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Acinas, S. G.

Publications and source records attributed to Acinas, S. G..

At least 19 recordsLinked to original sources

A cold-adapted Cas9 nuclease from the deep ocean

The abundance of CRISPR systems in bacteria and archaea fuels the search for Cas nucleases that perform where established enzymes fail. Deep Ocean 1 Cas9 (DO1Cas9) is to our knowledge the first Cas9 nuclease characterized from the deep ocean, recovered from a metagenomic sample at 1,500 m depth in the Atlantic Ocean. DO1Cas9 shows cold-adapted structural flexibility, thermal susceptibility, salt-dependent stability, higher specificity than SpCas9 and cleaves double-stranded DNA efficiently under cold conditions where mesophilic SpCas9 retains only residual activity. DO1Cas9 edits genomes in diverse organisms such as Caenorhabditis elegans, zebrafish, the marine tunicate Oikopleura dioica, and the malaria parasite Plasmodium falciparum. In the marine bacterium Marinomonas mediterranea, DO1Cas9 programmed against an invading phage reduced plaquing efficiency about 10-fold more than SpCas9. These results expand the CRISPR-Cas9 toolbox with a nuclease for cold-chain editing and marine biotechnology.

genetics↗

The ultrasmall ocean microbiome: a reservoir of microbial diversity and nitrogen fixation.

Marine microbiology has long considered ultrasmall (<0.2 {micro}m) size fractions as virus-dominated, yet emerging evidence suggests potential prokaryotic activity with implications for global biogeochemical cycles. Here, we present the first comprehensive genome-resolved survey of this fraction, built on 4,058 metagenome-assembled genomes (MAGs) representing 1,152 species across Bacteria (90.7%) and Archaea (9.3%), dominated by Pseudomonadota, Bacteroidota, and Nanoarchaeota. Over 490 non-redundant MAGs occurred exclusively in the ultrasmall fraction, with 66.8% representing novel taxa, particularly abundant in Arctic surface waters. Beyond known ultrasmall organisms (e.g., DPANN archaea and Patescibacteria), which show expected genomic and metabolic reduction, functional annotation revealed diverse metabolic potential across nitrogen, sulfur, and carbon cycling. Focusing on nitrogen fixation, we identified 13 non-cyanobacterial diazotroph species with complete nitrogenase operons spanning four bacterial classes. These resolved into two ecotypes: cosmopolitan low-abundance taxa, and Arctic ultrasmall-restricted strains reaching up to 16.7% relative abundance. Two lineages (50-400-T64 and Novosphingobium) showed ultrasmall exclusive bipolar distributions across Arctic and Southern Oceans. Beyond nitrogen fixation, these diazotrophs encoded pathways for denitrification, DNRA, sulfur oxidation, and carbon fixation. Our findings reveal an overlooked reservoir of microbial diversity including diazotrophs in the ultrasmall ocean microbiome, with significant implications for polar nitrogen budgets and global biogeochemical models.

microbiology↗

Widespread and Abundant CRISPR-Cas Systems in the Deep Ocean

CRISPR-Cas systems have revolutionized modern biology. Most CRISPR-Cas systems in use for biotechnological applications derive from cultivated bacteria, but evidence suggests that environmental microbiomes harbor a large untapped diversity of these systems. Yet, our understanding of which environmental and biological factors drive the prevalence of CRISPR-Cas systems in the oceans remains limited. A search for CRISPR-Cas systems was conducted among 176 globally-distributed marine microbial metagenomes from the Malaspina expedition, which sampled both free-living and particle-attached microbiomes with emphasis on the deep ocean. We show that CRISPR-Cas systems are proportionally more abundant among microbiomes from the deep ocean than in the photic layers and among free-living microbes compared to those attached to particles, reflecting the higher concentrations of archaea and their viruses in these habitats. We identified 1,146 CRISPR-cas loci, some of which displayed unique loci architectures. From these loci, a total of 48 Cas9 proteins were identified, many of which are potentially novel. These discoveries expand the scope of CRISPR-Cas diversity and point at the deep-sea as a rich reservoir of these resources, which helps guide future bioprospecting efforts.

