Marinna Gaudin

Microalgal-bacterial interactions are central to nutrient cycling and ecosystem functioning in marine habitats, yet the mechanisms structuring these associations under defined nutrient constraints remain poorly resolved. Using a synthetic 15-member bacterial community (SynCom) and controlled nitrogen (N), phosphorus (P), and vitamin B12-limitation, we investigated how nutrient scarcity shapes the physiology, metabolism, and transcriptional activity of the harmful alga Prymnesium parvum and its associated microbiota. Under N- and P-limitation, the SynCom had minimal impact on algal growth despite nutrient-dependent shifts in toxin production and metabolite profiles. In contrast, B12-limitation triggered a strong mutualistic interaction in which the SynCom enabled a three-fold increase in algal biomass and drove restructuring of intracellular and extracellular metabolomes, including the accumulation of ectoine and membrane-associated lipids and the depletion of thiamine-like and stress-associated metabolites. Metabarcoding revealed stable community composition but enrichment of B12-producing taxa under B12-limited conditions, while metatranscriptomics uncovered functional divergence among SynCom members. Bacteria displayed contrasting response strategies, including nutrient-responsive specialists and transcriptionally flexible generalists maintaining gene expression across all nutrient regimes. B12-producers (Marinovum algicola, Roseobacter sp., Halomonas sp.) upregulated cobalamin biosynthesis exclusively under B12-limitation, whereas several B12-auxotrophic taxa induced B12-transport and B12-requiring enzymes, indicating active vitamin exchange within the holobiont. P. parvum displayed transcriptional programs specific to each nutrient limitation, with B12-limited co-cultures shifting toward growth-associated gene expression despite constitutive expression of the B12-dependent metH gene. These results demonstrate that vitamin auxotrophy acts as a key metabolic lever reorganizing holobiont function, driving reciprocal benefits and reprogramming algal-bacterial metabolism in our synthetic system.

Microalgal-bacterial interactions are central to nutrient cycling and ecosystem functioning in marine habitats, yet the mechanisms structuring these associations under defined nutrient constraints remain poorly resolved. Using a synthetic 15-member bacterial community (SynCom) and controlled nitrogen (N), phosphorus (P), and vitamin B12 limitation, we investigated how nutrient scarcity shapes the physiology, metabolism, and transcriptional activity of the harmful alga Prymnesium parvum and its associated microbiota. Under N- and P-limitation, the SynCom had minimal impact on algal growth despite nutrient-dependent shifts in toxin production and metabolite profiles. In contrast, B12-limitation triggered a strong mutualistic interaction in which the SynCom enabled a three-fold increase in algal biomass and drove restructuring of intracellular and extracellular metabolomes, including the accumulation of ectoine and membrane-associated lipids and the depletion of thiamine-like and stress-associated metabolites. Metabarcoding revealed stable community composition but enrichment of B12-producing taxa under B12-limited conditions, while metatranscriptomics uncovered functional divergence among SynCom members. Bacteria segregated into specialized B12- or N-responsive strains and metabolically plastic generalists sustaining broad transcriptional activity across all nutrient regimes. B12 producers ( Marinovum algicola , Roseobacter sp., Halomonas sp.) upregulated cobalamin biosynthesis exclusively under B12 limitation, whereas several dependent taxa induced B12 transport and B12-requiring enzymes, indicating active vitamin exchange within the holobiont. P. parvum displayed nutrient-specific transcriptional programs, with B12-limited co-cultures shifting toward growth-associated gene expression despite constitutive expression of the B12-dependent metH gene. These results demonstrate that vitamin auxotrophy acts as a key metabolic lever reorganizing holobiont function, driving reciprocal benefits and reprogramming algal-bacterial metabolism in our synthetic system.

Marine microbial communities are fundamental to nutrient and biogeochemical cycling, with intricate networks of metabolic interdependencies influencing their structure and dynamics. Among these, vitamins B₁ (thiamin) and B₁₂ (cobalamin) play crucial roles as enzymatic cofactors in central metabolic pathways. Despite their importance, the temporal dynamics of vitamin production, bioavailability, and associated microbial interactions, remain poorly understood. Using a 7-year monthly metagenomic time series from the NW Mediterranean Sea (SOLA station), we found that vitamin B₁/B₁₂ auxotrophs (need for an exogenous vitamin source) were present throughout the year. Among B₁ auxotrophs, those requiring the thiamin precursor HMP were the most prevalent, with peak abundances in summer. Distinct metagenome-assembled genome co-abundance patterns between B₁ and B₁₂ producers/auxotrophs across seasons suggested mutualistic relationships. Double B₁/B₁₂ vitamin complementarities were more common in summer, and single vitamin complementarity was dominant in winter. As previously shown for vitamin B₁₂, which is limiting during winter, bioassays revealed variable availability of vitamin B₁ in winter seawater despite the abundance of its producers, suggesting potential transfer of vitamin B₁ among microorganisms. Finally, microcosm experiments showed that B₁ and B₁₂ amendments significantly influenced the composition of microbial communities, with temporal variations in their impact. In some cases, B₁₂ and B₁ amendments favored both vitamin auxotrophs and producers, highlighting complex interdependencies between B₁ and B₁₂ producers and consumers. Our findings highlight the complexity of B vitamin-mediated metabolic interactions that shape microbial community dynamics and underscore the need for long-term, high-resolution studies to better understand vitamin-driven ecological processes in marine systems.

