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Latorre, F.

Publications and source records attributed to Latorre, F..

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Seasonal population structure and adaptive signatures across long-term marine microbial time series

Long-term microbial population dynamics can reveal how ocean microbiomes respond to environmental variation, but resolving within-species change requires suitable genomic references. We integrated 30 PacBio HiFi long-read metagenome-assembled genomes (MAGs) from the northwestern Mediterranean Sea with monthly Illumina metagenomes from neighboring time series spanning 12 and 7 years. Population differentiation varied widely among genomes and often differed in magnitude between sites, while a subset showed increasing differentiation with temporal distance. Genetic diversity and population structure were frequently seasonal, with populations associated with warm or cold waters and others spanning both thermal regimes. Candidate adaptive genes accounted for 1.6-3.0% of coding sequences, and many were detected in both time series. Their pN/pS trajectories included regular seasonal fluctuations consistent with changing strain or ecotype contributions, alongside irregular temporal patterns. These results show that combining long-read MAG references with dense short-read time series can resolve seasonal population structure, site-specific differentiation, and candidate adaptive variation within marine microbial species, providing a framework for tracking contemporary population-genomic change in the ocean.

ecology↗

Temperature-driven dynamics of Chlorella sorokiniana and its microbiome

Temperature is a critical factor in microalgal production, yet its impact on microalgae and their microbiome remains poorly understood. Here, we investigated the responses of Chlorella sorokiniana and its microbial community to temperature increases in four wastewater-based cultures over two months. Two Test cultures were subjected to a thermal gradient from 20 {degrees}C to 34 {degrees}C, and two were Controls at 20 {degrees}C. Eukaryotic and bacterial communities were analyzed using 18S and 16S rRNA gene sequencing, and the microalga genome was reconstructed using PacBio HiFi sequencing and functionally annotated. Control cultures remained stable, whereas Test cultures showed a decline in C. sorokiniana relative abundance and biomass from approximately 24 {degrees}C. In contrast, photosynthetic efficiency remained stable until temperatures exceeded 33 {degrees}C. Above 22-24 {degrees}C, the bacterial community, dominated by Fontibacter, Flavobacterium, and Luteolibacter, was replaced by taxa whose relative abundance increased with rising temperature and microalgal decline, pointing to bacteria better adapted to the stress conditions. Candidate predator-prey dynamics with the protist Cercozoa also intensified as temperature increased. Microalgal genome annotation identified 28 candidate genes corresponding to seven of eight literature-informed high-temperature/heat-stress targets, primarily associated with protein homeostasis, Reactive oxygen species protection, membrane lipid remodeling, and protein degradation. Collectively, these genes likely support the microalga's response and adaptation to environmental stress. Overall, culture destabilization resulted from interacting thermal, microbial, and grazing-related processes rather than temperature alone. Early microbiome changes may therefore provide useful warning signals of culture instability and help improve the management of large-scale microalgal production systems.

microbiology↗

Decadal signatures of seasonal and ENSO-driven selection in microbial populations in distant oceans

Despite the crucial role of the ocean microbiome for global ecosystem processes, its response to global change remains poorly understood. Global change will exert selection on microbial species through changes in the genetic composition of their populations, favouring strains that are better adapted to new conditions. Analyzing long-term genomic variation in microbial populations inhabiting climatically comparable but oceanographically distinct regions may provide insights into their responses to future environmental conditions. We analyzed coastal marine microbiomes from two distant long-term observatories with Mediterranean-type climates but contrasting oceanographic regimes: the Blanes Bay Microbial Observatory (BBMO; Northwestern Mediterranean Sea) and the Microbes in the Coastal Region of Orange County (MiCRO; California coast, Pacific Ocean). Sampling conducted at least monthly during 15 and 10 years, respectively, yielded 1,535 Metagenome-Assembled Genomes (MAGs) in BBMO and 1,068 MAGs plus 187 Single-Amplified Genomes (SAGs) in MiCRO. Among these, we found 250 genomes with intraspecific (>95% genome similarity) representatives occurring at both sites. In contrast, at the strain-level threshold ([≥]99% genome similarity), only 13 BBMO genomes matched 15 closely related representatives in MiCRO. As genome similarity increased, we observed a shift from cosmopolitan to more coastal distributions and a slight increase in genome size, pointing to niche adaptation. Across both time series, we observed widespread seasonal population structure, with most genomes (~70%) showing significant seasonal structuring of variant composition. Moreover, in MiCRO, ~76% of the tested genomes also showed El Nino Southern Oscillation (ENSO)-associated structure in variant composition beyond seasonal effects. Focusing on a Prochlorococcus genome with intraspecific representatives at both locations (>96% genome similarity) we further found recurrent seasonal mutations and non-synonymous to synonymous mutation ratios (pN/pS) from multiple genes, together with signatures of positive selection (higher pN/pS) coinciding with El Nino events in MiCRO. This suggests an imprint of ENSO in marine microbial populations. Thus, beyond seasonality, long-term climatic oscillations may shape microbial populations. This has implications for understanding how the ocean microbiome will respond to long-term environmental change and prolonged disturbances through population-level genomic variation.