microbiology↗

Marine picoplankton metagenomes from eleven vertical profiles obtained by the Malaspina Expedition in the tropical and subtropical oceans

The Ocean microbiome has a crucial role on Earths biogeochemical cycles, but also represents a tremendous potential for biological applications as part of the bluebiotechnology. During the last decade, global cruises such as Tara Oceans or the Malaspina Expedition have expanded our knowledge on the diversity and genetic repertoire of marine microbes. Nevertheless, there is still a gap of knowledge on broad scale patterns between photic and bathypelagic dark ocean microbes derived from the lack of detailed vertical profiles covering contrasting oceans depth regions. Here we present a dataset of 76 microbial metagenomes of the picoplankton size fraction (0.2-3.0 m) collected in 11 stations along the Malaspina Expedition circumnavigation that cover vertical profiles sampling at 7 depths, from the surface to the 4000 m deep (or the sea floor in shallower waters). This Malaspina Microbial Vertical Profiles metagenomes (MProfile) dataset produced 1.66 Tbp of raw DNA sequences that assembled into a total 25.3 Gbp. After gene prediction and annotation, we built a 46.3 million non-redundant gene compendium with their corresponding annotations (M-GeneDB-VP), clustered at 95% sequence similarity. This dataset will be a valuable resource for exploring the functional and taxonomic connectivity between the photic and bathypelagic tropical and subtropical ocean at a global scale, while increasing our general knowledge on the Ocean microbiome.

microbiology↗

Global biogeography of the smallest plankton across ocean depths

Tiny ocean plankton (picoplankton) are fundamental for the functioning of the biosphere, but the ecological mechanisms shaping their biogeography are partially understood. Comprehending whether these microorganisms are structured by niche vs. neutral processes is highly relevant in the context of global change. The ecological drivers structuring picoplankton communities differ between prokaryotes and minute eukaryotes (picoeukaryotes) in the global surface ocean: while prokaryotic communities are shaped by a balanced combination of dispersal, selection, and drift, picoeukaryotic communities are mainly shaped by dispersal limitation. Yet, whether or not the relative importance of these processes in structuring picoplankton varies as we dive into the deep ocean was unknown. Here we investigate the mechanisms structuring picoplanktonic communities inhabiting different ocean depths. We analyzed 451 samples from the tropical and subtropical global ocean and the Mediterranean Sea covering the epi- (0-200m), meso- (200- 1,000m), and bathypelagic (1,000-4,000m) depth zones. We found that selection decreased with depth possibly due to lower habitat heterogeneity. In turn, dispersal limitation increased with depth, possibly due to dispersal barriers such as water masses and bottom topography. Picoplankton {beta}-diversity positively correlated with environmental heterogeneity and water mass variability in both the open-ocean and the Mediterranean Sea. However, this relationship tended to be weaker for picoeukaryotes than for prokaryotes. Community patterns were generally more pronounced in the Mediterranean Sea, probably because of its substantial cross-basin environmental heterogeneity and deep-water isolation. Altogether, we found that different combinations of ecological mechanisms shape the biogeography of the smallest members of the ocean microbiome across ocean depths.

ecology↗

Abundant deep ocean heterotrophic bacteria are culturable

Traditional culture techniques usually retrieve only a small fraction of the environmental marine microbial diversity, which mainly belong to the so-called rare biosphere. However, this paradigm has not been fully tested at a broad scale, especially in the deep ocean. Here, we examined the fraction of heterotrophic bacterial communities in photic and deep ocean layers that could be recovered by culture-dependent techniques at a large scale. We compared 16S rRNA gene sequences from a collection of 2003 cultured isolates of heterotrophic marine bacteria with global 16S rRNA metabarcoding datasets (16S TAGs) covering surface, mesopelagic and bathypelagic ocean samples that included 16 of the 22 samples used for isolation. These global datasets represent 60,322 unique 16S amplicon sequence variants (ASVs). Our results reveal a significantly higher proportion of isolates identical to ASVs in deeper ocean layers reaching up to a 28% of the 16S TAGs of the bathypelagic microbial communities, which included the isolation of 3 of the top 10 most abundant 16S ASVs in the global bathypelagic ocean, related to the genera Sulfitobacter, Halomonas and Erythrobacter. These cultured isolates contributed differently to the prokaryotic communities across different plankton size fractions, recruiting between 38% in the free-living size fraction (0.2-0.8 m) and up to 45% in the largest plankton size fraction (20-200 m) in the bathypelagic ocean. Our findings support the hypothesis that sinking particles in the bathypelagic realm act as resource-rich habitats, suitable for the growth of heterotrophic bacteria with a copiotroph lifestyle that can be cultured, and that these cultivable bacteria can also thrive as free-living bacteria.