Understanding the drivers and consequences of horizontal gene transfer (HGT) is a key goal of microbial evolution research. Although co-occurring taxa have long been appreciated to undergo HGT more often, this association is confounded with other factors, most notably their phylogenetic relatedness. To disentangle these factors, we analyzed 15 339 marine prokaryotic genomes (mainly bacteria) and their distribution in the global ocean. We identified HGT events across these genomes and enrichments for functions previously shown to be prone to HGT. By mapping metagenomic reads from 1862 ocean samples to these genomes, we also identified co-occurrence patterns and environmental associations. Although we observed an expected negative association between HGT rates and phylogenetic distance, we only detected an association between co-occurrence and phylogenetic distance for closely related taxa. This observation refines the previously reported trend to closely related taxa, rather than a consistent pattern across all taxonomic levels, at least here within marine environments. In addition, we identified a significant association between co-occurrence and HGT, which remains even after controlling for phylogenetic distance and measured environmental variables. In a subset of samples with extended environmental data, we identified higher HGT levels associated with particle-attached prokaryotes and associations of varying directions with specific environmental variables, such as chlorophyll a and photosynthetically available radiation. Overall, our findings demonstrate the significant influence of ecological associations in shaping marine prokaryotic evolution through HGT.

Understanding the drivers and consequences of horizontal gene transfer (HGT) is a key goal of microbial evolution research. Although co-occurring taxa have long been appreciated to undergo HGT more often, this association is confounded with other factors, most notably their phylogenetic relatedness. To disentangle these factors, we analyzed 15,339 marine prokaryotic genomes (mainly bacteria) and their distribution in the global ocean. We identified HGT events across these genomes and enrichments for functions previously shown to be prone to HGT. By mapping metagenomic reads from 1,862 ocean samples to these genomes, we also identified co-occurrence patterns and environmental associations. Although we observed an expected negative association between HGT rates and phylogenetic distance, we only detected an association between co-occurrence and phylogenetic distance for closely related taxa. This observation refines the previously reported trend to closely related taxa, rather than a consistent pattern across all taxonomic levels, at least here within marine environments. In addition, we identified a significant association between co-occurrence and HGT, which remains even after controlling for phylogenetic distance and measured environmental variables. In a subset of samples with extended environmental data, we identified higher HGT levels associated with particle-attached bacteria and associations of varying directions with specific environmental variables, such as chlorophyll a and photosynthetically available radiation. Overall, our findings demonstrate the significant influence of ecological associations in shaping marine bacterial evolution through HGT.

Marine plankton communities form intricate networks of interacting organisms at the base of the food chain, and play a central role in regulating ocean biogeochemical cycles and climate. However, predicting plankton community shifts in response to climate change remains challenging. While species distribution models are valuable tools for predicting changes in species biogeography under climate change scenarios, they generally overlook the key role of biotic interactions, which can significantly shape ecological processes and ecosystem responses. Here, we introduce a novel statistical framework, association distribution modelling (ADM), designed to model and predict ecological associations distribution in space and time. Applied on a Tara Oceans genome-resolved metagenomics dataset, the present-day biogeography of ADM-inferred marine plankton associations revealed four major biogeographic biomes organized along a latitudinal gradient. We predicted the evolution of these biome-specific communities in response to a climate change scenario, highlighting differential responses to environmental change. Finally, we explored the functional potential of impacted plankton communities, focusing on carbon fixation, outlining the predicted evolution of its geographical distribution and implications for ecosystem function. This article is part of the theme issue ‘Connected interactions: enriching food web research by spatial and social interactions’.

Marine microorganisms form complex communities of interacting organisms that influence central ecosystem functions in the ocean such as primary production and nutrient cycling. Identifying the mechanisms controlling their assembly and activities is a major challenge in microbial ecology. Here, we integrated Tara Oceans meta-omics data to predict genome-scale community interactions within prokaryotic assemblages in the euphotic ocean. A global genome-resolved co-activity network revealed a significant number of inter-lineage associations across diverse phylogenetic distances. Identified co-active communities include species displaying smaller genomes but encoding a higher potential for quorum sensing, biofilm formation, and secondary metabolism. Community metabolic modelling reveals a higher potential for interaction within co-active communities and points towards conserved metabolic cross-feedings, in particular of specific amino acids and group B vitamins. Our integrated ecological and metabolic modelling approach suggests that genome streamlining and metabolic auxotrophies may act as joint mechanisms shaping bacterioplankton community assembly in the global ocean surface.