ISME Communications

Microbial plankton play fundamental roles in biogeochemical cycles, driving nutrient cycling that influences the global climate and supports life on Earth. Picoplankton are the smallest and most abundant planktonic organisms. The distribution and ecology of these organisms is determined by environmental factors and their biogeography is largely shaped by basin-scale patterns of physicochemical composition of ocean waters. The increased availability of high-throughput sequencing data of microbial communities has enabled the description of how the global oceans are partitioned into distinct microbial biogeographical provinces. However, the key attributes associated with such provinces are still unclear. Here we present a model of picoplankton biogeography based on 1454 metagenomes from multiple sampling consortia, resulting in the largest integrated surface ocean metagenome analysis to date. We identify ten distinct groups based on metagenomic dissimilarity, divided into three categories: polar (Arctic and Antarctic), temperate (coastal temperate, temperate/subtropical transition, oceanic temperate, Mediterranean-like) and tropical (tropical low nutrient, tropical high nutrient, subtropical oceanic gyres). Using machine learning and omics data integration techniques, we predict province areas across the surface oceans and describe their environmental, taxonomical, and functional features. We quantify the relationship between environmental factors and each biogeographical province, identify their main representative taxa and the importance of carbon degradation and antimicrobial resistance pathways in functional community composition, and discuss implications for establishing a model for global picoplankton biogeography.

Linking bacteriophages (phages) to their hosts remains a fundamental challenge to understanding microbial ecology, viral evolution, and horizontal gene transfer. Although phages are the most abundant biological entities on Earth, the majority of them remain uncharacterized due to the lack of efficient host-linking approaches. Traditional methods, such as plaque assays, have significant limitations as they depend on visible lysis and therefore fail to detect phages that do not form plaques. Conversely, shotgun metagenomics can recover viral genomes directly from environmental samples; however, it cannot directly link phages to their bacterial hosts. In this study, we addressed this limitation by tackling the critical question of "who infects whom?" through the development of a novel, culture-independent approach that utilises an anucleate bacterial minicells-based platform to enrich for phages capable of infecting a target bacterial host. To validate our approach, purified Escherichia coli minicells were exposed to a concentrated viral fraction derived from sewage samples. Genomic DNA from phages that successfully infected and interacted with the E. coli minicells was isolated, amplified, and sequenced. Metagenomic analysis revealed a distinct E. coli-specific virome, including several putatively novel phage species and genera. This platform effectively bridges the gap between culture-dependent and metagenomic methods, providing a scalable, host-targeted tool for identifying phage-host pairs. Our approach also opens new opportunities for studying phage-host interaction networks in complex microbial ecosystems and enhances our ability to investigate viral diversity, host specificity, and the ecological roles of phages in natural environments.

Semi-permeable capsules (SPCs) create enclosed porous microenvironments, diffusible to only small proteins and macromolecules. This presents a powerful tool for single cell observation, isolation, and sequencing. However, their range of use for sustaining viable microbial eukaryotes is largely unexplored. Single-cell eukaryotes are often understudied, with a wealth of unknown lifecycles, culturing methods and inter-microbial interactions, which are difficult to visualize. Here, we show that eukaryotes from eight different supergroups can be captured and propagated in SPCs. Encapsulation allowed observations of cell stages, motility and growth in a traceable and parallelized manner.

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.

The surface ocean exhibits strong vertical gradients in light, nutrients, and temperature, shaping the phytoplankton distribution which often defines a deep chlorophyll maximum (DCM). Aerobic anoxygenic phototrophic (AAP) bacteria inhabit the euphotic zone, with their abundances following the chlorophyll a variability. While AAP bacterial communities are known to differ across regions with contrasting environmental conditions, their vertical distribution remains poorly understood. We hypothesized that the diversity and community structure of AAP bacteria would vary across the vertical gradient, in relation to changes in environmental variables and following the DCM profile. To test this hypothesis, we studied the composition of AAP communities at different depths along the DCM structure in the South and Central Atlantic Ocean, by means of amplicon sequencing of the pufM gene. The results show significant differences in richness, community structure, and taxonomic composition of samples from different layers of the DCM, highlighting the dependance of AAP bacteria on its structure. Remarkably, the use of primers with broad phylogenetic coverage enabled the recovery of several phylogroups previously detected only through metagenomics. We show that they represent a significant fraction of marine AAP communities, provide clues on their ecological preferences, and confirm their association with the family Candidatus Luxescamonaceae, with genomic potential for carbon fixation.

