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Gasol, J. M.

Publications and source records attributed to Gasol, J. M..

32 records · Page 2Linked to original sources

Disentangling temporal associations in marine microbial networks

BackgroundMicrobial interactions are fundamental for Earths ecosystem functioning and biogeochemical cycling. Nevertheless, they are challenging to identify and remain barely known. Omics-based censuses are helpful in predicting microbial interactions through the statistical inference of single (static) association networks. Yet, microbial interactions are dynamic and we have limited knowledge of how they change over time. Here we investigate the dynamics of microbial associations in a 10-year marine time series in the Mediterranean Sea using an approach inferring a time-resolved (temporal) network from a single static network. ResultsA single static network including microbial eukaryotes and bacteria was built using metabarcoding data derived from 120 monthly samples. For the decade, we aimed to identify persistent, seasonal, and temporary microbial associations by determining a temporal network that captures the interactome of each individual sample. We found that the temporal network appears to follow an annual cycle, collapsing and reassembling when transiting between colder and warmer waters. We observed higher association repeatability in colder than in warmer months. Only 16 associations could be validated using observations reported in literature, underlining our knowledge gap in marine microbial ecological interactions. ConclusionsOur results indicate that marine microbial associations follow recurrent temporal dynamics in temperate zones, which need to be accounted for to better understand the functioning of the ocean microbiome. The constructed marine temporal network may serve as a resource for testing season-specific microbial interaction hypotheses. The applied approach can be transferred to microbiome studies in other ecosystems.

microbiology↗

Disentangling marine microbial networks across space

Microbial interactions underpin ocean ecosystem function, but they remain barely known. Multiple studies have analyzed microbial interactions using static association networks based on omics data, yet microbial interactions are dynamic and can change across spatiotemporal scales. Understanding the dynamics of microbial interactions is needed for a better comprehension of ocean ecosystems. Here, we explored associations between archaea, bacteria, and picoeukaryotes along the water column, from the surface to the deep ocean, across the northern subtropical to the southern temperate ocean and the Mediterranean Sea by defining sample-specific subnetworks, which allowed us to examine changes in microbial associations across space. We found that associations tend to change with depth as well as with geographical scale, with a few associations being global (i.e., present across regions within the same depth layer) and 11-36% being regional within specific water layers. The lowest fraction of global associations was found in the bathypelagic zone, while associations restricted to certain regions increased with depth. The majority of associations observed in surface waters disappeared with depth, suggesting that surface ocean associations are not transferred to the deep sea, despite microbial sinking. Altogether, our results suggest that microbial associations have highly heterogeneous distributions in the horizontal and vertical dimensions of the ocean and that such distributions do not mirror taxonomic distributions. Our work contributes to better understand the dynamics of microbial interactions in the global ocean, which is urgently needed in a context of global change.

microbiology↗

A robust approach to estimate relative phytoplankton cell abundance from metagenomic data

Phytoplankton account for >45% of global primary production, and have an enormous impact on aquatic food webs and on the entire Earth System. Their members are found among prokaryotes (cyanobacteria) and multiple eukaryotic lineages containing chloroplasts. Phytoplankton communities are generally studied by PCR amplification of bacterial (16S), nuclear (18S) or chloroplastic (16S) rRNA marker genes from DNA extracted from environmental samples. However, our appreciation of phytoplankton abundance or biomass is limited by PCR-amplification biases, rRNA gene copy number variations across taxa, and the fact that rRNA genes do not provide insights into metabolic traits such as photosynthesis. In addition, rRNA marker genes fail to capture both cyanobacteria and photosynthetic eukaryotes simultaneously. Here, we targeted the photosynthetic gene psbO from metagenomes to circumvent these limitations: the method is PCR-free, and the gene is universally and exclusively present in photosynthetic prokaryotes and eukaryotes, mainly in one copy per genome. We applied and validated this new strategy with the Tara Oceans datasets, and showed improved correlations with flow cytometry and microscopy than when based on rRNA genes. Furthermore, we revealed unexpected features of the ecology of these organisms, such as the high abundance of picocyanobacterial aggregates and symbionts in the ocean, and the decrease in relative abundance of phototrophs towards the larger size classes of marine dinoflagellates. To facilitate the incorporation of psbO in molecular-based surveys, we compiled a curated database of >18,000 unique sequences. Overall, psbO appears to be a promising new gene marker for molecular-based evaluations of entire phytoplankton communities.

ecology↗

The quality of dissolved organic matter shapes the biogeography of the active bathypelagic microbiome

