Biology subjects

Logares, R.

Publications and source records attributed to Logares, R..

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bioRxiv2021

Disentangling environmental effects in microbial association networks

BackgroundEcological interactions among microorganisms are fundamental for ecosystem function, yet they are mostly unknown or poorly understood. High-throughput-omics can indicate microbial interactions through associations across time and space, which can be represented as association networks. Associations could result from either ecological interactions between microorganisms, or from environmental selection, where the associations are environmentally-driven. Therefore, before downstream analysis and interpretation, we need to distinguish the nature of the association, particularly if it is due to environmental selection or not. ResultsWe present EnDED (Environmentally-Driven Edge Detection), an implementation of four approaches as well as their combination to predict which links between microorganisms in an association network are environmentally-driven. The four approaches are Sign Pattern, Overlap, Interaction Information, and Data Processing Inequality. We tested EnDED on networks from simulated data of 50 microorganisms. The networks contained on average 50 nodes and 1087 edges, of which 60 were true interactions but 1026 false associations (i.e. environmentally-driven or due to chance). Applying each method individually, we detected a moderate to high number of environmentally-driven edges--87% Sign Pattern and Overlap, 67% Interaction Information, and 44% Data Processing Inequality. Combining these methods in an intersection approach resulted in retaining more interactions, both true and false (32% of environmentally-driven associations). After validation with the simulated datasets, we applied EnDED on a marine microbial network inferred from 10 years of monthly observations of microbial-plankton abundance. The intersection combination predicted that 8.3% of the associations were environmentally-driven, while individual methods predicted 24.8% (Data Processing Inequality), 25.7% (Interaction Information), and up to 84.6% (Sign Pattern as well as Overlap). The fraction of environmentally-driven edges among negative microbial associations in the real network increased rapidly with the number of environmental factors. ConclusionsTo reach accurate hypotheses about ecological interactions, it is important to determine, quantify, and remove environmentally-driven associations in marine microbial association networks. For that, EnDED offers up to four individual methods as well as their combination. However, especially for the intersection combination, we suggest using EnDED with other strategies to reduce the number of false associations and consequently the number of potential interaction hypotheses.

microbiology↗

bioRxiv2021

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↗

bioRxiv2021

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↗

bioRxiv2021

Microbial communities network structure across strong environmental gradients: How do they compare to macroorganisms?

The way strong environmental gradients shape multispecific assemblages has allowed us to examine a suite of ecological and evolutionary hypotheses about structure, regulation, and community responses to fluctuating environments. But whether the highly diverse co-occurring, free-living microorganisms are shaped in similar ways as macroscopic organisms, across the same gradients, has yet to be addressed in most ecosystems. The everything is everywhere hypothesis suggests they are not, at least not to the same extent. Here we characterize the structure of intertidal microbial biofilm communities and compare the intensity of zonation at the species level, changes in taxonomic diversity and composition at the community level, and network attributes, with those observed in co-occurring macroalgae and invertebrates. At the level of species and OTUs, for dominant macro and microorganisms respectively, microbes showed less variability across the tidal gradient than macroorganisms. At the community-level, however, microbes and macro-organisms showed similarly strong patterns of tidal zonation, with major changes in composition and relative abundances across tides. Moreover, the proportion of environmental specialists in different tidal zones was remarkably similar in micro and macroscopic communities, and taxonomic richness and diversity followed similar trends, with lower values in the high intertidal zone. Network analyses showed similar connectivity and transitivity, despite the large differences in absolute richness between the groups. A high proportion of positive co-occurrences within all tidal zones and mostly negative links between the high and low tidal zones were observed among habitat specialist taxa of micro-and macro-organisms. Thus, our results provide partial support to the idea that microbes are less affected by environmental variability than macroscopic counterparts. At the species-level, the most common microbe species exhibit less variation across tides than most common macroscopic organisms, suggesting the former perceive a more homogeneous environment and/or are more resistant to the associated stress. At the community-level, most indicators of community and network structure across the gradient are similar between microbes and macro-organisms, suggesting that despite orders of magnitude differences in richness and size, these two systems respond to stress gradients, giving rise to zonation patterns.

ecology↗

bioRxiv2021

Elucidating the diversity of microeukaryotes and epi-endophytes in the brown algal holobiome

