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 β-glucosidase activity) which, as a whole, resulted in a moderate increase of oligotrophy in Blanes Bay after the lockdown.
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•COVID-19 lockdown effects on marine planktonic communities are still unknown.•A set of 23 variables were compared between spring 2020 and the 15 previous years.•Data show a decrease of some microbial groups, and a moderate increase in oligotrophy.•Induced, among others, by reduced fishing, wastewater flux and N atmospheric load
Viruses play important roles in the ocean's biogeochemical cycles. Yet, deep ocean viruses are one of the most under-explored fractions of the global biosphere. Little is known about the ...environmental factors that control the composition and functioning of their communities or how they interact with their free-living or particle-attached microbial hosts.
We analysed 58 viral communities associated with size-fractionated free-living (0.2-0.8 μm) and particle-attached (0.8-20 μm) cellular metagenomes from bathypelagic (2150-4018 m deep) microbiomes obtained during the Malaspina expedition. These metagenomes yielded 6631 viral sequences, 91% of which were novel, and 67 represented high-quality genomes. Taxonomic classification assigned 53% of the viral sequences to families of tailed viruses from the order Caudovirales. Computational host prediction associated 886 viral sequences to dominant members of the deep ocean microbiome, such as Alphaproteobacteria (284), Gammaproteobacteria (241), SAR324 (23), Marinisomatota (39), and Chloroflexota (61). Free-living and particle-attached viral communities had markedly distinct taxonomic composition, host prevalence, and auxiliary metabolic gene content, which led to the discovery of novel viral-encoded metabolic genes involved in the folate and nucleotide metabolisms. Water mass age emerged as an important factor driving viral community composition. We postulated this was due to changes in quality and concentration of dissolved organic matter acting on the host communities, leading to an increase of viral auxiliary metabolic genes associated with energy metabolism among older water masses.
These results shed light on the mechanisms by which environmental gradients of deep ocean ecosystems structure the composition and functioning of free-living and particle-attached viral communities. Video Abstract.
Due to the scarcity of organic matter (OM) sources in the bathypelagic (1000–4000 m depth), prokaryotic metabolism is believed to be concentrated on particles originating from the surface. However, ...the structure of active bathypelagic prokaryotic communities and how it changes across environmental gradients remains unexplored. Using a combination of 16S rRNA gene and transcripts sequencing, metagenomics, and substrate uptake potential measurements, here we aimed to explore how water masses aging and the quality of OM influence the structure of the active microbiome, and the potential implications for community function. We found that the relative contribution of taxa with a free‐living lifestyle to the active microbiome increased in older water masses that were enriched in recalcitrant OM, suggesting that these prokaryotes may also play a substantial role in the bathypelagic metabolism of vast areas of the ocean. In comparison to particle‐associated prokaryotes, free‐living prokaryotes exhibited lower potential metabolic rates, and harbored a limited number of two‐component sensory systems, suggesting they have less ability to sense and respond to environmental cues. In contrast, particle‐associated prokaryotes carried genes for particle colonization and carbohydrate utilization that were absent in prokaryotes with a free‐living lifestyle. Consistently, we observed that prokaryotic communities inhabiting older waters displayed reduced abilities to colonize particles, and higher capabilities to use complex carbon sources, compared to communities in waters with a higher proportion of labile OM. Our results provide evidence of regionalization of the bathypelagic active prokaryotic microbiome, unveiling a niche partitioning based on the quality of OM.
Deep ocean microbial communities rely on the organic carbon produced in the sunlit ocean, yet it remains unknown whether surface processes determine the assembly and function of bathypelagic ...prokaryotes to a larger extent than deep‐sea physicochemical conditions. Here, we explored whether variations in surface phytoplankton assemblages across Atlantic, Pacific and Indian ocean stations can explain structural changes in bathypelagic (ca. 4,000 m) free‐living and particle‐attached prokaryotic communities (characterized through 16S rRNA gene sequencing), as well as changes in prokaryotic activity and dissolved organic matter (DOM) quality. We show that the spatial structuring of prokaryotic communities in the bathypelagic strongly followed variations in the abundances of surface dinoflagellates and ciliates, as well as gradients in surface primary productivity, but were less influenced by bathypelagic physicochemical conditions. Amino acid‐like DOM components in the bathypelagic reflected variations of those components in surface waters, and seemed to control bathypelagic prokaryotic activity. The imprint of surface conditions was more evident in bathypelagic than in shallower mesopelagic (200–1,000 m) communities, suggesting a direct connectivity through fast‐sinking particles that escape mesopelagic transformations. Finally, we identified a pool of endemic deep‐sea prokaryotic taxa (including potentially chemoautotrophic groups) that appear less connected to surface processes than those bathypelagic taxa with a widespread vertical distribution. Our results suggest that surface planktonic communities shape the spatial structure of the bathypelagic microbiome to a larger extent than the local physicochemical environment, likely through determining the nature of the sinking particles and the associated prokaryotes reaching bathypelagic waters.
