Higher contribution of globally rare bacterial taxa reflects environmental transitions across the surface ocean.

Microbial taxa range from being ubiquitous and abundant across space to extremely rare and endemic, depending on their ecophysiology and on different processes acting locally or regionally. However, little is known about how cosmopolitan or rare taxa combine to constitute communities and whether environmental variations promote changes in their relative abundances. Here we identified the Spatial Abundance Distribution (SpAD) of individual prokaryotic taxa (16S rDNA-defined Operational Taxonomic Units, OTUs) across 108 globally-distributed surface ocean stations. We grouped taxa based on their SpAD shape ("normal-like"- abundant and ubiquitous; "logistic"- globally rare, present in few sites; and "bimodal"- abundant only in certain oceanic regions), and investigated how the abundance of these three categories relates to environmental gradients. Most surface assemblages were numerically dominated by a few cosmopolitan "normal-like" OTUs, yet there was a gradual shift towards assemblages dominated by "logistic" taxa in specific areas with productivity and temperature differing the most from the average conditions in the sampled stations. When we performed the SpAD categorization including additional habitats (deeper layers and particles of varying sizes), the SpAD of many OTUs changed towards fewer "normal-like" shapes, and OTUs categorized as globally rare in the surface ocean became abundant. This suggests that understanding the mechanisms behind microbial rarity and dominance requires expanding the context of study beyond local communities and single habitats. We show that marine bacterial communities comprise taxa displaying a continuum of SpADs, and that variations in their abundances can be linked to habitat transitions or barriers that delimit the distribution of community members.

Deep ocean prokaryotic communities are remarkably malleable when facing long-term starvation.

The bathypelagic ocean is one of the largest ecosystems on Earth and sustains half of the ocean's microbial activity. This microbial activity strongly relies on surface-derived particles, but there is growing evidence that the carbon released through solubilization of these particles may not be sufficient to meet the energy demands of deep ocean prokaryotes. To explore how bathypelagic prokaryotes respond to the absence of external inputs of carbon, we followed the long-term (1 year) dynamics of an enclosed community. Despite the lack of external energy supply, we observed a continuous succession of active prokaryotic phylotypes, which was driven by recruitment of taxa from the seed bank (i.e., initially rare operational taxonomic units [OTUs]). A single OTU belonging to Marine Group I of Thaumarchaeota, which was originally rare, dominated the microbial community for ∼ 4 months and played a fundamental role in this succession likely by introducing new organic carbon through chemolithoautotrophy. This carbon presumably produced a priming effect, because after the decline of Thaumarchaeota, the diversity and metabolic potential of the community increased back to the levels present at the start of the experiment. Our study demonstrates the profound versatility of deep microbial communities when facing organic carbon deprivation.

Marine picoplankton metagenomes and MAGs from eleven vertical profiles obtained by the Malaspina Expedition.

The Ocean microbiome has a crucial role in Earth's biogeochemical cycles. During the last decade, global cruises such as Tara Oceans and the Malaspina Expedition have expanded our understanding of the diversity and genetic repertoire of marine microbes. Nevertheless, there are still knowledge gaps regarding their diversity patterns throughout depth gradients ranging from the surface to the deep ocean. Here we present a dataset of 76 microbial metagenomes (MProfile) of the picoplankton size fraction (0.2-3.0 µm) collected in 11 vertical profiles covering contrasting ocean regions sampled during the Malaspina Expedition circumnavigation (7 depths, from surface to 4,000 m deep). The MProfile dataset produced 1.66 Tbp of raw DNA sequences from which we derived: 17.4 million genes clustered at 95% sequence similarity (M-GeneDB-VP), 2,672 metagenome-assembled genomes (MAGs) of Archaea and Bacteria (Malaspina-VP-MAGs), and over 100,000 viral genomic sequences. This dataset will be a valuable resource for exploring the functional and taxonomic connectivity between the photic and bathypelagic tropical and sub-tropical ocean, while increasing our general knowledge of the Ocean microbiome.

COVID-19 lockdown moderately increased oligotrophy at a marine coastal site.

COVID-19 has led to global population lockdowns that have had indirect effects on terrestrial and marine fauna, yet little is known on their effects on marine planktonic communities. We analysed the effect of the spring 2020 lockdown in a marine coastal area in Blanes Bay, NW Mediterranean. We compared a set of 23 oceanographic, microbial and biogeochemical variables sampled right after the strict lockdown in Spain, with data from the previous 15 years after correcting for long-term trends. Our analysis shows a series of changes in the microbial communities which may have been induced by the combination of the decreased nitrogen atmospheric load, the lower wastewater flux and the reduced fishing activity in the area, among other factors. In particular, we detected a slight decrease beyond the long-term trend in chlorophyll a, in the abundance of several microbial groups (phototrophic nanoflagellates and total prokaryotes) and in prokaryotic activity (heterotrophic prokaryotic production and ß-glucosidase activity) which, as a whole, resulted in a moderate increase of oligotrophy in Blanes Bay after the lockdown.

