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Ice-binding proteins (IBPs) are a group of ecologically and biotechnologically relevant enzymes produced by psychrophilic organisms. Although putative IBPs containing the domain of unknown function (DUF) 3494 have been identified in many taxa of polar microbes, our knowledge of their genetic and structural diversity in natural microbial communities is limited. Here, we used samples from sea ice and sea water collected in the central Arctic Ocean as part of the MOSAiC expedition for metagenome sequencing and the subsequent analyses of metagenome-assembled genomes (MAGs). By linking structurally diverse IBPs to particular environments and potential functions, we reveal that IBP sequences are enriched in interior ice, have diverse genomic contexts and cluster taxonomically. Their diverse protein structures may be a consequence of domain shuffling, leading to variable combinations of protein domains in IBPs and probably reflecting the functional versatility required to thrive in the extreme and variable environment of the central Arctic Ocean.

Fragilariopsiskerguelensis (O’ Meara) Hust. is a ubiquitous diatom of the Southern Ocean. Its thick frustules are the numerically dominant component of the siliceous sediment layer covering large parts of the seafloor beneath. Morphometric variability of frustules of this diatom has been of interest for paleoenvironmental reconstructions. Recently, two morphotypes differentiated by the morphometric descriptor rectangularity were described from a Southern Ocean sediment core, the relative abundance of which correlated with reconstructed paleotemperatures. In the present study, we use semi-automated microscopic and image analysis methods to answer whether these morphotypes also appear in recent assemblages, and if yes, do their distributions reflect geographic location or environmental factors. Three transects from the water column, sampled along the Greenwich meridian with hand nets, and one sediment surface transect from the South Pacific, were analyzed. In each of these transects, both morphotypes were detected, and annual mean sea surface temperatures (SST) were found to be a good predictor of their relative abundances. The transition between dominance of one or the other morphotype appeared roughly between the Antarctic Polar Front and the Southern Boundary of the Antarctic Circumpolar Current. Although more extensive circumpolar sampling will be needed to confirm the generality of our conclusions, the observed morphometric cline is a novel aspect of the biology of this species and can in the future potentially be used for further developing paleoproxies especially for highly F.kerguelensis-dominated sediment in the Southern Ocean.

The Southern Ocean is characterized by longitudinal water circulations crossed by strong latitudinal gradients. How this oceanographic background shapes planktonic populations is largely unknown, despite the significance of this region for global biogeochemical cycles. Here, we show, based on genomic, morphometric, ecophysiological and mating compatibility data, an example of ecotypic differentiation and speciation within an endemic pelagic inhabitant, the diatom Fragilariopsis kerguelensis. We discovered three genotypic variants, one present throughout the latitudinal transect sampled, the others restricted to the north and south, respectively. The latter two showed reciprocal monophyly across all three genomes and significant ecophysiological differences consistent with local adaptation, but produced viable offspring in laboratory crosses. The third group was also reproductively isolated from the latter two. We hypothesize that this pattern originated by an adaptive expansion accompanied by ecotypic divergence, followed by sympatric speciation.

Ecological research in recent decades revealed that species loss has a predominantly negative effect on ecosystem functioning and stability. Most of these studies were based on random species loss scenarios, but extinctions in nature are not random. Recent experimental studies using macroscopic communities largely advanced knowledge about the effects of non-random species loss. However, in microscopic communities like the phytoplankton, implementing realistic species loss scenarios is challenging and experimental data are scarce. Creating more realistic experiments to study the role of phytoplankton diversity for ecosystem functioning is particularly important, as they provide up to 50% of global primary productivity, form the basis of all pelagic food webs, and are important for biogeochemical cycling. In this study, we experimentally tested and evaluated three methods for non-random species loss in a natural marine phytoplankton community. Dilution, filtration, and heat stress removed the targeted rare, large, and sensitive species, respectively. All these species groups are extremely vulnerable to extinction in future climate scenarios and play important roles in the communities. Dilution and filtration with a fine mesh additionally decreased initial biomass, which increased the variability of species left in the respective replicates. The methods tested in this study can be used to non-randomly manipulate phytoplankton species diversity in communities used for experiments. However, in studies where species identities are more important than species richness, the dilution and filtration methods should be modified to eliminate the effect of decreasing initial biomass.