BackgroundBrown algae (Phaeophyceae) are essential species in coastal ecosystems where they form kelp forests and seaweed beds that support a wide diversity of marine life. Host-associated microbial communities are an integral part of phaeophyte biology. The bacterial microbial partners of brown algae have received far more attention than microbial eukaryotes. To our knowledge, this is the first study to investigate brown algal-associated eukaryotes (the eukaryome) using broadly targeting pan-eukaryotic primers and high throughput sequencing (HTS). Using this approach, we aimed to unveil the eukaryome of seven large common brown algal species. We also aimed to assess whether these macroalgae harbour novel eukaryotic diversity and to ascribe putative functional roles to the host-associated eukaryome, based on taxonomic affiliation and phylogenetic placement. ResultsOur sequence dataset was dominated by brown algal reads, from the host species and potential symbionts. We also detected a broad taxonomic diversity of eukaryotes in the brown algal holobiomes, with OTUs taxonomically assigned to ten of the eukaryotic major Kingdoms or supergroups. A total of 265 microeukaryotic and epi-endophytic operational taxonomic units (OTUs) were defined, using 97% similarity cut off during clustering, and were dominated by OTUs assigned to stramenopiles, Alveolata and Fungi. Almost one third of the OTUs we detected have not been found in previous molecular environmental surveys, and represented potential novel eukaryotic diversity. This potential novel diversity was particularly prominent in phylogenetic groups comprising heterotrophic and parasitic organisms, such as labyrinthulids and oomycetes, Cercozoa, and Amoebozoa. ConclusionsOur findings provide important baseline data for future studies of seaweed-associated microorganisms, and demonstrate that microeukaryotes and epi-endophytic eukaryotes should be considered as an integral part of brown algal holobionts. The potential novel eukaryotic diversity we found and the fact that the vast majority of macroalgae in marine habitats remain unexplored, demonstrates that brown algae and other seaweeds are potentially rich sources for a large and hidden diversity of novel microeukaryotes and epi-endophytes.

ecology↗

bioRxiv2021

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↗

bioRxiv2020

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↗

bioRxiv2020

Evolutionary diversification of tiny ocean predators

Unicellular eukaryotic predators have a crucial role in the functioning of the ocean ecosystem by recycling nutrients and energy that are channeled to upper trophic levels. Traditionally, these evolutionary-diverse organisms have been combined into a single functional group (Heterotrophic flagellates), overlooking their organismal differences. Here we investigate four evolutionary related species belonging to one cosmopolitan family of uncultured marine picoeukaryotic predators: MAST-4 (species A, B, C, and E). Co-occurrence and distribution analyses in the global surface ocean indicated contrasting patterns in MAST-4A & C, suggesting adaptation to different temperatures. We then investigated whether these spatial distribution patterns were mirrored by MAST-4 genomic content using Single-Cell Genomics. Analyses of 69 single-cells recovered 66-83% of the MAST-4A/B/C/E genomes, which displayed substantial inter-species divergence. MAST-4 genomes were similar in terms of broad gene functional categories, but they differed in enzymes of ecological relevance, such as glycoside hydrolases (GHs), which are part of the food degradation machinery in MAST-4. Interestingly, MAST-4 species featuring a similar GH composition co-excluded each other (A & C) in the surface global ocean, while species with a different set of GHs appeared to be able to co-exist (species B & C) suggesting further niche diversification associated to prey digestion. We propose that differential niche adaptation to temperature and prey type has promoted adaptive evolutionary diversification in MAST-4. Altogether, we show that minute ocean predators from the same family may have different biogeography and genomic content, which need to be accounted to better comprehend marine food webs.

ecology↗

bioRxiv2019

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↗

bioRxiv2019

The planktonic protist interactome: emerging trends after a century of research

Microbial interactions are crucial for Earth ecosystem function, yet our knowledge about them is limited and has so far mainly existed as scattered records. Here, we have surveyed the literature involving planktonic protist interactions and gathered the information in a manually curated Protist Interaction DAtabase (PIDA). In total, we have registered ~2,500 ecological interactions from ~500 publications, spanning the last 150 years. All major protistan lineages were involved in interactions as hosts, symbionts, parasites, predators and/or prey. Symbiosis was the most common interaction (43% of all records), followed by predation (39%) and parasitism (18%). Using bipartite networks, we found that protistan predators seem to be \"multivorous\", while parasite-host and symbiont-host interactions appear to have moderate degrees of specialization. The SAR supergroup (i.e. Stramenopiles, Alveolata and Rhizaria) heavily dominated PIDA, and comparisons against a global-ocean molecular survey (TARA Oceans) indicated that several SAR lineages, which are abundant and diverse in the marine realm, were underrepresented among the compiled interactions. All in all, despite historical biases, our work not only unveils large-scale eco-evolutionary trends in the protist interactome, but it also constitutes an expandable resource to investigate protist interactions and to test hypotheses deriving from omics tools.

ecology↗

bioRxiv2019

Uncovering the gene machinery of the Amazon River microbiome to degrade rainforest organic matter