BackgroundCloud water harbors diverse microbial communities despite its extreme oligotrophic conditions. However, the ecological and evolutionary dynamics of viruses in these transient atmospheric habitats remain poorly understood. Clouds have traditionally been regarded primarily as passive carriers of microorganisms rather than as active ecological environments supporting microbial interactions. In this study, cloud water was sampled at Mount Verde, Cape Verde Islands (744 m a.s.l.). We performed metagenomic analyses of iron-flocculated cloud water alongside genome analyses of a bacterial isolate and metagenome-assembled genomes using established bioinformatic approaches. Viral diversity, virus-host interactions, metabolic functions, genetic adaptations, and viral population dynamics across cloud events were investigated. In addition, UV-B resistance experiments were conducted for a novel cloud-water isolate. ResultsWe isolated 24 cloud water bacteria, including four novel species lineages, and recovered 62 high-quality metagenome-assembled genomes, including 10 novel species lineages. We identified 458 viral operational taxonomic units and 237 virus-host linkages across diverse prokaryotic hosts, revealing active viral predation across diverse bacterial taxa. In addition, CRISPR spacer matches from isolates of novel bacterial lineages such as Deinococcus nubigenus MPC36 were found. Viruses carried genes involved in host adaptation to environmental stressors, including cold-shock response, UV radiation resistance, and osmotic stress. In addition, viral populations exhibited SNP-level microdiversity and shifts in single-nucleotide variant composition across temporally proximate cloud events, indicating rapid population turnover. Experimental characterization of the cloud isolate Curtobacterium nubigenum MPC39 further revealed pronounced resistance to UV-B radiation and the presence of an inducible prophage, Curtobacterium phage vB_CnuS_Cirrus1 assigned to the new viral family Nebulaviridae, which could be validated in transmission electron microscopy. Reconstructed genomes from cloud-associated bacteria encoded carbon monoxide dehydrogenase genes and UV resistance genes, suggesting trace gas metabolism and enhanced UV protection as survival strategies in oligotrophic cloud droplets. In silico replication rates estimated using iRep were consistent with active bacterial replication at the time of sampling. ConclusionsTogether, these findings demonstrate that clouds are not merely passive carriers of microorganisms, but dynamic atmospheric ecosystems in which virus-host interactions shape microbial diversity and contribute to microbial turnover, atmospheric dispersal, and cloud-water biogeochemistry.

Chlorophyll is one of the most abundant pigments on Earth. Although its degradation is well understood in plants, the role of prokaryotes in this process - despite their vast metabolic capabilities - remains unknown. Recent developments in the field of AI-predicted protein structures have opened new avenues for investigating functional homologies between evolutionary-distant organisms previously inaccessible through traditional sequence- or profile-based methods. Here, we present the first evidence of Chlorophyll a (Chl a) degradation by prokaryotes, discovered through a novel bioinformatic framework which bridges the gap across the domains of life via structural alignments of functionally characterised plant proteins, followed by structure similarity graph-based clustering. Metagenomic sequencing data was assembled and binned, yielding over 70,000 medium- to high-quality genomes in total, furthermore publicly available datasets containing genomes from prokaryotic isolates, metagenome-assembled genomes, as well as single-cell genomes were then mined for prokaryotic homologues of Chl a degradation genes. Our analysis revealed over 400 genomes from diverse taxonomic groups and habitats that possess a complete pathway, more than 50% stemming from isolates. Additionally, many other genomes harbour partial pathways, suggesting that Chl a degradation capabilities are globally widespread across diverse ecosystems. We then validated our in silico findings using the model organism Shewanella acanthi and confirmed its Chl a degradation capability via growth experiments, fluorescence spectroscopy and HPLC analyses. Our findings reveal a previously unrecognised pathway in prokaryotes, highlighting the power of structure-based remote homology detection for uncovering metabolic capabilities and evolutionary relationships.