microbiology↗

Global geography outweighs long-term dynamics in shaping marine microbial population structure

Marine microbial populations play essential roles in ocean ecosystems, yet the processes shaping their genomic structure across space and time remain poorly understood. Here, we examined the population-scale patterns of 1,505 prokaryotic metagenome-assembled genomes (MAGs) retrieved from the Northwestern Mediterranean Sea in two long-term coastal time series, along 15 and 7 years in these sites, as well as in the global ocean. We found that populations were generally more genomically differentiated across large spatial scales than across long temporal scales. Among a subset of 389 MAGs well represented in all datasets, 68.4% showed weak population divergence over time but strong global-scale differentiation. This was evident in the abundant and widespread cyanobacteria Prochlorococcus and Synechococcus. In contrast, only 6.4% of the MAGs exhibited weak divergence over time and space, with SAR11 MAGs being a clear example, likely reflecting their high dispersal and recombination rates. Other groups, such as SAR86 and Flavobacteriales, showed strong divergence at temporal and spatial scales, suggesting seasonal and/or regional adaptation. Positive selection was more readily detectable in the long-term coastal observatories than in the global ocean, despite the more significant population divergence observed across broad geographic scales. Temperature consistently showed a significant association with the population structure of many MAGs. Overall, our results highlight the dominant influence of large geographic scales in shaping microbial population structure alongside taxon-specific responses to temporal variation, particularly seasonality. Altogether, our work advances the understanding of microbial population structure across broad spatial and temporal scales, a critical step toward predicting microbial dynamics in a changing ocean.

ecology↗

Microbiome composition and function vary with depth in the Mediterranean gorgonian Eunicella singularis

BackgroundThe Gorgonian coral, Eunicella singularis, is one of the main components of Mediterranean marine animal forests, whose canopies play a key role in Mediterranean sublittoral ecosystems due to their capacity to provide shelter, food, and nursery ground to several species. Like other gorgonian species, E. singularis faces environmental threats with potential repercussions on the associated biodiversity. This photophilic octocoral, spanning the Western Mediterranean, Adriatic, and Aegean Seas at depths of 10-70m, engages in symbiosis with Symbiodiniaceae dinoflagellates, thereby influencing their resilience in nutrient-poor habitats. However, mesophotic populations ([~]60m depth) are characterized by very low Symbiodiniaceae density, prompting questions regarding metabolic adaptations. The associations of corals with specific bacteria that differ from those in the surrounding seawater suggest a role in host health and physiology. In particular, in mesophotic colonies, bacteria may perform activities that Symbiodinium typically carries out in shallow colonies. Here, we applied metagenomics techniques to analyze the changes in the microbiome of Eunicella singularis with depth, analyzing DNA samples from shallow (12m) and mesophotic (57m) colonies in the Northwestern Mediterranean Sea. ResultsHigh-coverage metagenomes (ca. 80 Gb per sample) were generated from E. singularis colony samples. We observed significant changes in the relative abundance of prokaryotic and microbial eukaryotic symbionts with depth. Mesophotic samples exhibited higher levels of symbiotic prokaryotes, dominated by Endozoicomonas and Bermanella, whereas shallow samples were enriched with the symbiotic dinoflagellate Symbiodiniaceae. The metabolic potential of the microbiome also varied with depth. The shallow microbiome showed a prevalence of photosynthesis and carbon fixation pathways. In turn, the mesophotic microbiome exhibited a higher abundance of metabolic functions related to vitamin biosynthesis, energy metabolism, especially carbon metabolism, as well as pathways associated with carbohydrates, amino acids, and cofactors. ConclusionsOur results indicate that the structure and metabolic function of the microbiome of Eunicella singularis change with depth. In the absence of symbiotic dinoflagellates, associated bacteria seem to use different sources of carbon, in addition to cycling nutrients and vitamins, which could influence coral health. These findings gain significance in the context of global change, as shifts in oceanic conditions may affect the coral microbiome.