ecology↗

Water mass age structures the auxiliary metabolic gene content of free-living and particle-attached deep ocean viral communities

Viruses play important roles on the biogeochemical cycles that take place in the ocean.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. Thus, we analysed 58 viral communities associated to size fractionated free-living (0.2-0.8 m) and particle-attached (0.8-20 m) cellular metagenomes from bathypelagic (2,150-4,018 m deep) microbiomes obtained during the Malaspina expedition. These metagenomes yielded 6,631 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.

microbiology↗

Global observation of plankton communities from space

Satellite remote sensing from space is a powerful way to monitor the global dynamics of marine plankton. Previous research has focused on developing models to predict the size or taxonomic groups of phytoplankton. Here we present an approach to identify representative communities from a global plankton network that included both zooplankton and phytoplankton and using global satellite observations to predict their biogeography. Six representative plankton communities were identified from a global co-occurrence network inferred using a novel rDNA 18S V4 planetary-scale eukaryotic metabarcoding dataset. Machine learning techniques were then applied to train a model that predicted these representative communities from satellite data. The model showed an overall 67% accuracy in the prediction of the representative communities. The prediction based on 17 satellite-derived parameters showed better performance than based only on temperature and/or the concentration of chlorophyll a. The trained model allowed to predict the global spatiotemporal distribution of communities over 19-years. Our model exhibited strong seasonal changes in the community compositions in the subarctic-subtropical boundary regions, which were consistent with previous field observations. This network-oriented approach can easily be extended to more comprehensive models including prokaryotes as well as viruses.

ecology↗

A consensus protocol for the recovery of mercury methylation genes from metagenomes

Mercury methylation genes (hgcAB) mediate the formation of the toxic methylmercury and have been identified from diverse environments, including freshwater and marine ecosystems, Arctic permafrost, forest and paddy soils, coal-ash amended sediments, chlor-alkali plants discharges and geothermal springs. Here we present the first attempt at a standardized protocol for the detection, identification and quantification of hgc genes from metagenomes. Our Hg-MATE (Hg-cycling Microorganisms in Aquatic and Terrestrial Ecosystems) database, a catalogue of hgc genes, provides the most accurate information to date on the taxonomic identity and functional/metabolic attributes of microorganisms responsible for Hg methylation in the environment. Furthermore, we introduce "marky-coco", a ready-to-use bioinformatic pipeline based on de novo single-metagenome assembly, for easy and accurate characterization of hgc genes from environmental samples. We compared the recovery of hgc genes from environmental metagenomes using the marky-coco pipeline with an approach based on co-assembly of multiple metagenomes. Our data show similar efficiency in both approaches for most environments except those with high diversity (i.e., paddy soils) for which a co-assembly approach was preferred. Finally, we discuss the definition of true hgc genes and methods to normalize hgc gene counts from metagenomes.

microbiology↗

Prevalence of heterotrophic methylmercury detoxifying bacteria across oceanic regions