Hydrocarbons are vital for energy production and lead to serious environmental issues due to pollution. Microorganisms largely drive the production and degradation of hydrocarbons, yet little is known about viral contributions to hydrocarbon degradation. Here we identified 786 viral contigs from IMG/VR(v4), encoding five aerobic (alkB, ladA, almA, ndoB and dszC) and three anaerobic (bssA, ebdA and abcA) hydrocarbon-degrading genes (HDGs). vOTUs encoding HDGs span 26 distinct viral families, including 249 are mainly associated with host-associated environment and 463 are derived from aquatic habitat, respectively, implying that these viruses are broadly engaged in hydrocarbon-degradation processes across the entire biosphere. alkB (35%) and almA (28%) was tended to be encoded by Schizomimiviridae, bssA was tended to be encoded by T5-like bacteriophages (29%) and SPO1-like bacteriophages (22%), suggesting that the carriage of HDGs by viruses exhibits taxonomic specificity. With respect to host associations, Pseudomonadota and Bacillota constitute the two main potential host lineages, associated with 268 and 71 vOTUs, respectively. The profiling of ecological footprint reveals that viruses contribute a total of up to 30% gene abundance and 32% transcribing activity to hydrocarbon degradation in the global ocean. This study systematically revealed the distribution, diversity, virus-host correlation and activity of virus-encoded HDGs, underscoring the significant role of viruses in hydrocarbon metabolism on a global scale.

Viruses shape microbial community structures, impacting metabolic pathways and influencing biogeochemical cycles. Despite their importance, the influence of biotic and abiotic factors on viral community structures across environmental gradients in soil is relatively unknown compared to their prokaryotic hosts. While soil pH strongly influences microbial community structure, it is unclear whether there is a similar influence on soil virus communities. In this study, prokaryotic and viral communities were characterized in soils sampled from the extremes of a long-term pH-manipulated soil gradient (pH 4.5 and 7.5), and viral populations were compared to those in a variety of soil ecosystems ranging in pH (4.0 - 7.5). Prokaryotic and viral community structure were significantly influenced by soil pH at the local scale. Of 1,910 viral operational taxonomic units (vOTUs), 99% were restricted to pH 4.5 or 7.5 soil only. These were compared in gene sharing networks of populations from six other European and North American soil systems. A selection of viral clusters from acidic and neutral pH soils were more associated with those from the local gradient pH 4.5 or 7.5 soils, respectively. Results indicate that as with prokaryotes, soil pH is a factor structuring viral communities at the local and global scale.

The coupling between ocean and atmosphere across the strong seasonal gradients in the Arctic is poorly understood. Here, we explored the microbial and glycobiological connectivity between the sea surface microlayer (SML), the underlying seawater (ULW), snow, and aerosol particles in Kongsfjorden (Svalbard, 79{degrees}N) during autumn and spring. The marked overlap between marine and atmospheric microbiomes illustrates considerable sea-air transfer, linked to seasonally distinct environmental communities. For instance, Polaribacter and Formosa were aerosolized during the spring bloom, compared to Colwellia in autumn. Air-mass trajectories and microbial source tracking revealed a greater marine contribution in autumn, whereas spring aerosols were shaped by stronger winds and the cryosphere. Aerosol particles nonetheless contained numerous unique taxa, including Actinobacteria likely originating from terrestrial sources. Linking bacterial, microeukaryotic, carbohydrate, and meteorological dynamics established an overarching perspective across seasons and habitats, identifying four distinct ecosystem states. Genome-sequenced bacterial model isolates, representing key environmental populations, encode adaptive traits such as carotenoid and ectoine biosynthesis, supporting survival in the SML and atmospheric transfer. Comparison with time-series records from the nearby Fram Strait revealed that many aerosolized bacteria are consistent microbiome components; with implications for ecology and biogeochemistry across the wider Arctic.