The bathypelagic ocean (1000-4000 m depth) is the largest aquatic biome on Earth but it is still largely unexplored. Due to its prevalent low dissolved organic carbon concentrations, most of the prokaryotic metabolic activity is assumed to be associated to particles. The role of free-living prokaryotes has thus been mostly ignored, except that of some chemolithoautotrophic lineages. Here we used a global bathypelagic survey of size-fractionated metagenomic and 16S (genes and transcripts) data and performed a differential abundance analysis to explore the functional traits of the different prokaryotic life-strategies, their contribution to the active microbiome, and the role that the quality of the dissolved organic matter (DOM) plays in driving this contribution. We found that free-living prokaryotes have limited capacity to uplift their metabolism in response to environmental changes and display comparatively lower growth rates than particle associated prokaryotes, but are responsible for the synthesis of vitamins in the bathypelagic. Furthermore, their contribution to the active prokaryotic microbiome increased towards waters depleted of labile DOM, which represented a large fraction of the tropical and subtropical ocean sampled stations. This points to a relevant yet overlooked role of free-living prokaryotes in DOM cycling in the vast bathypelagic desert.

ecology↗

Long-term patterns of an interconnected core marine microbiota

BackgroundOcean microbes constitute [~]70% of the marine biomass, are responsible for [~]50% of the Earths primary production, and are crucial for global biogeochemical cycles. Marine microbiotas include core taxa that are usually key for ecosystem function. Despite their importance, core marine microbes are relatively unknown, which reflects the lack of consensus on how to identify them. So far, most core microbiotas have been defined based on species occurrence and abundance. Yet, species interactions are also important to identify core microbes, as communities include interacting species. Here, we investigate interconnected bacteria and small protists of the core pelagic microbiota populating a long-term marine-coastal observatory in the Mediterranean Sea over a decade. ResultsCore microbes were defined as those present in >30% of the monthly samples over 10 years, with the strongest associations. The core microbiota included 259 Operational Taxonomic Units (OTUs) including 182 bacteria, 77 protists, and 1,411 strong and mostly positive ([~]95%) associations. Core bacteria tended to be associated with other bacteria, while core protists tended to be associated with bacteria. The richness and abundance of core OTUs varied annually, decreasing in stratified warmers waters and increasing in colder mixed waters. Most core OTUs had a preference for one season, mostly winter, which featured subnetworks with the highest connectivity. Groups of highly associated taxa tended to include protists and bacteria with predominance in the same season, particularly winter. A group of 13 highly-connected hub-OTUs, with potentially important ecological roles dominated in winter and spring. Similarly, 18 connector OTUs with a low degree but high centrality were mostly associated with summer or autumn and may represent transitions between seasonal communities. ConclusionsWe found a relatively small and dynamic interconnected core microbiota in a model temperate marine-coastal site, with potential interactions being more deterministic in winter than in other seasons. These core microbes would be essential for the functioning of this ecosystem over the year. Other non-core taxa may also carry out important functions but would be redundant and non-essential. Our work contributes to the understanding of the dynamics and potential interactions of core microbes possibly sustaining ocean ecosystem function.

ecology↗

Seasonal niche differentiation between evolutionary closely related marine bacteria

Bacteria are highly dynamic in marine environments, where they play key biogeochemical roles. Here, we tested how similar the niche of closely related marine bacteria is and what are the environmental parameters modulating their ecological responses in a coastal oligotrophic time series. We further explored how conserved the niche is at broader taxonomic levels. We found that, for certain genera, niche similarity decreases as nucleotide divergence increases between closely related amplicon sequence variants, a pattern compatible with selection of similar taxa through habitat filtering. Additionally, we observed evidence of niche partitioning within various genera shown by the distinct seasonal patterns of closely related taxa. At broader levels, we did not observe coherent seasonal trends at the class level, with the order and family ranks conditioned to the patterns that exist at the genus level. This study explores the coexistence of niche overlap and niche partitioning in a coastal marine environment.

microbiology↗

Rapid Evolution of Plastic-degrading Enzymes Prevalent in the Global Ocean

Estimates of marine plastic stocks, a major threat to marine life (1), are far lower than expected from exponentially-increasing litter inputs, suggesting important loss factors (2, 3). These may involve microbial degradation, as the plastic-degrading polyethylene terephthalate enzyme (PETase) has been reported in marine microbial communities (4). An assessment of 416 metagenomes of planktonic communities across the global ocean identifies 68 oceanic PETase variants (oPETase) that evolved from ancestral enzymes degrading polycyclic aromatic hydrocarbons. Twenty oPETases show predicted efficiencies comparable to those of laboratory-optimized PETases, suggesting strong selective pressures directing the evolution of these enzymes. We found oPETases in 90.1% of samples across all oceans and depths, particularly abundant at 1,000 m depth, with a strong dominance of Pseudomonadales containing putative highly-efficient oPETase variants in the dark ocean. Enzymatic degradation may be removing plastic from the marine environment while providing a carbon source for bathypelagic microbial communities.