Enhanced Viral Activity in the Surface Microlayer of the Arctic and Antarctic Oceans.

The ocean surface microlayer (SML), with physicochemical characteristics different from those of subsurface waters (SSW), results in dense and active viral and microbial communities that may favor virus-host interactions. Conversely, wind speed and/or UV radiation could adversely affect virus infection. Furthermore, in polar regions, organic and inorganic nutrient inputs from melting ice may increase microbial activity in the SML. Since the role of viruses in the microbial food web of the SML is poorly understood in polar oceans, we aimed to study the impact of viruses on prokaryotic communities in the SML and in the SSW in Arctic and Antarctic waters. We hypothesized that a higher viral activity in the SML than in the SSW in both polar systems would be observed. We measured viral and prokaryote abundances, virus-mediated mortality on prokaryotes, heterotrophic and phototrophic nanoflagellate abundance, and environmental factors. In both polar zones, we found small differences in environmental factors between the SML and the SSW. In contrast, despite the adverse effect of wind, viral and prokaryote abundances and virus-mediated mortality on prokaryotes were higher in the SML than in the SSW. As a consequence, the higher carbon flux released by lysed cells in the SML than in the SSW would increase the pool of dissolved organic carbon (DOC) and be rapidly used by other prokaryotes to grow (the viral shunt). Thus, our results suggest that viral activity greatly contributes to the functioning of the microbial food web in the SML, which could influence the biogeochemical cycles of the water column.

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.

Prokaryotic Capability to Use Organic Substrates Across the Global Tropical and Subtropical Ocean.

Prokaryotes play a fundamental role in decomposing organic matter in the ocean, but little is known about how microbial metabolic capabilities vary at the global ocean scale and what are the drivers causing this variation. We aimed at obtaining the first global exploration of the functional capabilities of prokaryotes in the ocean, with emphasis on the under-sampled meso- and bathypelagic layers. We explored the potential utilization of 95 carbon sources with Biolog GN2 plates® in 441 prokaryotic communities sampled from surface to bathypelagic waters (down to 4,000 m) at 111 stations distributed across the tropical and subtropical Atlantic, Indian, and Pacific oceans. The resulting metabolic profiles were compared with biological and physico-chemical properties such as fluorescent dissolved organic matter (DOM) or temperature. The relative use of the individual substrates was remarkably consistent across oceanic regions and layers, and only the Equatorial Pacific Ocean showed a different metabolic structure. When grouping substrates by categories, we observed some vertical variations, such as an increased relative utilization of polymers in bathypelagic layers or a higher relative use of P-compounds or amino acids in the surface ocean. The increased relative use of polymers with depth, together with the increases in humic DOM, suggest that deep ocean communities have the capability to process complex DOM. Overall, the main identified driver of the metabolic structure of ocean prokaryotic communities was temperature. Our results represent the first global depiction of the potential use of a variety of carbon sources by prokaryotic communities across the tropical and the subtropical ocean and show that acetic acid clearly emerges as one of the most widely potentially used carbon sources in the ocean.

High Growth Potential of Long-Term Starved Deep Ocean Opportunistic Heterotrophic Bacteria.

Experiments with bacteria in culture have shown that they often display "feast and famine" strategies that allow them to respond with fast growth upon pulses in resource availability, and enter a growth-arrest state when resources are limiting. Although feast responses have been observed in natural communities upon enrichment, it is unknown whether this blooming ability is maintained after long periods of starvation, particularly in systems that are energy limited like the bathypelagic ocean. Here we combined bulk and single-cell activity measurements with 16S rRNA gene amplicon sequencing to explore the response of a bathypelagic community, that had been starved for 1.6 years, to a sudden organic carbon supply. We observed a dramatic change in activity within 30 h, with leucine incorporation rates increasing over two orders of magnitude and the number of translationally active cells (mostly Gammaproteobacteria) increasing 4-fold. The feast response was driven by a single operational taxonomic unit (OTU) affiliated with the Marinobacter genus, which had remained rare during 7 months of starvation. Our work suggests that bathypelagic communities harbor a seed bank of highly persistent and resourceful "feast and famine" strategists that might disproportionally contribute to carbon fluxes through fast responses to occasional pulses of organic matter.

Distribution of transparent exopolymer particles (TEP) in distinct regions of the Southern Ocean.