The keystone species concept suggests that certain members of an ecological community, despite their low abundance, exert disproportionately large effects on species diversity and composition. In microbial ecology, experimental validation of this concept is limited due to significant technical challenges associated with selective species manipulation. Here, we tested this concept within a soil microbial food web by selectively suppressing a protist predator using phototoxicity induced by excessive excitation light during fluorescence microscopy within a microfluidic soil chip system. We targeted a Hypotrichia ciliate taxon--presumed primarily bacterivorous under our experimental conditions--and combined microscopy with metabarcoding of multiple microbial trophic levels to evaluate the effects of this suppression on microbial community abundance, diversity, and composition. Over the 20-day incubation, the chip system supported complex communities of bacteria, fungi, and protists. Following Hypotrichia suppression, two distinct ecological responses were observed: first, an increase in flagellate abundance that was consistent with mesopredator release and accompanied a significant rise in overall protist diversity; second, a convergence in protist community composition, indicative of biotic homogenization. Surprisingly, bacterial community abundance, richness, and composition remained unaffected, likely due to compensatory predation by increased numbers of bacterivorous flagellates. In contrast, fungal diversity decreased following Hypotrichia suppression, presumably resulting from the altered protist communities that favored facultative fungal consumers. Collectively, these findings provide direct experimental evidence that low-abundance microbial predators can function as keystone species, modulating predator community composition and diversity and having cascading effects on lower trophic levels within the brown microbial food web.

Marine viruses are key players of ocean biogeochemistry, profoundly influencing microbial community ecology and evolution. Despite their importance, few studies have explored the temporal dynamics of viral genome abundances in marine environments. Viral dynamics are complex, influenced by multiple factors such as host population dynamics and environmental conditions. To disentangle the complexity of viral communities, we developed an unsupervised machine learning framework to classify viral genomes into "chronotypes" based on temporal abundance patterns. Analysing an inter-seasonal monthly time-series of surface viral metagenomes from the Western English Channel, we identified chronotypes and compared their functional and evolutionary profiles. Results revealed a consistent annual cycle with steep compositional changes from winter to summer and steadier transitions from summer to winter. Seasonal chronotypes were enriched in potential auxiliary metabolic genes like ferrochelatases and 2OG-Fe(II) oxygenases compared to non-seasonal types. Chronotypes clustered into four groups based on their correlation profiles with environmental parameters, primarily driven by temperature and nutrients. Viral genomes exhibited a rapid turnover of polymorphisms, akin to Red Queen dynamics. However, within seasonal chronotypes, some sequences exhibited annual polymorphism recurrence, which declined over a 16-month period, suggesting that a fraction of the seasonal viral populations evolve more slowly. Classification into chronotypes revealed viral genomic signatures linked to temporal patterns, likely reflecting metabolic adaptations to environmental fluctuations and host dynamics. This novel framework enables the identification of long-term trends in viral composition, environmental influences on genomic structure, and potential viral interactions.

Bacterial bloomers,populations that experience rapid and significant increases in abundance in response to environmental triggers, briefly dominate marine microbial communities, potentially impacting the ecosystem by channeling large amounts of nutrients and affecting carbon fluxes. Due to their ephemeral nature, bacterial bloomers are challenging to capture, and it remains unknown whether they are restricted to specific taxonomic groups or whether they exhibit recurrent patterns. We analyzed a decade-long time series from the Blanes Bay Microbial Observatory (BBMO, NW Mediterranean Sea) to investigate bacterial bloomers in two size fractions (free-living (0.2-3 um) and particle-attached (3-20 um) communities. We identified 57 Amplicon Sequence Variants (ASVs), less than 1% of the total bacterial richness, exhibiting recurrent or chaotic blooming-like behavior. Bloomers spanned diverse phyla, though some taxonomic coherence appeared within families containing multiple blooming taxa. Monthly sampling detected bloom events on average 4.6 +- 1.9 times per year across both size fractions. Once seasonality was accounted for, blooms showed weak associations with biological and physicochemical variables, likely a consequence of monthly sampling resolution. Nonetheless, a marked shift in the blooming community within the particle-attached size fraction coincided with ecosystem disturbances from the nearby harbour restoration, suggesting that bloomers may act as disturbance sentinels. Metagenomic data showed that blooms led to marked shifts in the community functional potential. Overall, our findings underscore the importance of investigating bloom dynamics to understand microbial contributions to biogeochemical cycles and stress the need for higher-frequency sampling to accurately capture these transient but ecologically relevant events.

