Viral infection switches the balance between bacterial and eukaryotic recyclers of organic matter during coccolithophore blooms.

Algal blooms are hotspots of marine primary production and play central roles in microbial ecology and global elemental cycling. Upon demise of the bloom, organic carbon is partly respired and partly transferred to either higher trophic levels, bacterial biomass production or sinking. Viral infection can lead to bloom termination, but its impact on the fate of carbon remains largely unquantified. Here, we characterize the interplay between viral infection and the composition of a bloom-associated microbiome and consequently the evolving biogeochemical landscape, by conducting a large-scale mesocosm experiment where we monitor seven induced coccolithophore blooms. The blooms show different degrees of viral infection and reveal that only high levels of viral infection are followed by significant shifts in the composition of free-living bacterial and eukaryotic assemblages. Intriguingly, upon viral infection the biomass of eukaryotic heterotrophs (thraustochytrids) rivals that of bacteria as potential recyclers of organic matter. By combining modeling and quantification of active viral infection at a single-cell resolution, we estimate that viral infection causes a 2-4 fold increase in per-cell rates of extracellular carbon release in the form of acidic polysaccharides and particulate inorganic carbon, two major contributors to carbon sinking into the deep ocean. These results reveal the impact of viral infection on the fate of carbon through microbial recyclers of organic matter in large-scale coccolithophore blooms.

High CO2 concentration and iron availability determine the metabolic inventory in an Emiliania huxleyi-dominated phytoplankton community.

Ocean acidification (OA), a consequence of anthropogenic carbon dioxide (CO2 ) emissions, strongly impacts marine ecosystems. OA also influences iron (Fe) solubility, affecting biogeochemical and ecological processes. We investigated the interactive effects of CO2 and Fe availability on the metabolome response of a natural phytoplankton community. Using mesocosms we exposed phytoplankton to ambient (390 µatm) or future CO2 levels predicted for the year 2100 (900 µatm), combined with ambient (4.5 nM) or high (12 nM) dissolved iron (dFe). By integrating over the whole phytoplankton community, we assigned functional changes based on altered metabolite concentrations. Our study revealed the complexity of phytoplankton metabolism. Metabolic profiles showed three stages in response to treatments and phytoplankton dynamics. Metabolome changes were related to the plankton group contributing respective metabolites, explaining bloom decline and community succession. CO2 and Fe affected metabolic profiles. Most saccharides, fatty acids, amino acids and many sterols significantly correlated with the high dFe treatment at ambient pCO2 . High CO2 lowered the abundance of many metabolites irrespective of Fe. However, sugar alcohols accumulated, indicating potential stress. We demonstrate that not only altered species composition but also changes in the metabolic landscape affecting the plankton community may change as a consequence of future high-CO2 oceans.

Simple models combining competition, defence and resource availability have broad implications in pelagic microbial food webs.

In food webs, interactions between competition and defence control the partitioning of limiting resources. As a result, simple models of these interactions contain links between biogeochemistry, diversity, food web structure and ecosystem function. Working at hierarchical levels, these mechanisms also produce self-similarity and therefore suggest how complexity can be generated from repeated application of simple underlying principles. Reviewing theoretical and experimental literature relevant to the marine photic zone, we argue that there is a wide spectrum of phenomena, including single cell activity of prokaryotes, microbial biodiversity at different levels of resolution, ecosystem functioning, regional biogeochemical features and evolution at different timescales; that all can be understood as variations over a common principle, summarised in what has been termed the 'Killing-the-Winner' (KtW) motif. Considering food webs as assemblages of such motifs may thus allow for a more integrated approach to aquatic microbial ecology.

Bacterial community composition responds to changes in copepod abundance and alters ecosystem function in an Arctic mesocosm study.

Combining a minimum food web model with Arctic microbial community dynamics, we have suggested that top-down control by copepods can affect the food web down to bacterial consumption of organic carbon. Pursuing this hypothesis further, we used the minimum model to design and analyse a mesocosm experiment, studying the effect of high (+Z) and low (-Z) copepod density on resource allocation, along an organic-C addition gradient. In the Arctic, both effects are plausible due to changes in advection patterns (affecting copepods) and meltwater inputs (affecting carbon). The model predicts a trophic cascade from copepods via ciliates to flagellates, which was confirmed experimentally. Auto- and heterotrophic flagellates affect bacterial growth rate and abundance via competition for mineral nutrients and predation, respectively. In +Z, the model predicts low bacterial abundance and activity, and little response to glucose; as opposed to clear glucose consumption effects in -Z. We observed a more resilient bacterial response to high copepods and demonstrate this was due to changes in bacterial community equitability. Species able to use glucose to improve their competitive and/or defensive properties, became predominant. The observed shift from a SAR11-to a Psychromonodaceae - dominated community suggests the latter was pivotal in this modification of ecosystem function. We argue that this group used glucose to improve its defensive or its competitive abilities (or both). Adding such flexibility in bacterial traits to the model, we show how it creates the observed resilience to top-down manipulations observed in our experiment.