The Amazon River receives, from the surrounding rainforest, huge amounts of terrestrial organic matter (TeOM), which is typically resistant to microbial degradation. However, only a small fraction of the TeOM ends up in the ocean, indicating that most of it is degraded in the river. So far, the nature of the genes involved in TeOM degradation and their spatial distributions are barely known. Here, we examined the Amazon River microbiome gene repertoire and found that it contains a substantial gene-novelty, compared to other environments (rivers and rainforest soil). We predicted ~3.7 million non-redundant genes, affiliating mostly to bacteria. The gene-functions involved in TeOM degradation revealed that lignin degradation correlated to tricarboxylates and hemicellulose processing, pointing to higher lignin degradation rates under consumption of labile compounds. We describe the biochemical machinery that could be speeding up the decomposition of recalcitrant compounds in Amazonian waters, previously reported only in incubation experiments.

biochemistry↗

bioRxiv2019

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↗

bioRxiv2019

Bacterioplankton dynamics driven by inter-annual variation in phytoplankton spring bloom communities in the Baltic Sea

In the Baltic Sea, climate change has caused shifts in the phytoplankton spring bloom communities with co-occurrence of diatoms and dinoflagellates. Such changes likely affect the composition and function of associated bacterioplankton, key members of the carbon cycling, although the actual effects are unknown. To understand how changes in phytoplankton impact on bacterioplankton composition and function, we analysed bacterioplankton communities and their production during different phases of the spring bloom in four consecutive years across the Baltic Sea, and related them to environmental variables. Phytoplankton communities varied largely in composition, modifying the taxonomic structure and richness of the associated bacterioplankton assemblages. In presence of certain diatoms (Achnanthes taeniata, Skeletonema costatum and Chaetoceros spp.), bacterial production and diversity were high and with more relative abundance of Flavobacteriia, Gammaproteobacteria and Betaproteobacteria. This bacterial community structure correlated positively with high diatom biomass and with high bacterial production rates. In contrast, during dinoflagellate-dominated blooms or when the diatom Thalassiosira baltica was abundant, both bacterial production rates and diversity were low, with bacterial communities dominated by SAR11 and Rhodobacteraceae. Our results demonstrate that, changes in the phytoplankton spring bloom will have profound consequences on bacterial community structure and their role in carbon cycling.

microbiology↗

bioRxiv2018

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↗

bioRxiv2018

Microzooplankton distribution in the Amundsen Sea Polynya (Antarctica) during an extensive Phaeocystis antarctica bloom

In Antarctica, summer is a time of extreme environmental shifts resulting in large coastal phytoplankton blooms fueling the food web. Despite the importance of the microbial loop in remineralizing biomass from primary production, studies of how microzooplankton communities respond to such blooms in the Southern Ocean are rather scarce. Microzooplankton (ciliates and dinoflagellates) communities were investigated combining microscopy and 18S rRNA sequencing analyses in the Amundsen Sea Polynya during an extensive summer bloom of Phaeocystis antarctica. The succession of microzooplankton was further assessed during a 15-day induced bloom microcosm experiment. Dinoflagellates accounted for up to 58% the microzooplankton biomass in situ with Gymnodinium spp., Protoperidium spp. and Gyrodinium spp. constituting 87% of the dinoflagellate biomass. Strombilidium spp., Strombidium spp. and tintinids represented 90% of the ciliates biomass. Gymnodinium, Gyrodinium and tintinnids are known grazers of Phaeocystis, suggesting that this prymnesiophyte selected for the key microzooplankton taxa. Availability of other potential prey, such as diatoms, heterotrophic nanoflagellates and bacteria, also correlated to changes in microzooplankton community structure. Overall, both heterotrophy and mixotrophy appeared to be key trophic strategies of the dominant microzooplankton observed, suggesting that they influence carbon flow in the microbial food web through top-down control on the phytoplankton community.

ecology↗

bioRxiv2017

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↗

bioRxiv2017

Habitat diversification promotes environmental selection in planktonic prokaryotes and ecological drift in microbial eukaryotes

Whether or not communities of microbial eukaryotes are structured in the same way as prokaryotes is a basic and poorly explored question in ecology. Here we investigated this question in a set of planktonic lake microbiotas in Eastern Antarctica that represent a natural community ecology experiment. Most of the analysed lakes emerged from the sea during the last 6,000 years, giving rise to waterbodies that originally contained marine microbiotas and that subsequently evolved into habitats ranging from freshwater to hypersaline. We show that habitat diversification has promoted environmental selection driven by a salinity gradient in prokaryotes and ecological drift in microeukaryotes. Nevertheless, we detected also a number of microeukaryotes with specific responses to salinity, indicating that albeit minor, environmental selection has had a role in the assembly of their communities. Altogether, we conclude that habitat diversification can promote contrasting responses in planktonic microeukaryotes and prokaryotes belonging to the same communities.

ecology↗