BackgroundBacteria of the Candidate Phyla Radiation (CPR), constituting about 25% of the bacterial biodiversity, are characterized by small cell size and patchy genomes without complete key metabolic pathways, suggesting a symbiotic lifestyle. Gracilibacteria (BD1-5), which are part of the CPR branch, possess alternate coded genomes and have not yet been cultivated. However, besides genomic evidence, little is known about the lifestyle of Gracilibacteria, their temporal dynamics, and activity in natural ecosystems, particularly in groundwater, where they were initially been genomically resolved. Therefore, we here aimed to investigate Gracilibacteria activity in situ and to discern expressed genes involved in their lifestyle, using the metaproteogenome of Gracilibacteria as a function of time in the cold-water geyser Wallender Born in the Volcanic Eifel region in Germany. ResultsWe coupled genome-resolved metagenomics and metaproteomics to investigate a cold-water geyser microbial community enriched in Gracilibacteria across a 12-day time-series. Groundwater was collected and sequentially filtered to fraction CPR and other bacteria. Based on 670 Gbps of metagenomic data, 1129 different ribosomal protein S3 marker genes and 751 high-quality genomes (123 population genomes after dereplication), we identified dominant bacteria belonging to Galionellales and Gracilibacteria along with keystone microbes, which were low in genomic abundance but substantially contributing to proteomic abundance. Seven high-quality Gracilibacteria genomes showed typical limitations, such as limited amino acid or nucleotide synthesis, in their central metabolism but no co-occurrence with potential hosts. The genomes of these Gracilibacteria encoded for a high number of proteins related to a symbiotic or even predatory lifestyle, e.g., type IV and type II secretion system subunits and features related to cell-cell interactions and cell motility, which were also detected on protein level. ConclusionsCoupling metagenomics to metaproteomics enabled us to identify microbial keystone taxa in a high-CO2 aquifer, and to reveal microbial dynamics of Gracilibacteria. We posit that Gracilibacteria might be successful microbial predators in this ecosystem, potentially aiding in population control of this highly perturbed microbial geyser community from the deep biosphere.

Understanding how microbial populations respond to disturbances represents a major goal for microbial ecology. While several theories have been advanced to explain microbial community compositional changes in response to disturbances, appropriate data to test these theories is scarce, especially when considering the challenges to define rare vs. abundant taxa and generalists vs. specialists, a prerequisite for testing the theories. Here, we define these two key concepts by employing the patterns of coverage of a (target) genome by a metagenome to define rare populations, and by borrowing concepts from macroecology, the proportional similarity index (PS index), to define generalists. Using these concepts, we found that coastal microbial communities are resilient to major perturbations such as tropical cyclones and (uncommon) cold or warm weather events snaps-in part-due to the response of rare populations, providing support for the insurance hypothesis (i.e., the rare biosphere has the buffering capacity to mitigate the effects of disturbances). Generalists appear to contribute proportionally more than specialists to community adaptation to perturbations like warming, supporting the disturbance-specialization hypothesis, i.e., disturbance favors generalists. Taken together, our results advance understanding of the mechanisms governing microbial populations dynamics under changing environmental conditions and have potential applications for ecosystem management.

