SignificanceProkaryotes dominate the living biomass and the biological diversity of the ocean, one of the largest ecosystems on earth. The sinking of particles is a widespread mechanism that transports materials to the deep ocean, with a significant role in the global carbon cycle. Whether this process constitutes a global dispersal pathway for prokaryotic diversity connecting surface communities to those in the dark ocean has never been tested. Here we show that surface and deep-sea prokaryotic communities are strongly connected, constituting a vast oceanic metacommunity where local assemblages are linked through the transport of sinking particles. This vertical dispersal, mediated mainly by the largest sinking particles, emerges as a fundamental process shaping the assembly and biogeography of deep ocean prokaryotic communities.
Background: The ocean microbiota modulates global biogeochemical cycles and changes in its configuration may have large-scale consequences. Yet, the underlying ecological mechanisms structuring it are unclear. Here, we investigate how fundamental ecological mechanisms (selection, dispersal and ecological drift) shape the smallest members of the tropical and subtropical surface-ocean microbiota: prokaryotes and minute eukaryotes (picoeukaryotes). Furthermore, we investigate the agents exerting abiotic selection on this assemblage as well as the spatial patterns emerging from the action of ecological mechanisms. To explore this, we analysed the composition of surface-ocean prokaryotic and picoeukaryotic communities using DNA-sequence data (16S-and 18S-rRNA genes) collected during the circumglobal expeditions Malaspina-2010 and TARA-Oceans. Results: We found that the two main components of the tropical and subtropical surface-ocean microbiota, prokaryotes and picoeukaryotes, appear to be structured by different ecological mechanisms. Picoeukaryotic communities were predominantly structured by dispersal-limitation, while prokaryotic counterparts appeared to be shaped by the combined action of dispersal-limitation, selection and drift. Temperature-driven selection appeared as a major factor, out of a few selected factors, influencing species co-occurrence networks in prokaryotes but not in picoeukaryotes, indicating that association patterns may contribute to understand ocean microbiota structure and response to selection. Other measured abiotic variables seemed to have limited selective effects on community structure in the tropical and subtropical ocean. Picoeukaryotes displayed a higher spatial differentiation between communities and a higher distance decay when compared to prokaryotes, consistent with a scenario of higher dispersal limitation in the former after considering environmental heterogeneity. Lastly, random dynamics or drift seemed to have a more important role in structuring prokaryotic communities than picoeukaryotic counterparts.
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.
Depending on their relationship with the pelagic particulate matter, planktonic prokaryotes have traditionally been classified into two types of communities: free-living (FL) or attached (ATT) to particles, and are generally separated using only one pore-size filter in a differential filtration. Nonetheless, particulate matter in the oceans appears in a continuum of sizes. Here we separated this continuum into six discrete size-fractions, from 0.2 to 200 μm, and described the prokaryotes associated to each of them. Each size-fraction presented different bacterial communities, with a range of 23-42% of unique (OTUs) in each size-fraction, supporting the idea that they contained distinct types of particles. An increase in richness was observed from the smallest to the largest size-fractions, suggesting that increasingly larger particles contributed new niches. Our results show that a multiple size-fractionation provides a more exhaustive description of the bacterial diversity and community structure than the use of only one filter. In addition, and based on our results, we propose an alternative to the dichotomy of FL or ATT lifestyles, in which we differentiate the taxonomic groups with preference for the smaller fractions, those that do not show preferences for small or large fractions, and those that preferentially appear in larger fractions.
