Viral-Mediated Microbe Mortality Modulated by Ocean Acidification and Eutrophication: Consequences for the Carbon Fluxes Through the Microbial Food Web.

Anthropogenic carbon emissions are causing changes in seawater carbonate chemistry including a decline in the pH of the oceans. While its aftermath for calcifying microbes has been widely studied, the effect of ocean acidification (OA) on marine viruses and their microbial hosts is controversial, and even more in combination with another anthropogenic stressor, i.e., human-induced nutrient loads. In this study, two mesocosm acidification experiments with Mediterranean waters from different seasons revealed distinct effects of OA on viruses and viral-mediated prokaryotic mortality depending on the trophic state and the successional stage of the plankton community. In the winter bloom situation, low fluorescence viruses, the most abundant virus-like particle (VLP) subpopulation comprising mostly bacteriophages, were negatively affected by lowered pH with nutrient addition, while the bacterial host abundance was stimulated. High fluorescence viruses, containing cyanophages, were stimulated by OA regardless of the nutrient conditions, while cyanobacteria of the genus Synechococcus were negatively affected by OA. Moreover, the abundance of very high fluorescence viruses infecting small haptophytes tended to be lower under acidification while their putative hosts' abundance was enhanced, suggesting a direct and negative effect of OA on viral-host interactions. In the oligotrophic summer situation, we found a stimulating effect of OA on total viral abundance and the viral populations, suggesting a cascading effect of the elevated pCO2 stimulating autotrophic and heterotrophic production. In winter, viral lysis accounted for 30 ± 16% of the loss of bacterial standing stock per day (VMMBSS) under increased pCO2 compared to 53 ± 35% in the control treatments, without effects of nutrient additions while in summer, OA had no significant effects on VMMBSS (35 ± 20% and 38 ± 5% per day in the OA and control treatments, respectively). We found that phage production and resulting organic carbon release rates significantly reduced under OA in the nutrient replete winter situation, but it was also observed that high nutrient loads lowered the negative effect of OA on viral lysis, suggesting an antagonistic interplay between these two major global ocean stressors in the Anthropocene. In summer, however, viral-mediated carbon release rates were lower and not affected by lowered pH. Eutrophication consistently stimulated viral production regardless of the season or initial conditions. Given the relevant role of viruses for marine carbon cycling and the biological carbon pump, these two anthropogenic stressors may modulate carbon fluxes through their effect on viruses at the base of the pelagic food web in a future global change scenario.

16S rRNA gene amplicon dataset of prokaryotic communities from a subantarctic marine ecosystem: Ushuaia Bay and surrounding waters.

We provide a 16S rRNA gene dataset of prokaryotic assemblages of a subantarctic marine ecosystem. Samples were collected at 2 stations (one near Ushuaia Bay and the other close to Bridges islands in the Beagle Channel). At each station, 2 depths (subsurface and bottom waters) were sampled in february, march, may and september during 2018, giving a total of 10 samples. 16S rRNA gene amplicon sequencing (V4 hypervariable region) was performed with the Illumina MiSeq platform. A total of 1116 amplicon sequence variants (ASVs) were recovered from the dataset. The sequences were taxonomically assigned to Alphaproteobacteria (23 ± 2%, mean ± standard error), Gammaproteobacteria (17 ± 1.5%), Flavobacteriia (8 ± 2%), Deltaproteobacteria (3.7 ± 0.5%), Acidimicrobiia (1.7 ± 0.1%), Planctomycetia (1.9 ± 0.4%), and AB16 group (1.7 ± 0.3%). Sequences affiliated with Archaea were abundant, reaching one third of analyzed sequences, mainly Thaumarchaeota (22 ± 3%), and Thermoplasmata (10 ± 1%). Together, sequences assigned to all these groups accounted for more than 90% of the sequences. This dataset constitutes a valuable resource for future scientific research aiming to unveil the role of these communities in ecosystem services such as carbon and nutrient cycling, and pollutants degradation. This will turn into benefits for future environmental monitoring and preservation actions, considering the tangible heritage of Ushuaia Bay and surrounding waters.

Microbial plankton configuration in the epipelagic realm from the Beagle Channel to the Burdwood Bank, a Marine Protected Area in Sub-Antarctic waters.