BackgroundBrazilian sponges of the genus Metania (phylum Porifera) are filter-feeding organisms from freshwater ecosystems. Here, we explored viral communities of Metania sp., their functional role in the sponge and how they differ from those in surrounding water. ResultsWe identified 1163 viral operational taxonomic units (vOTUs) from sponge tissue and adjacent water, with 555 vOTUs shared across habitats. Viral diversity was higher in sponges than in water, and community composition differed significantly (PERMANOVA, p = 0.037). Sponge-associated vOTUs exhibited broad phylogenetic diversity, including deep-branching and unclassified clades, and several exclusively sponge-associated Caudoviricetes. Virus-host predictions revealed 173 interactions, largely with sponge-associated bacteria, supported by CRISPR spacer matches, variant formation in multiple vOTUs across sponge individuals, and a high prevalence of microbial defence systems, particularly restriction-modification, abortive infection, and CRISPR-Cas pathways. Functionally, viral communities carried diverse auxiliary viral genes, including those involved in amino acid and central carbon metabolism, carbohydrate degradation, fatty acid biosynthesis, stress responses (e.g., metacaspase-1), and sulphur cycling. Nine sponge-associated vOTUs encoded carbonic anhydrase (CA), and phylogenomic as well as structural analyses showed strong conservation of CA active sites between sponge viruses, bacterial symbionts, and the sponge host. Protein-level homology searches revealed broad biogeographic distribution of viral CA homologs across global ocean microbiomes, despite limited nucleotide similarity, highlighting deep functional conservation. ConclusionsThese findings reveal a phylogenetically diverse and functionally rich viral community associated with freshwater Metania sp., characterized by extensive host interactions, diverse defence mechanisms, and auxiliary metabolic capacities. The structural conservation and widespread distribution of viral carbonic anhydrase genes further suggest ecologically significant roles in carbon transformation within freshwater sponges and potentially across aquatic ecosystems.

Competition for light has driven extensive pigment diversification among phytoplankton species, yet how this diversity shapes their spatiotemporal distribution in the field has been little studied so far. The cyanobacterium Synechococcus is an ideal model for addressing this issue, since this group has colonized most light spectral niches in marine environments. Here, we used an approach based on marker read recruitment from metagenomes to analyze the seasonal succession of Synechococcus pigment types (PTs) at two time-series stations off French coasts exhibiting contrasting oceanic regimes. Marked seasonality was observed at both sites. The shallow, permanently mixed English Channel site SOMLIT-Astan was characterized by an alternation between green-light specialists (PT 3a) peaking in spring, and chromatic acclimaters type A (PT 3dA) accounting for most of the Synechococcus community in winter. In contrast, the pigment diversity was much higher at the deep Mediterranean station BOUSSOLE. In the upper layer, the two main PTs were the blue light specialists (PT 3c), which dominated the community in summer and fall, and PT 3dA cells, which were more abundant in spring. The third most abundant PT was chromatic acclimaters type B (PT 3dB), which accounted for up to 15% of the surface community in late fall. Strikingly, PT 3dA was dominant at depth during most of the year. Multivariate analyses between PT abundances, clade abundances and environmental factors, notably water color indexes, suggested new associations between PTs to specific clades and ecological niches. This study provides novel insights for refining distribution models of Synechococcus PTs and phytoplankton groups in general.

Virus-host interactions are fundamental drivers of microbial community structure, yet whether viral ecological niches are confined within individual host niches (nested host niche scenario) or span multiple hosts and exceed any single host niche (expanded host niche scenario) remains poorly understood. To explore these patterns, we characterized prokaryotic and viral distributions and predicted virus-host interactions along a salinity gradient at Bras del Port salterns (Spain), ranging from seawater (3.6% salinity) to salt saturation (39.0%). We analyzed metagenomes and viromes from six ponds supplemented by 27 additional published viromes from the same hypersaline system, recovering 170 metagenome-assembled genomes (MAGs) dereplicated at the genomospecies level (MAGs clustered at 95 % average nucleotide identity), approximately 55,000 viral operational taxonomic units (vOTUs), and nearly 4,000 predicted virus-host pairs. Viruses exhibited broader niches than their putative hosts at the highest salinities, while at lower salinities the pattern was reversed or inconsistent depending on the site, and niche breadths of both viruses and hosts increased steadily toward higher salinities. Host taxonomy at the class level and below was the primary driver of viral genomic clustering, explaining more variance than salinity provenance (approximately 30% vs. approximately 19%), while the contribution of salinity to viral genomic composition appeared indirect, mediated through the salinity-driven distribution of distinct host classes rather than direct environmental filtering of viral sequences. Together, these findings support the expanded host niche scenario as the predominant virus-host interaction strategy, with evolutionary and ecological dynamics jointly shaped by salinity and host identity.