In experimental metacommunities with marine benthic microalgae, we tested whether heat stress changes effects of connectivity and habitat heterogeneity on metacommunity structure and functioning, by manipulating a simulated heat wave, dispersal frequency and a light intensity gradient. We found that all measures of mean local and regional diversity and community biomass significantly declined after the heat wave and showed no sign of recovery. Additionally, dispersal decreased diversity and increased dominance in both the heat stressed and control communities. Together the heat wave and high dispersal frequency induced a dominance shift by spreading a temperature tolerant but low yielding species from its source patches with low light intensity across the metacommunity, an effect that increased with time. Although different species became dominant at high dispersal frequency with and without the heat wave, the shift towards a temperature tolerant species was not sufficient to maintain total community biomass. Thus, short-term disturbance may cause longer-term loss of ecosystem function due to dominance shifts in the composition of communities. This study illustrates the importance of employing multispecies approaches when attempting to predict responses of communities to environmental changes.

The ongoing rise in atmospheric pCO2 and consequent increase in ocean acidification have direct effects on marine calcifying phytoplankton, which potentially alters carbon export. To date it remains unclear, firstly, how nutrient regime, in particular by coccolithophores preferred phosphate limitation, interacts with pCO2 on particulate carbon accumulation; secondly, how direct physiological responses on the cellular level translate into total population response. In this study, cultures of Emiliania huxleyi were full-factorially exposed to two different N:P regimes and three different pCO2 levels. Cellular biovolume and PIC and POC content significantly declined in response to pCO2 in both nutrient regimes. Cellular PON content significantly increased in the Redfield treatment and decreased in the high N:P regime. Cell abundance significantly declined in the Redfield and remained constant in the high N:P regime. We hypothesise that in the high N:P regime severe phosphorous limitation could be compensated either by reduced inorganic phosphorous demand and/or by enzymatic uptake of organic phosphorous. In the Redfield regime we suggest that enzymatic phosphorous uptake to supplement enhanced phosphorous demand with pCO2 was not possible and thus cell abundance declined. These hypothesised different physiological responses of E. huxleyi among the nutrient regimes significantly altered population carrying capacities along the pCO2 gradient. This ultimately led to the attenuated total population response in POC and PIC content and biovolume to increased pCO2 in the high N:P regime. Our results point to the fact that the physiological (i.e. cellular) PIC and POC response to ocean acidification cannot be linearly extrapolated to total population response and thus carbon export. It is therefore necessary to consider both effects of nutrient limitation on cell physiology and their consequences for population size when predicting the influence of coccolithophores on atmospheric pCO2 feedback and their function in carbon export mechanisms.

Ecosystem functioning is simultaneously affected by changes in community composition and environmental change such as increasing atmospheric carbon dioxide (CO2 ) and subsequent ocean acidification. However, it largely remains uncertain how the effects of these factors compare to each other. Addressing this question, we experimentally tested the hypothesis that initial community composition and elevated CO2 are equally important to the regulation of phytoplankton biomass. We full-factorially exposed three compositionally different marine phytoplankton communities to two different CO2 levels and examined the effects and relative importance (ω(2) ) of the two factors and their interaction on phytoplankton biomass at bloom peak. The results showed that initial community composition had a significantly greater impact than elevated CO2 on phytoplankton biomass, which varied largely among communities. We suggest that the different initial ratios between cyanobacteria, diatoms, and dinoflagellates might be the key for the varying competitive and thus functional outcome among communities. Furthermore, the results showed that depending on initial community composition elevated CO2 selected for larger sized diatoms, which led to increased total phytoplankton biomass. This study highlights the relevance of initial community composition, which strongly drives the functional outcome, when assessing impacts of climate change on ecosystem functioning. In particular, the increase in phytoplankton biomass driven by the gain of larger sized diatoms in response to elevated CO2 potentially has strong implications for nutrient cycling and carbon export in future oceans.

Climate change has the potential to profoundly influence the community structure and function of marine ecosystems. Prior to testing the consequences of altered environmental conditions on ecosystem functioning, it is first necessary to better understand how the functioning of an ecosystem is affected by its structure. Using phytoplankton communities with 4 naturally co‑occurring coccolithophores including species of Emiliania, Gephyrocapsa, and Calcidiscus collected off the Azores, we experimentally tested whether varying initial dominance leads to different competitive outcomes and consequently affects community functioning, such as biomass and carbon accumulation. We manipulated initial community structure by creating 5 different dominance scenarios: (1) all species contributing evenly to total initial biomass, and (2–5) one of each species contributing 4× that of the remaining 3 species to total initial biomass. All 4 species were simultaneously grown in monocultures starting with the same total initial biomass as the communities. Monocultures differed significantly in total final biomass, particulate inorganic carbon, and particulate organic carbon content. Priority effects in the communities caused the initially dominant species to remain dominant during the stationary phase in 3 out of 4 cases. However, despite varying dominant species and different outcomes in the monocultures, community functioning was unaffected. We suggest that selective and facilitative effects are responsible for the equalization of community functioning. We conclude that monoculture experiments are not sufficient to predict whole-community responses, since species interactions can significantly alter the expected functional outcome.