhibit high diversity and niche diversification. Despite such diversity, our understanding of the clade relies on knowledge of Emiliana huxleyi. To address this, we examine carbon (C) and nitrogen (N) content of strains (n = 9) from the main families of the calcifying Haptophyceae, as well as allometry and cell size frequency across extant species. Coccolithophore cell size is constrained, with ~71% of 159 species smaller than 10 µm in diameter. Growth rates scale with cell biovolume (µ = 1.83 × cell volume-0.19), with an exponent close to metabolic theory. Organic carbon (C) per cell is lower than for other phytoplankton, providing a coccolithophore-specific relationship between cell organic C content and biovolume (pg C cell-1 = 0.30 × cell volume0.70). Organic C to N ratios (~8.3 mol:mol) are similar to other phytoplankton, implying little additional N cost for calcification and efficient retention and recycling of cell N. Our results support observations that coccolithophores are efficient competitors in low-nutrient conditions, able to photosynthesize, calcify and run the routine metabolic machinery necessary without any additional need for N relative to noncalcifying algae.

Algal plankton turn to hunting to survive and recover from end-Cretaceous impact darkness.

The end-Cretaceous bolide impact triggered the devastation of marine ecosystems. However, the specific kill mechanism(s) are still debated, and how primary production subsequently recovered remains elusive. We used marine plankton microfossils and eco-evolutionary modeling to determine strategies for survival and recovery, finding that widespread phagotrophy (prey ingestion) was fundamental to plankton surviving the impact and also for the subsequent reestablishment of primary production. Ecological selectivity points to extreme post-impact light inhibition as the principal kill mechanism, with the marine food chain temporarily reset to a bacteria-dominated state. Subsequently, in a sunlit ocean inhabited by only rare survivor grazers but abundant small prey, it was mixotrophic nutrition (autotrophy and heterotrophy) and increasing cell sizes that enabled the eventual reestablishment of marine food webs some 2 million years later.

Warm plankton soup and red herrings: calcareous nannoplankton cellular communities and the Palaeocene-Eocene Thermal Maximum.

Past global warming events such as the Palaeocene-Eocene Thermal Maximum (PETM-56 Ma) are attributed to the release of vast amounts of carbon into the ocean, atmosphere and biosphere with recovery ascribed to a combination of silicate weathering and organic carbon burial. The phytoplanktonic nannoplankton are major contributors of organic and inorganic carbon but their role in this recovery process remains poorly understood and complicated by their contribution to marine calcification. Biocalcification is implicated not only in long-term carbon burial but also both short-term positive and negative climatic feedbacks associated with seawater buffering and responses to ocean acidification. Here, we use exceptional records of preserved fossil coccospheres to reconstruct cell size distribution, biomass production (particulate organic carbon, POC) and (particulate) inorganic carbon (PIC) yields of three contrasting nannoplankton communities (Bass River-outer shelf, Maud Rise-uppermost bathyal, Shatsky Rise-open ocean) through the PETM onset and recovery. Each of the sites shows contrasting community responses across the PETM as a function of their taxic composition and total community biomass. Our results indicate that nannoplankton PIC:POC had no role in short-term climate feedback and, as such, their importance as a source of CO2 to the environment is a red herring. It is nevertheless likely that shifts to greater numbers of smaller cells at the shelf site in particular led to greater carbon transfer efficiency, and that nannoplankton productivity and export across the shelves had a significant modulating effect on carbon sequestration during the PETM recovery.This article is part of a discussion meeting issue 'Hyperthermals: rapid and extreme global warming in our geological past'.

Geographical CO2 sensitivity of phytoplankton correlates with ocean buffer capacity.

Accumulation of anthropogenic CO2 is significantly altering ocean chemistry. A range of biological impacts resulting from this oceanic CO2 accumulation are emerging, however, the mechanisms responsible for observed differential susceptibility between organisms and across environmental settings remain obscure. A primary consequence of increased oceanic CO2 uptake is a decrease in the carbonate system buffer capacity, which characterizes the system's chemical resilience to changes in CO2 , generating the potential for enhanced variability in pCO2 and the concentration of carbonate [ CO32- ], bicarbonate [ HCO3- ], and protons [H+ ] in the future ocean. We conducted a meta-analysis of 17 shipboard manipulation experiments performed across three distinct geographical regions that encompassed a wide range of environmental conditions from European temperate seas to Arctic and Southern oceans. These data demonstrated a correlation between the magnitude of natural phytoplankton community biological responses to short-term CO2 changes and variability in the local buffer capacity across ocean basin scales. Specifically, short-term suppression of small phytoplankton (<10 µm) net growth rates were consistently observed under enhanced pCO2 within experiments performed in regions with higher ambient buffer capacity. The results further highlight the relevance of phytoplankton cell size for the impacts of enhanced pCO2 in both the modern and future ocean. Specifically, cell size-related acclimation and adaptation to regional environmental variability, as characterized by buffer capacity, likely influences interactions between primary producers and carbonate chemistry over a range of spatio-temporal scales.

Evidence for polyploidy in the globally important diazotroph Trichodesmium.