Temperature and light play a crucial role in regulating phytoplankton blooms in the Ocean. To assess the importance of these two parameters experimentally, microcosms were conducted on seven picoplankton communities (<3 m) sampled in December, March, June and September 2015 and 2016 in the North Western Mediterranean Sea. Each community was exposed to 4 realistic seasonal conditions (December, March, June and September). Metabarcoding was used to investigate the eukaryotic diversity in the 56 microcosms experiments in parallel to high-frequency monitoring of environmental diversity in the sea. The three major lineages identified were the Stramenopiles, Alveolata and Archaeplastida. Overall, the five-day incubations were not sufficient to reshape the initial microbial communities completely. The microcosm outcome was strongly influenced by the dynamics of phytoplankton starting communities. In pre-bloom conditions, phytoplanktonic species were the most sensitive to temperature and light conditions. During a bloom, species belonging to diatoms or Chlorodendrophyceae usually did not respond to light and temperature in microcosms and continued to bloom independently of the applied seasonal condition. Together, these results suggest that light and temperature seasonal conditions play a crucial role in regulating phytoplankton dynamics in pre-bloom conditions and biotic interactions may be preponderant in bloom and post-bloom conditions.

Blooming microalgae (phytoplankton) release diverse organic molecules that fuel the marine pools of dissolved and particulate organic matter. A highly specialized community of heterotrophic bacteria rapidly remineralizes substantial parts of this organic matter in the sun-lit upper ocean. In particular, microalgae produce large quantities of various organosulfur compounds that can serve as carbon and sulfur sources for bacteria. Here, we report on the analyses of a time series of previously generated 30 long-read metagenomes, 30 corresponding deeply sequenced short-read metatranscriptomes and 15 metaproteomes from 0.2-3 {micro}m size fractions that we sampled in 2020 during a biphasic phytoplankton bloom in the German Bight (Southern North Sea). We analyzed the assembled contigs as well as 70 bacterial metagenome-assembled genomes that recruited the highest transcript numbers with respect to the utilization of methyl sulfur compounds (dimethylsulfoniopropionate (DMSP), dimethyl sulfide (DMS), dimethyl sulfone (DMSO2)), C3-sulfonates (2,3-dihydroxypropane-1-sulfonate (DHPS), 3-sulfolactate, 3-sulfopyruvate) and 2-aminoethanesulfonic acid (taurine). We observed a pronounced resource partitioning among bacterial clades that utilize distinct organosulfur compounds, which may explain successions of these clades during the studied bloom. Alphaproteobacteria were the most active and degraded a variety of organosulfonates via various metabolic routes. However, we also found previously underreported roles of members of the Bacteroidota and Gammaproteobacteria as efficient degraders of DMSP, DMS, and DMSO2. One striking observation was a strong preference for DMSP cleavage in Bacteroidota as opposed to DMSP demethylation in Alphaproteobacteria and indications for a particular proficiency for taurine utilization in Ilumatobacter_A and Acidimicrobiia. ImportanceSulfur-containing low-molecular-weight algal metabolites play an important role in overall marine carbon and sulfur fluxes. This study highlights that such compounds may play a crucial role in governing the succession of distinct bacterioplankton clades in response to phytoplankton blooms in coastal shelf areas of the temperate zone, such as the German Bight of the North Sea. While Alphaproteobacteria are the most versatile and competitive degraders of dissolved organosulfur compounds during such blooms, this study repositions clades previously thought to play only a more limited role in dissolved organosulfur metabolism in situ, such as Gammaproteobacteria, Bacteroidota, and Acidimicrobiia, as crucial contributors to the remineralization of organosulfur compounds in the upper ocean. This study also highlights the high level of interconnectedness of bacterial carbon and sulfur cycling during phytoplankton blooms.