Transparent exopolymer particles (TEP) are an abundant class of suspended organic particles, mainly formed by polysaccharides, which play important roles in biogeochemical and ecological processes in the ocean. In this study we investigated horizontal and vertical TEP distributions (within the euphotic layer, including the upper surface) and their short-term variability along with a suite of environmental and biological variables in four distinct regions of the Southern Ocean. TEP concentrations in the surface (4 m) averaged 102.3 ±â€¯40.4 µg XG eq. L-1 and typically decreased with depth. Chlorophyll a (Chl a) concentration was a better predictor of TEP variability across the horizontal (R2 = 0.66, p < 0.001) and vertical (R2 = 0.74, p < 0.001) scales than prokaryotic heterotrophic abundance and production. Incubation experiments further confirmed the main role of phytoplankton as TEP producers. The highest surface TEP concentrations were found north of the South Orkney Islands (144.4 ±â€¯21.7 µg XG eq. L-1), where the phytoplankton was dominated by cryptophytes and haptophytes; however, the highest TEP:Chl a ratios were found south of these islands (153.4 ±â€¯29.8 µg XG eq (µg Chl a)-1, compared to a mean of 79.3 ±â€¯54.9 µg XG eq (µg Chl a)-1 in the whole cruise, in association with haptophyte dominance, proximity of sea ice and high exposure to solar radiation. TEP were generally enriched in the upper surface (10 cm) respect to 4 m, despite a lack of biomass enrichment, suggesting either upward transport by positive buoyancy or bubble scavenging, or higher production at the upper surface by light stress or aggregation. TEP concentrations did not present any significant cyclic diel pattern. Altogether, our results suggest that photobiological stress, sea ice melt and turbulence add to phytoplankton productivity in driving TEP distribution across the Antarctic Peninsula area and Atlantic sector of the Southern Ocean.

Metabolic diversity of heterotrophic bacterioplankton over winter and spring in the coastal Arctic Ocean.

Metabolic diversity of heterotrophic bacterioplankton was tracked from early winter through spring with Biolog Ecoplates under the seasonally ice covered arctic shelf in the Canadian Arctic (Franklin Bay, Beaufort Sea). Samples were taken every 6 days from December 2003 to May 2004 at the surface, the halocline where a temperature inversion occurs, and at 200 m, close to the bottom. Despite the low nutrient levels and low chlorophyll a, suggesting oligotrophy in the winter surface waters, the number of substrates used (NSU) was greater than in spring, when chlorophyll a concentrations increased. Denaturing gradient gel electrophorisis analysis also indicated that the winter and spring bacterial communities were phylogenetically distinct, with several new bands appearing in spring. In spring, the bacterial community would have access to the freshly produced organic carbon from the early phytoplankton bloom and the growth of rapidly growing specialist phenotypes would be favoured. In contrast, in winter bacterioplankton consumed more complex organic matter originated during the previous year's phytoplankton production. At the other depths we tested the NSU was similar to that for the winter surface, with no seasonal pattern. Instead, bacterioplankton metabolism seemed to be influenced by resuspension, advection, and sedimentation events that contributed organic matter that enhanced bacterial metabolism.

Eutrophication and acidification: Do they induce changes in the dissolved organic matter dynamics in the coastal Mediterranean Sea?

Two mesocosms experiments were conducted in winter 2010 and summer 2011 to examine how increased pCO2 and/or nutrient concentrations potentially perturbate dissolved organic matter dynamics in natural microbial assemblages. The fluorescence signals of protein- and humic-like compounds were used as a proxy for labile and non-labile material, respectively, while the evolution of bacterial populations, chlorophyll a (Chl a) and dissolved organic carbon (DOC) concentrations were used as a proxy for biological activity. For both seasons, the presence of elevated pCO2 did not cause any significant change in the DOC dynamics (p-value<0.05). The conditions that showed the greatest changes in prokaryote abundances and Chl a content were those amended with nutrients, regardless of the change in pH. The temporal evolution of fluorophores and optical indices revealed that the degree of humification of the organic molecules and their molecular weight changed significantly in the nutrient-amended treatment. The generation of protein-like compounds was paired to increases in the prokaryote abundance, being higher in the nutrient-amended tanks than in the control. Different patterns in the magnitude and direction of the generation of humic-like molecules suggested that these changes depended on initial microbial populations and the availability of extra nutrient inputs. Based on our results, it is expected that in the future projected coastal scenarios the eutrophication processes will favor the transformations of labile and recalcitrant carbon regardless of changes in pCO2.

Phylogenetic and functional diversity of bacterioplankton during Alexandrium spp. blooms.

The phylogenetic and functional diversity of the bacterioplankton assemblage associated with blooms of toxic Alexandrium spp. was studied in three harbours of the NW Mediterranean. Denaturing gradient gel electrophoresis and DNA sequence analysis revealed the presence of a bacterium within the Roseobacter clade related to the presence of Alexandrium cells. Phylogenetic diversity was affected by the presence of Alexandrium spp., geographic situation and seasonality. In contrast, functional diversity, assessed with Biolog plates, was clearly affected by seasonality, but not by the presence of Alexandrium, indicating that the presence of the bacterium associated with the blooms was not enough to modify the metabolic pattern of the bacterioplankton assemblage.

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.