Polyploidy is a well-described trait in some prokaryotic organisms; however, it is unusual in marine microbes from oligotrophic environments, which typically display a tendency towards genome streamlining. The biogeochemically significant diazotrophic cyanobacterium Trichodesmium is a potential exception. With a relatively large genome and a comparatively high proportion of non-protein-coding DNA, Trichodesmium appears to allocate relatively more resources to genetic material than closely related organisms and microbes within the same environment. Through simultaneous analysis of gene abundance and direct cell counts, we show for the first time that Trichodesmium spp. can also be highly polyploid, containing as many as 100 genome copies per cell in field-collected samples and >600 copies per cell in laboratory cultures. These findings have implications for the widespread use of the abundance of the nifH gene (encoding a subunit of the N2-fixing enzyme nitrogenase) as an approach for quantifying the abundance and distribution of marine diazotrophs. Moreover, polyploidy may combine with the unusual genomic characteristics of this genus both in reflecting evolutionary dynamics and influencing phenotypic plasticity and ecological resilience.

Why marine phytoplankton calcify.

Calcifying marine phytoplankton-coccolithophores- are some of the most successful yet enigmatic organisms in the ocean and are at risk from global change. To better understand how they will be affected, we need to know "why" coccolithophores calcify. We review coccolithophorid evolutionary history and cell biology as well as insights from recent experiments to provide a critical assessment of the costs and benefits of calcification. We conclude that calcification has high energy demands and that coccolithophores might have calcified initially to reduce grazing pressure but that additional benefits such as protection from photodamage and viral/bacterial attack further explain their high diversity and broad spectrum ecology. The cost-benefit aspect of these traits is illustrated by novel ecosystem modeling, although conclusive observations remain limited. In the future ocean, the trade-off between changing ecological and physiological costs of calcification and their benefits will ultimately decide how this important group is affected by ocean acidification and global warming.

Coccolithophore calcification response to past ocean acidification and climate change.

Anthropogenic carbon dioxide emissions are forcing rapid ocean chemistry changes and causing ocean acidification (OA), which is of particular significance for calcifying organisms, including planktonic coccolithophores. Detailed analysis of coccolithophore skeletons enables comparison of calcite production in modern and fossil cells in order to investigate biomineralization response of ancient coccolithophores to climate change. Here we show that the two dominant coccolithophore taxa across the Paleocene-Eocene Thermal Maximum (PETM) OA global warming event (~56 million years ago) exhibited morphological response to environmental change and both showed reduced calcification rates. However, only Coccolithus pelagicus exhibits a transient thinning of coccoliths, immediately before the PETM, that may have been OA-induced. Changing coccolith thickness may affect calcite production more significantly in the dominant modern species Emiliania huxleyi, but, overall, these PETM records indicate that the environmental factors that govern taxonomic composition and growth rate will most strongly influence coccolithophore calcification response to anthropogenic change.

Southern Ocean deep-water carbon export enhanced by natural iron fertilization.

The addition of iron to high-nutrient, low-chlorophyll regions induces phytoplankton blooms that take up carbon. Carbon export from the surface layer and, in particular, the ability of the ocean and sediments to sequester carbon for many years remains, however, poorly quantified. Here we report data from the CROZEX experiment in the Southern Ocean, which was conducted to test the hypothesis that the observed north-south gradient in phytoplankton concentrations in the vicinity of the Crozet Islands is induced by natural iron fertilization that results in enhanced organic carbon flux to the deep ocean. We report annual particulate carbon fluxes out of the surface layer, at three kilometres below the ocean surface and to the ocean floor. We find that carbon fluxes from a highly productive, naturally iron-fertilized region of the sub-Antarctic Southern Ocean are two to three times larger than the carbon fluxes from an adjacent high-nutrient, low-chlorophyll area not fertilized by iron. Our findings support the hypothesis that increased iron supply to the glacial sub-Antarctic may have directly enhanced carbon export to the deep ocean. The CROZEX sequestration efficiency (the amount of carbon sequestered below the depth of winter mixing for a given iron supply) of 8,600 mol mol(-1) was 18 times greater than that of a phytoplankton bloom induced artificially by adding iron, but 77 times smaller than that of another bloom initiated, like CROZEX, by a natural supply of iron. Large losses of purposefully added iron can explain the lower efficiency of the induced bloom(6). The discrepancy between the blooms naturally supplied with iron may result in part from an underestimate of horizontal iron supply.

Rapid growth rates of aerobic anoxygenic phototrophs in the ocean.

We analysed bacteriochlorophyll diel changes to assess growth rates of aerobic anoxygenic phototrophs in the euphotic zone across the Atlantic Ocean. The survey performed during Atlantic Meridional Transect cruise 16 has shown that bacteriochlorophyll in the North Atlantic Gyre cycles at rates of 0.91-1.08 day(-1) and in the South Atlantic at rates of 0.72-0.89 day(-1). In contrast, in the more productive equatorial region and North Atlantic it cycled at rates of up to 2.13 day(-1). These results suggest that bacteriochlorophyll-containing bacteria in the euphotic zone of the oligotrophic gyres grow at rates of about one division per day and in the more productive regions up to three divisions per day. This is in striking contrast with the relatively slow growth rates of the total bacterial community. Thus, aerobic anoxygenic phototrophs appear to be a very dynamic part of the marine microbial community and due to their rapid growth, they are likely to be larger sinks for dissolved organic matter than their abundance alone would predict.