The dark ocean is one of the largest biomes on Earth, with critical roles in organic matter remineralization and global carbon sequestration. Despite its recognized importance, little is known about some key microbial players, such as the community of heterotrophic protists (HP), which are likely the main consumers of prokaryotic biomass. To investigate this microbial component at a global scale, we determined their abundance and biomass in deepwater column samples from the Malaspina 2010 circumnavigation using a combination of epifluorescence microscopy and flow cytometry. HP were ubiquitously found at all depths investigated down to 4000 m. HP abundances decreased with depth, from an average of 72 ± 19 cells ml À 1 in mesopelagic waters down to 11 ± 1 cells ml À 1 in bathypelagic waters, whereas their total biomass decreased from 280±46 to 50±14 pg C ml À 1 . The parameters that better explained the variance of HP abundance were depth and prokaryote abundance, and to lesser extent oxygen concentration. The generally good correlation with prokaryotic abundance suggested active grazing of HP on prokaryotes. On a finer scale, the prokaryote:HP abundance ratio varied at a regional scale, and sites with the highest ratios exhibited a larger contribution of fungi molecular signal. Our study is a step forward towards determining the relationship between HP and their environment, unveiling their importance as players in the dark ocean's microbial food web.
Background The ocean microbiota modulates global biogeochemical cycles and changes in its configuration may have largescale consequences. Yet, the underlying ecological mechanisms structuring it are unclear. Here we investigate how fundamental ecological mechanisms ( selection , dispersal and ecological drift ) shape the smallest members of the tropical and subtropical surface-ocean microbiota: prokaryotes and minute eukaryotes (picoeukaryotes). Furthermore, we investigate the agents exerting abiotic selection on this assemblage as well as the spatial patterns emerging from the action of ecological mechanisms. To explore the previous, we analysed the composition of surface-ocean prokaryotic and picoeukaryotic communities using DNA-sequence data (16S- and 18S-rRNA genes) collected during the circumglobal expeditions Malaspina-2010 and TARA-Oceans . Results We found that the two main components of the tropical and subtropical surface-ocean microbiota, prokaryotes and picoeukaryotes, appear to be structured by different ecological mechanisms. Picoeukaryotic communities were predominantly structured by dispersal-limitation, while prokaryotic counterparts appeared to be shaped by the combined action of dispersal-limitation, selection and drift. Temperature-driven selection appeared as a major factor, out of a few selected factors, influencing species co-occurrence networks in prokaryotes but not in picoeukaryotes, indicating that association patterns may contribute to understand ocean microbiota structure and response to selection. Other measured abiotic variables seemed to have limited selective effects on community structure in the tropical and subtropical ocean. Picoeukaryotes displayed a higher spatial differentiation between communities and a higher distance decay when compared to prokaryotes, consistent with a scenario of higher dispersal limitation in the former after considering environmental heterogeneity. Lastly, random dynamics or drift seemed to have a more important role in structuring prokaryotic communities than picoeukaryotic counterparts. Conclusions The differential action of ecological mechanisms seems to cause contrasting biogeography, in the tropical and subtropical ocean, among the smallest surface plankton, prokaryotes and picoeukaryotes. This suggests that the idiosyncrasy of the main constituents of the ocean microbiota should be considered in order to understand its current and future configuration, which is especially relevant in a context of global change, where the reaction of surface ocean plankton to temperature increase is still unclear.
We investigated the effects of an increase in dissolved CO2 on the microbial communities of the Mediterranean Sea during two mesocosm experiments in two contrasting seasons: winter, at the peak of the annual phytoplankton bloom, and summer, under low nutrient conditions. The experiments included treatments with acidification and nutrient addition, and combinations of the two. We followed the effects of ocean acidification (OA) on the abundance of the main groups of microorganisms (diatoms, dinoflagellates, nanoeukaryotes, picoeukaryotes, cyanobacteria, and heterotrophic bacteria) and on bacterial activity, leucine incorporation, and extracellular enzyme activity. Our results showed a clear stimulation effect of OA on the abundance of small phytoplankton (pico- and nanoeukaryotes), independently of the season and nutrient availability. A large number of the measured variables showed significant positive effects of acidification in summer compared with winter, when the effects were sometimes negative. Effects of OA were more conspicuous when nutrient concentrations were low. Our results therefore suggest that microbial communities in oligotrophic waters are considerably affected by OA, whereas microbes in more productive waters are less affected. The overall enhancing effect of acidification on eukaryotic pico- and nanophytoplankton, in comparison with the non-significant or even negative response to nutrient-rich conditions of larger groups and autotrophic prokaryotes, suggests a shift towards medium-sized producers in a future acidified ocean.
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.
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