evolutionary biology↗

Diversity patterns of marine heterotrophic culturable bacteria along vertical and latitudinal gradients

Nowadays, there is a significant gap in the knowledge of the diversity and patterns for marine heterotrophic culturable microorganisms. In addition, most of the bacterial isolation efforts have focused on the photic ocean leaving the deep ocean less explored. We have isolated 1561 bacterial strains covering both photic (817) and aphotic layers (744) including isolates from the oxygen minimum zone (362) and the bathypelagic (382) from a variety of oceanographic regions including the North Western Mediterranean Sea, the North and South Atlantic Oceans, the Indian, the Pacific, and the Arctic Oceans. The partial sequencing of the 16S rRNA gene of all isolates revealed that they mainly affiliate with the classes Alphaproteobacteria (35.9%) and Gammaproteobacteria (38.6%), as well as, phylum Bacteroidetes (16.5%). The genera Alteromonas and Erythrobacter were the most widespread heterotrophic bacteria in the ocean able to grow on solid agar media. When comparing the sequences of all isolates, 37% of them were 100% identical. In fact, we found that 59% of the total aphotic isolates were 100% identical to photic isolates, indicating the ubiquity of some bacterial isolates along the water column. Unweighted UniFrac distances did not show significant differences among stations regardless of their geographic distance or depth, reflecting the wide dispersion of the culturable bacterial assemblage. This isolates collection provides an overview of the distribution patterns of cosmopolitan marine culturable heterotrophic bacteria.

microbiology↗

Metabolic Architecture of the Deep Ocean Microbiome

The deep sea, the largest compartment of the ocean, is an essential component of the Earth system, but the functional exploration of its microbial communities lags far behind that of other marine realms. Here we analyze 58 bathypelagic microbial metagenomes from the Atlantic, Indian, and Pacific Oceans in an unprecedented sampling effort from the Malaspina Global Expedition, to resolve the metabolic architecture of the deep ocean microbiome. The Malaspina Deep-Sea Gene Collection, 71% of which consists of novel genes, reveals a strong dichotomy between the functional traits of free-living and particle-attached microorganisms, and shows relatively patchy composition challenging the paradigm of a uniform dark ocean ecosystem. Metagenome Assembled Genomes uncovered 11 potential new phyla, establishing references for deep ocean microbial taxa, and revealed mixotrophy to be a widespread trophic strategy in the deep ocean. These results expand our understanding of the functional diversity, metabolic versatility, and carbon cycling in the largest ecosystem on Earth.\n\nOne Sentence SummaryA whole community genomic survey of the deep microbiome sheds light on the microbial and functional diversity of the dark ocean.

microbiology↗

Marked changes in diversity and relative activity of picoeukaryotes with depth in the global ocean

Microbial eukaryotes are key components of the ocean plankton. Yet, our understanding of their community composition and activity in different water layers of the ocean is limited, particularly for picoeukaryotes (0.2-3{micro}m cell size). Here we examined the picoeukaryotic communities inhabiting different vertical zones of the tropical and subtropical global ocean: surface, deep chlorophyll maximum, mesopelagic (including the deep scattering layer and minimum oxygen zone) and bathypelagic. Communities were analysed by high-throughput sequencing of the 18S rRNA gene, as represented by DNA (community structure) and RNA (metabolic expression), followed by delineation of Operational Taxonomic Units (OTUs). We found a clear stratification of the picoeukaryotic communities along the water column, with two differentiated assemblages corresponding to the sunlit and dark ocean. Specific taxonomic groups either increased or decreased their abundances with depth. We used the rRNA:rDNA ratio of each individual OTU as a proxy of its metabolic activity. The highest relative activity was found in the mesopelagic layer for most taxonomic groups, and the lowest in the bathypelagic. Overall, our results characterize the change in community structure and activity of picoeukaryotes in the global-ocean water column, suggesting that the mesopeagic layer is a hot-spot of picoeukaryotic activity.

microbiology↗

Different processes shape prokaryotic and picoeukaryotic assemblages in the sunlit ocean microbiome