Marine microbial plankton hold high structural and functional diversity, however, high-resolution data are lacking in a large part of the Global Ocean, such as in subpolar areas of the SW Atlantic. The Burdwood Bank (BB) is a submerged plateau (average depth 100 m) that constitutes the westernmost segment of the North Scotia Ridge (54°-55°S; 56°-62°W). The BB hosts rich benthic biodiversity in low chlorophyll waters of the southern Patagonian Shelf, Argentina, declared Namuncurá Marine Protected Area (NMPA) in 2013. So far, the pelagic microorganisms above the bank have not been described. During austral summer 2016, we assessed the microbial plankton (0.2-200 µm cell size) biomass and their taxonomical and functional diversity along a longitudinal transect (54.2-55.3°S, 58-68°W) from the Beagle Channel (BC) to the BB, characterized by contrasting hydrography. Results displayed a marked zonation in the composition and structure of the microbial communities. The biomass of phytoplankton >5 µm was 28 times higher in the BC, attributed mainly to large diatom blooms, than in oceanic waters above the BB, where the small coccolithophore Emiliania huxleyi and flagellates <10 µm dominated. In turn, the biomass of microheterotrophs above the BB doubled the biomass in the BC due to large ciliates. Notably, toxic phytoplankton species and their phycotoxins were detected, in particular high abundance of Dinophysis acuminata and pectenotoxins above the bank, highlighting their presence in open subpolar regions. Picophytoplankton (<2 µm), including Synechococcus and picoeukaryotes, were remarkably important above the BB, both at surface and deep waters (up to 150 m). Their biomass surpassed by 5 times that of phytoplankton > 5 µm, emphasizing the importance of small-sized phytoplankton in low chlorophyll waters. The homogeneous water column and high retention above the bank seem to favor the development of abundant picophytoplankton and microzooplankton communities. Overall, our findings unfold the plankton configuration in the Southern Patagonian Shelf, ascribed as a sink for anthropogenic CO2, and highlight the diverse ecological traits that microorganisms develop to adjust their yield to changing conditions.

Viral control of bacterial biodiversity--evidence from a nutrient-enriched marine mesocosm experiment.

We demonstrate here results showing that bottom-up and top-down control mechanisms can operate simultaneously and in concert in marine microbial food webs, controlling prokaryote diversity by a combination of viral lysis and substrate limitation. Models in microbial ecology predict that a shift in the type of bacterial growth rate limitation is expected to have a major effect on species composition within the community of bacterial hosts, with a subsequent shift in the composition of the viral community. Only moderate effects would, however, be expected in the absolute number of coexisting virus-host pairs. We investigated these relationships in nutrient-manipulated systems, under simulated in situ conditions. There was a strong correlation in the clustering of the viral and bacterial community data supporting the existence of an important link between the bacterial and viral communities. As predicted, the total number of viral populations was the same in all treatments, while the composition of the viral community varied. Our results support the theoretical prediction that there is one control mechanism for the number of niches for coexisting virus-host pairs (top-down control), and another mechanism that controls which virus-host pairs occupy these niches (bottom-up control).

Effect of natural iron fertilization on carbon sequestration in the Southern Ocean.

The availability of iron limits primary productivity and the associated uptake of carbon over large areas of the ocean. Iron thus plays an important role in the carbon cycle, and changes in its supply to the surface ocean may have had a significant effect on atmospheric carbon dioxide concentrations over glacial-interglacial cycles. To date, the role of iron in carbon cycling has largely been assessed using short-term iron-addition experiments. It is difficult, however, to reliably assess the magnitude of carbon export to the ocean interior using such methods, and the short observational periods preclude extrapolation of the results to longer timescales. Here we report observations of a phytoplankton bloom induced by natural iron fertilization--an approach that offers the opportunity to overcome some of the limitations of short-term experiments. We found that a large phytoplankton bloom over the Kerguelen plateau in the Southern Ocean was sustained by the supply of iron and major nutrients to surface waters from iron-rich deep water below. The efficiency of fertilization, defined as the ratio of the carbon export to the amount of iron supplied, was at least ten times higher than previous estimates from short-term blooms induced by iron-addition experiments. This result sheds new light on the effect of long-term fertilization by iron and macronutrients on carbon sequestration, suggesting that changes in iron supply from below--as invoked in some palaeoclimatic and future climate change scenarios--may have a more significant effect on atmospheric carbon dioxide concentrations than previously thought.

Changes in bacterioplankton composition under different phytoplankton regimens.

The results of empirical studies have revealed links between phytoplankton and bacterioplankton, such as the frequent correlation between chlorophyll a and bulk bacterial abundance and production. Nevertheless, little is known about possible links at the level of specific taxonomic groups. To investigate this issue, seawater microcosm experiments were performed in the northwestern Mediterranean Sea. Turbulence was used as a noninvasive means to induce phytoplankton blooms dominated by different algae. Microcosms exposed to turbulence became dominated by diatoms, while small phytoflagellates gained importance under still conditions. Denaturing gradient gel electrophoresis (DGGE) of 16S rRNA gene fragments showed that changes in phytoplankton community composition were followed by shifts in bacterioplankton community composition, both as changes in the presence or absence of distinct bacterial phylotypes and as differences in the relative abundance of ubiquitous phylotypes. Sequencing of DGGE bands showed that four Roseobacter phylotypes were present in all microcosms. The microcosms with a higher proportion of phytoflagellates were characterized by four phylotypes of the Bacteroidetes phylum: two affiliated with the family Cryomorphaceae and two with the family Flavobacteriaceae. Two other Flavobacteriaceae phylotypes were characteristic of the diatom-dominated microcosms, together with one Alphaproteobacteria phylotype (Roseobacter) and one Gammaproteobacteria phylotype (Methylophaga). Phylogenetic analyses of published Bacteroidetes 16S rRNA gene sequences confirmed that members of the Flavobacteriaceae are remarkably responsive to phytoplankton blooms, indicating these bacteria could be particularly important in the processing of organic matter during such events. Our data suggest that quantitative and qualitative differences in phytoplankton species composition may lead to pronounced differences in bacterioplankton species composition.