The heterotrophic bacterial community of the Eastern Mediterranean Sea is believed to be limited by phosphorus (P) availability. This observation assumes that all bacterial groups are equally ...limited, something that has not been hitherto examined. To test this hypothesis, we performed nutrient addition experiments and investigated the response of probe-identified groups using microautoradiography combined with catalyzed reporter deposition fluorescence in situ hybridization. Our results show contrasting responses between the bacterial groups, with Gammaproteobacteria being the group more affected by P availability. The Roseobacter clade was likely colimited by P and nitrogen (N), whereas Bacteroidetes by P, N and organic carbon (C). In contrast, SAR11 cells were active regardless of the nutrient concentration. These results indicate that there is high heterogeneity in the nutrient limitation of the different components of the bacterioplankton community.
Microbial interactions are vital in maintaining ocean ecosystem function, yet their dynamic nature and complexity remain largely unexplored. Here, we use association networks to investigate possible ...ecological interactions in the marine microbiome among archaea, bacteria, and picoeukaryotes throughout different depths and geographical regions of the tropical and subtropical global ocean. Our findings reveal that potential microbial interactions change with depth and geographical scale, exhibiting highly heterogeneous distributions. A few potential interactions were global, meaning they occurred across regions at the same depth, while 11-36% were regional within specific depths. The bathypelagic zone had the lowest proportion of global associations, and regional associations increased with depth. Moreover, we observed that most surface water associations do not persist in deeper ocean layers despite microbial vertical dispersal. Our work contributes to a deeper understanding of the tropical and subtropical global ocean interactome, which is essential for addressing the challenges posed by global change.
Upon phosphorus (P) deficiency, marine phytoplankton reduce their requirements for P by replacing membrane phospholipids with alternative non-phosphorus lipids. It was very recently demonstrated that ...a SAR11 isolate also shares this capability when phosphate starved in culture. Yet, the extent to which this process occurs in other marine heterotrophic bacteria and in the natural environment is unknown. Here, we demonstrate that the substitution of membrane phospholipids for a variety of non-phosphorus lipids is a conserved response to P deficiency among phylogenetically diverse marine heterotrophic bacteria, including members of the Alphaproteobacteria and Flavobacteria. By deletion mutagenesis and complementation in the model marine bacterium Phaeobacter sp. MED193 and heterologous expression in recombinant Escherichia coli, we confirm the roles of a phospholipase C (PlcP) and a glycosyltransferase in lipid remodelling. Analyses of the Global Ocean Sampling and Tara Oceans metagenome data sets demonstrate that PlcP is particularly abundant in areas characterized by low phosphate concentrations. Furthermore, we show that lipid remodelling occurs seasonally and responds to changing nutrient conditions in natural microbial communities from the Mediterranean Sea. Together, our results point to the key role of lipid substitution as an adaptive strategy enabling heterotrophic bacteria to thrive in the vast P-depleted areas of the 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.
Prokaryotes represent a major fraction of marine biomass and play a key role in the global carbon cycle. We studied the vertical profiles (0–3500 m) of abundance, viability, and activity of ...prokaryotic communities along a productivity gradient in the subtropical and tropical Atlantic to assess whether there is a vertical linkage between surface productivity regimes and deep ocean prokaryotic communities. We found that latitudinal changes in the vertical patterns of cytometric variables were coupled with surface productivity: higher prokaryotic abundances and viabilities, and smaller cell sizes were observed below highly productive surface waters, an effect reaching down to the bathypelagic layer. Leucine uptake rates in deep waters showed no clear relationship with surface productivity. Changes in resource and energy allocation to growth vs. maintenance in hostile environments, cell‐size‐dependent metabolic requirements, and variability in leucine‐to‐carbon conversion may all be part of the array of factors involved in controlling the prokaryotic activity patterns that were measured. Our work adds to the recent findings that highlight the importance of vertical connectivity for prokaryotic communities in the dark ocean and unveils a remarkable impact of surface conditions in the viability of deep ocean prokaryotes. This is a key aspect when considering metabolic rates of prokaryotic communities in the bathypelagic realm.
Bacteroidetes is one of the dominant phyla of ocean bacterioplankton, yet its diversity and population structure is poorly understood. To advance in the delineation of ecologically meaningful units ...within this group, we constructed near full‐length 16S rRNA gene clone libraries from contrasting marine environments in the NW Mediterranean. Based on phylogeny and the associated ecological variables (depth and season), 24 different Bacteroidetes clades were delineated. By considering their relative abundance (from iTag amplicon sequencing studies), we described the distribution patterns of each of these clades, delimiting them as Ecologically Significant Taxonomic Units (ESTUs). Spatially, there was almost no overlap among ESTUs at different depths. In deep waters there was predominance of Owenweeksia, Leeuwenhoekiella, Muricauda‐related genera, and some depth‐associated ESTUs within the NS5 and NS2b marine clades. Seasonally, multi‐annual dynamics of recurring ESTUs were present with dominance of some ESTUs within the NS4, NS5 and NS2b marine clades along most of the year, but with variable relative frequencies between months. A drastic change towards the predominance of Formosa‐related ESTUs and one ESTU from the NS5 marine clade was typically present after the spring bloom. Even though there are no isolates available for these ESTUs to determine their physiology, correlation analyses identified the environmental preference of some of them. Overall, our results suggest that there is a high degree of niche specialisation within these closely related clades. This work constitutes a step forward in disentangling the ecology of marine Bacteroidetes, which are essential players in organic matter processing in the oceans.
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