ecology↗

Metagenomic-based network analysis reveals the importance of vitamin cross-feeding in marine microbial assemblages

Vitamins play a fundamental role in microbial metabolism and interactions, yet their scarcity in marine environments and the limited ability for de novo synthesis of some vitamins often leads to metabolic dependencies and cross-feeding among microbial taxa. Using a decade-long time-series metagenomics dataset from the Blanes Bay Microbial Observatory (BBMO), we investigated the role of vitamin biosynthesis in structuring the seasonal marine microbial interactions among prokaryotes and eukaryotes. Gene co-occurrence analysis revealed that vitamin-related metabolism had the highest number of associations among all metabolic pathways, underscoring the potential role of vitamins in microbial interactions. Metagenome-assembled genome (MAG) co-occurrence analysis further identified the prokaryotic biosynthesis of cobalamin (B12) and thiamine (B1) as key mediators of these associations. Rather than between complete vitamin synthesizers and auxotrophs, the main associations were found between partial synthesizers, suggesting that vitamer cross-feeding may represent an essential microbial interaction in sustaining vitamin biosynthesis throughout the year. While complete cobalamin synthesizers dominate in summer, partial synthesizers and lower-ligand activators are more prevalent in winter, driving cross-feeding interactions. In contrast, thiamine biosynthesis is more widespread, with complete synthesizers peaking in winter. The association strength, however, was maximum between prokaryotic vitamin producers and eukaryotes, highlighting the dependence of eukaryotes on bacterial vitamin production. These results provide novel insights into seasonal metabolic interdependencies, emphasizing the ecological significance of vitamin biosynthesis in marine ecosystems.

microbiology↗

Global population structure of a unicellular marine predator

Unicellular predators, especially marine heterotrophic flagellates (HFs), are fundamental to marine food webs, facilitating the flow of nutrients from bacteria and the smallest primary producers to upper trophic levels. Comprehending their distributions and diversity is essential for understanding the functioning of marine ecosystems. The uncultured MArine STramenopiles clade 4 (MAST-4) constitutes a crucial HF member of the ocean microbiome with a predatory (bacterivorous) lifestyle. Temperature gradients have influenced the evolution and biogeography of MAST-4 species. Yet, similarly to most uncultured microbes, there is limited information on the population diversity and structure within MAST-4 species. This information is key for better comprehending the ecological roles and adaptations of different MAST-4 species to specific ocean niches. Here, we investigate the population diversity and structure on the global scale of the MAST-4 species A, B, C, and E by combining metagenomics and single-cell genomics data from the Tara Oceans expedition. We found substantial population divergence in the abundant MAST-4A and C species, while lower levels of divergence were observed in species B and E. Temperature and salinity were the main drivers structuring the populations within the four MAST-4 species. The analysis of positively selected gene clusters within each MAST-4 species revealed genomic areas likely the basis of population adaptation to different niches. Overall, our results contribute to a better comprehension of the population diversity and structure of four species belonging to an important group of unicellular predators, offering insights into their ecological roles and adaptations in the global ocean. The results also contribute to understanding microbial populations, a dimension of diversity that remains poorly known for most wild species and is pivotal in global change.

ecology↗

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↗

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↗