Microbial reduction of inorganic divalent mercury (Hg2+) and methylmercury (MeHg) demethylation is performed by the mer operon, specifically by merA and merB genes respectively, but little is known about the mercury tolerance capacity of marine microorganisms and its prevalence in the global ocean. Here, we explored the distribution of these genes in 290 marine heterotrophic bacteria (Alteromonas and Marinobacter spp.) isolated from different oceanographic regions and depths, and assessed their tolerance to diverse concentrations of Hg2+ and MeHg. About 25% of the isolates presented merA and only 8.9% presented both merAB genes, including the strain ISS312 that exhibited the highest tolerance capacity and a degradation efficiency of 98.2% in 24 h. Fragment recruitment analyses of ISS312 genome against microbial metagenomes indicated an extensive distribution across the global bathypelagic ocean. Our findings highlighted that mercury resistance genes are widely distributed in a non-highly polluted environment such as the pelagic marine environment, and that degradation of the neurotoxic MeHg can be performed through the ocean water column by some heterotrophic bacteria at high efficiency with important implications in the biogeochemical cycle of mercury and potentially for the environment and human health. TeaserActive mercury resistance genes detected in marine cultured bacteria are widely distributed in the ocean including the bathypelagic zone.

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↗

Uncharted biosynthetic potential of the ocean microbiome

Microbes are phylogenetically and metabolically diverse. Yet capturing this diversity, assigning functions to host organisms and exploring the biosynthetic potential in natural environments remains challenging. We reconstructed >25,000 draft genomes, including from >2,500 uncharacterized species, from globally-distributed ocean microbial communities, and combined them with [~]10,000 genomes from cultivated and single cells. Mining this resource revealed [~]40,000 putative biosynthetic gene clusters (BGCs), many from unknown phylogenetic groups. Among these, we discovered Candidatus Eudoremicrobiaceae as one of the most biosynthetically diverse microbes detected to date. Discrete transcriptional states structuring natural populations were associated with a potentially niche-partitioning role for BGC products. Together with the characterization of the first Eudoremicrobiaceae natural product, this study demonstrates how microbiomics enables prospecting for candidate bioactive compounds in underexplored microbes and environments.

microbiology↗

Environmental vulnerability of the global ocean plankton community interactome

Marine plankton form complex communities of interacting organisms at the base of the food web, which sustain oceanic biogeochemical cycles, and help regulate climate. Though global surveys are starting to reveal ecological drivers underlying planktonic community structure, and predicted climate change responses, it is unclear how community-scale species interactions will be affected by climate change. Here we leveraged Tara Oceans sampling to infer a global ocean cross-domain plankton co-occurrence network - the community interactome - and used niche modeling to assess its vulnerabilities to environmental change. Globally, this revealed a plankton interactome self-organized latitudinally into marine biomes (Trades, Westerlies, Polar), and more connected poleward. Integrated niche modeling revealed biome-specific community interactome responses to environmental change, and forecasted most affected lineages for each community. These results provide baseline approaches to assess community structure and organismal interactions under climate scenarios, while identifying plausible plankton bioindicators for ocean monitoring of climate change.

ecology↗

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↗

Ecogenomics of key prokaryotes in the Arctic Ocean

The Arctic Ocean is a key player in the regulation of climate and at the same time is under increasing pressure as a result of climate change. Predicting the future of this ecosystem requires understanding of the responses of Arctic microorganisms to environmental change, as they are the main drivers of global biogeochemical cycles. However, little is known about the ecology and metabolic potential of active Arctic microbes. Here, we reconstructed a total of 3,550 metagenomic bins from 41 seawater metagenomes collected as part of the Tara Oceans expedition, covering five different Arctic Ocean regions as well as the sub-Arctic North Atlantic Ocean and including various depths and different seasons (spring to autumn). Of these bins, 530 could be classified as Metagenome Assembled Genomes (MAGs) and over 75% of them represented novel species. We describe their habitat range and environmental preferences, as well as their metabolic capabilities, building the most comprehensive dataset of uncultured bacterial and archaeal genomes from the Arctic Ocean to date. We found a prevalence of mixotrophs, while chemolithoautotrophs were mostly present in the mesopelagic Arctic Ocean during spring and autumn. Finally, the catalogue of Arctic MAGs was complemented with metagenomes and metatranscriptomes from the global ocean to identify the most active MAGs present exclusively in polar metagenomes. These polar MAGs, which display a range of metabolic strategies, might represent Arctic sentinels of climate change and should be considered in prospective studies of the future state of the Arctic Ocean.

ecology↗

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↗