The smallest members of the sunlit-ocean microbiome (prokaryotes and picoeukaryotes) participate in a plethora of ecosystem functions with planetary-scale effects. Understanding the processes determining the spatial turnover of this assemblage can help us better comprehend the links between microbiome species composition and ecosystem function. Ecological theory predicts that selection, dispersal and drift are main drivers of species distributions, yet, the relative quantitative importance of these ecological processes in structuring the surface-ocean microbiome is barely known. Here we quantified the role of selection, dispersal and drift in structuring surface-ocean prokaryotic and picoeukaryotic assemblages by using community DNA-sequence data collected during the global Malaspina expedition. We found that dispersal limitation was the dominant process structuring picoeukaryotic communities, while a balanced combination of dispersal limitation, selection and drift shaped prokaryotic counterparts. Subsequently, we determined the agents exerting abiotic selection as well as the spatial patterns emerging from the action of different ecological processes. We found that selection exerted via temperature had a strong influence on the structure of prokaryotic communities, particularly on species co-occurrences, a pattern not observed among communities of picoeukaryotes. Other measured abiotic variables had limited selective effects on microbiome structure. Picoeukaryotes presented a higher differentiation between neighbouring communities and a higher distance-decay when compared to prokaryotes, agreeing with their higher dispersal limitation. Finally, drift seemed to have a limited role in structuring the sunlit-ocean microbiome. The different predominance of ecological processes acting on particular subsets of the ocean microbiome suggests uneven responses to environmental change.\n\nSIGNIFICANCE STATEMENTThe global ocean contains one of the largest microbiomes on Earth and changes on its structure can impact the functioning of the biosphere. Yet, we are far from understanding the mechanisms that structure the global ocean microbiome, that is, the relative importance of environmental selection, dispersal and random events (drift). We evaluated the role of these processes at the global scale, based on data derived from a circumglobal expedition and found that these ecological processes act differently on prokaryotes and picoeukaryotes, two of the main components of the ocean microbiome. Our work represents a significant contribution to understand the assembly of marine microbial communities, providing also insights on the links between ecological mechanisms, microbiome structure and ecosystem function.

ecology↗

Long-term seasonality of marine photoheterotrophic bacteria reveals low cohesiveness within the different phylogroups

Aerobic anoxygenic phototrophic (AAP) bacteria play a relevant role in the marine microbial food web, but little is known about their long-term seasonal dynamics. Using Illumina amplicon sequencing of the pufM gene coupled with multivariate, time series and co-occurrence analyses we examined their temporal dynamics over a decade at the Blanes Bay Microbial Observatory (NW Mediterranean). Phylogroup K (Gammaproteobacteria) was the most abundant over all seasons, with phylogroups E and G (Alphaproteobacteria) being often abundant in spring. A clear seasonal trend was observed in diversity, with maximum values in winter. Multivariate analyses showed sample clustering by season, with a relevant proportion of the variance (38%) explained by day length, temperature, salinity, phototrophic nanoflagellate abundance and phosphate concentration. Time series analysis showed that only 42% of the Amplicon Sequence Variants (ASVs) analyzed presented marked seasonality but these represented most of the abundance (92%). Interestingly, distinct temporal dynamics were observed within the same phylogroup and even within different ASVs conforming the same Operational Taxonomic Unit (OTU). Likewise, co-occurrence analysis highlighted negative associations between various ASVs within the same phylogroup. Altogether our results picture the AAP assemblage as highly seasonal, containing ecotypes with distinctive niche partitioning rather than being a cohesive functional group.

microbiology↗

Quantifying long-term predictability in microbial plankton dynamics

Determining predictability in community turnover is a key ecological question. In the microbial world, seasonality has been reported for communities inhabiting temperate zones, but not much is known on seasonality for individual species. Specifically, we have a vague understanding on the amount of species displaying predictability during temporal community turnover as well as on their dynamics. Here we developed a Recurrence Index to quantify predictability in microbial species. Applying our index to 18S rDNA metabarcoding data from one of the longest temporal observatories of marine plankton we determined that 13% of the picoeukaryotic and 19% of the nanoeukaryotic species, accounting for about 40% of the community abundance in both fractions, feature predictable dynamics when sampled monthly during 10 years. Thus, most of the species analysed had unpredictable temporal abundance patterns. Altogether, we show that species with both predictable and unpredictable temporal dynamics can occur within the same seasonal microbial community.

ecology↗

Marine proteorhodopsins rival photosynthesis in solar energy capture

All known phototrophic metabolisms on Earth are based on one of three energy-converting pigments: chlorophyll-a, bacteriochlorophyll-a, and retinal, which is the chromophore in rhodopsins [1]. While the contribution of chlorophylls to global energy flows and marine carbon cycling has been studied for decades, the role of retinal-based phototrophy remains largely unexplored [1,2]. We report the first vertical distributions of the three energy-converting pigments measured along a contrasting nutrient gradient through the Mediterranean Sea and the Eastern Atlantic Ocean. The highest proteorhodopsin concentrations were observed above the deep chlorophyll-a maxima, and their geographical distribution tended to be inversely related to that of chlorophyll-a. We further show that proteorhodopsins potentially absorb as much or more light energy than chlorophyll-a -based phototrophy and this energy is sufficient to sustain bacterial basal metabolism. Our results suggest that ubiquitous proteorhodopsin-containing heterotrophs are important contributors to the light energy captured in the sea.

ecology↗