Seasonal variations in C:N:Si:Ca:P:Mg:S:K:Fe relationships of seston from Norwegian coastal water: Impact of extreme offshore forcing during winter-spring 2010.

The aim of this study was to reveal the relative content of C, N, Ca, Si, P, Mg, K, S and Fe in seston particles in Norwegian coastal water (NCW), and how it relates to biological and hydrographic processes during seasonal cycles from October 2009-March 2012. The following over all stoichiometric relationship for the time series was obtained: C66N11Si3.4Ca2.3P1Mg0.73S0.37K0.35Fe0.30, which is novel for marine waters. A record-breaking (187-year record) negative North Atlantic Oscillation (NAO) index caused extreme physical forcing on the Norwegian Coastal Current Water (NCCW) during the winter 2009-2010, and the inflow and upwelling of saline Atlantic water (AW) in the fjord was thus extraordinary during late spring-early summer in 2010. The element concentrations in fjord seston particles responded strongly to this convection, revealed by maximum values of all elements, except Fe, exceeding average values with 10.8 × for Ca, 9.3 for K, 5.3 for S, 5.1 for Mg, 4.6 for Si, 4.0 for P, 3.8 for C, and 3.3 for N and Fe. This indicates that the signature of the Atlantic inflow was roughly two times stronger for Ca and K than for the others, probably connected with peaks in coccolithophorids and diatoms. There is, however, 1.5 × more of Si than Ca contained in the seston, which could be due to a stronger dominance of diatoms than coccolithophorids, confirming their environmental fitness. In total our data do not indicate any severe nutrient limitation with respect to N, P and Fe, but accumulation of iron by Fe-sequestering bacteria might at times reduce the availability of the dissolved Fe-fraction. There is a high correlation between most of the measured elements, except for Ca, which together with Fe only weakly correlated with the other elements. It is to be expected that environmental alterations in NCW related to climate change will influence the seston elemental composition, but the full effect of this will be strongly dependent on the future dominance of the high pressure versus low pressure systems (i.e. NAO index), since they are key regulators for the direction of wind driven vertical convection (i.e. upwelling or downwelling). Changes in stratification, temperature, light, pH (ocean acidification), CaCO3 concentrations (carbon pump) and availability of nutrients in the euphotic zone (biogeochemical cycling) are essential for the future dominance of coccolithophorids versus diatoms.

Contrasting response to nutrient manipulation in Arctic mesocosms are reproduced by a minimum microbial food web model.

A minimum mathematical model of the marine pelagic microbial food web has previously shown to be able to reproduce central aspects of observed system response to different bottom-up manipulations in a mesocosm experiment Microbial Ecosystem Dynamics (MEDEA) in Danish waters. In this study, we apply this model to two mesocosm experiments (Polar Aquatic Microbial Ecology (PAME)-I and PAME-II) conducted at the Arctic location Kongsfjorden, Svalbard. The different responses of the microbial community to similar nutrient manipulation in the three mesocosm experiments may be described as diatom-dominated (MEDEA), bacteria-dominated (PAME-I), and flagellated-dominated (PAME-II). When allowing ciliates to be able to feed on small diatoms, the model describing the diatom-dominated MEDEA experiment give a bacteria-dominated response as observed in PAME I in which the diatom community comprised almost exclusively small-sized cells. Introducing a high initial mesozooplankton stock as observed in PAME-II, the model gives a flagellate-dominated response in accordance with the observed response also of this experiment. The ability of the model originally developed for temperate waters to reproduce population dynamics in a 10°C colder Arctic fjord, does not support the existence of important shifts in population balances over this temperature range. Rather, it suggests a quite resilient microbial food web when adapted to in situ temperature. The sensitivity of the model response to its mesozooplankton component suggests, however, that the seasonal vertical migration of Arctic copepods may be a strong forcing factor on Arctic microbial food webs.