Background: While oligotrophic bacteria are known to dominate most marine microbial habitats, under certain conditions, such as during phytoplankton blooms, copiotrophs can dramatically increase in abundance and reach towering proportions of the bacterial communities. We are uncertain whether the bacteria exhibiting this capacity, which we denote as "bloomers," have specific functional characteristics or if, instead, they are randomly selected from the broader pool of copiotrophs. To explore the genomic determinants of this ecological trait, we conducted a comparative genomic analysis of bacterial genomes from microcosm experiments where grazer and viral presence was reduced and nutrient availability was increased, conditions that triggered bacterial blooms.

Results: We tested which functional genes were overrepresented in the bacteria that responded to the treatments, examining a total of 305 genomes from isolates and metagenome-assembled genomes (MAGs) that were categorized as copiotrophs or oligotrophs according to their codon usage bias (CUB). The responsive bacteria were enriched in genes related to transcriptional regulation in response to stimuli (mostly via two-component systems), transport, secretion, cell protection, catabolism of sugars and amino acids, and membrane/cell wall biosynthesis. These genes confer on them capabilities for adhesion, biofilm formation, resistance to stress, quorum sensing, chemotaxis, nutrient uptake, and fast replication. They were overrepresented mainly in copiotrophic genomes from the families Alteromonadaceae, Vibrionaceae, Rhodobacteraceae, Sphingomonadaceae, and Flavobacteriaceae. Additionally, we found that these responsive bacteria, when abundant, could affect biogeochemical cycling, particularly the phosphorus cycle.

Conclusions: In this study, we provide insights into the functional characteristics that enable certain bacteria to rapidly respond to changes in the environment and bloom. We also hint at the ecological meaning and implications of these phenomena that could affect biogeochemical cycles in the oceans.

Bacteria in aquatic environments are a principal food source for predatory protists. Whereas interactions between bacteria and protists are recognized to determine the pathogenesis and epidemiology of several human pathogens, few studies have systematically characterized the interactions between specific aquatic bacteria and protists beyond the prey-predator relation. We, therefore, surveyed individual co-cultures between 18 different genome-sequenced marine bacteria with known virulence gene repertoires and three model protist species widely used for assessing bacteria-protist interactions. Strikingly, 10, 5, and 3 bacterial isolates were capable of lysing the protists Acanthamoeba polyphaga, Tetrahymena pyriformis, and Euglena gracilis, respectively. A majority of the bacteria were able to grow and/or maintain viable populations in the presence of viable protists. Some bacteria survived longer with viable protists but not heat-killed protists and were observed in protist vacuoles. In this respect, marine bacteria are similar to several protist-dependent human pathogens, including Legionella. Analyses of growth patterns in low-nutrient media showed that co-cultivation with A. polyphaga allowed one bacterial strain to overcome nutritional stress and obtain active growth. Five isolates depended on viable amoebae to grow, notwithstanding nutrient media status. The remarkable capability of these marine bacteria to survive encounters with, and even actively kill, model predatory protists under laboratory conditions suggests that diverse bacterial defense strategies and virulence mechanisms to access nutrients may be important in shaping microbial interactions. If verified with native marine and freshwater populations, the diversity of interactions uncovered here has implications for understanding ecological and evolutionary consequences of population dynamics in bacteria and protists.IMPORTANCEThe microbiome constitutes the base of food webs in aquatic environments. Its composition partly reflects biotic interactions, where bacteria primarily are considered prey of predatory protists. However, studies that focus on one or a few species have shown that some bacteria have abilities to escape grazing and may even be capable of lysing their protist predators. In this study, we substantially extend these findings by systematically investigating interactions among multiple taxa of both bacteria and protists. Our results show that marine bacteria display a wider and more complex range of interactions with their predators than generally recognized-from growth dependency to protist lysis. Given that such interactions play key roles in the pathogenesis and epidemiology of several human pathogens, our findings imply that bacterial virulence traits can contribute to defining the structure and ecology of aquatic microbiomes.

Background: Vitamin B1 (thiamin) is essential to life; yet little is known of the regulation of its availability in marine environments or how it varies seasonally. Since microbes are the key synthesizers of the vitamin in marine environments, we here used metatranscriptomics to examine the seasonal dynamics of B1 acquisition strategies (including both uptake and synthesis pathways) in Baltic Sea bacterioplankton.

Results: Elevated B1-related gene expression was observed in summer, coinciding with increased temperatures and bacterial activity and decreased nutrient availability. Different bacterial taxa exhibited distinct B1 acquisition strategies. We identified filamentous Cyanobacteria of the order Nostocales as critical to sustaining B1 production during summer, potentially compensating for limited synthesis in heterotrophic bacteria, especially for 4-amino-5-hydroxymethylpyrimidine (HMP) synthesis. Also, Pelagibacterales accounted for major portions of the community transcription, primarily taking up and salvaging the B1 precursor HMP during summer. This study highlights the partitioning of B1 synthesis, salvage, and uptake among microbial taxa, underscoring that transcriptional activity was more dynamic over time than changes in the genomic potential.

Conclusions: We emphasize the influence of environmental conditions on microbial community dynamics and B1 cycling in general, and the potential implications of global change-induced increases in filamentous Cyanobacteria blooms on vitamin food web transfer in particular.

In recent years, new contributors to the marine silica cycle have emerged, including pico-sized phytoplankton (<2-3 μm in size) such as Synechococcus and picoeukaryotes. Their contribution and relevance to silica cycling are still under investigation. Field studies reporting the biogenic silica (bSi) standing stock in the pico-sized fraction are limited to silica-poor oligotrophic environments, and the mechanism of bSi accumulation in picoplankton remains unknown. We investigated the variability of bSi standing stocks in two size fractions (picoplankton, 0.22-3 mu m and microplankton, >3 μm) in the dissolved silica-replete Baltic Sea via biweekly time series samplings spanning 2 years. Time series data showed that the large changes in bSi standing stock in the Baltic Proper were primarily related to microplankton biomass and community composition. Meanwhile, picoplankton were, at times, surprisingly high contributors to total bSi year-round (up to 21.6%). Simultaneously, we performed microcosm incubation experiments with natural phytoplankton communities in each season to examine how nutrient additions affected bSi concentrations. In these experiments, increases in microplankton bSi were directly correlated to increases in diatom biomass, highlighting their influential role in the Baltic Sea silica cycle. Meanwhile, phosphorus additions triggered an increase in picoplankton bSi accumulation in all experiments. This uncovers a potential control of bSi accumulation in picoplankton, which can help identify the cellular mechanisms behind this process and uncover their role in silica cycling. The results link phytoplankton community composition and silica cycling, which is important for understanding the consequences of organism shifts due to climate change.

Through biosilicification, organisms incorporate dissolved silica (dSi) and deposit it as biogenic silica (bSi), driving the silicon (Si) cycle in aquatic systems. While Si accumulation in marine picocyanobacteria has been recently observed, its mechanisms and ecological implications remain unclear. This study investigates biosilicification in marine and brackish picocyanobacteria of the Synechococcus clade and two model freshwater coccoid cyanobacteria. Brackish strains showed significantly higher Si quotas when supplemented with external dSi (100 mu M) compared to controls (up to 60.0 +/- 7.3 amol Si.cell-1 versus 9.2 to 16.3 +/- 2.9 amol Si.cell-1). Conversely, freshwater strains displayed no significant differences in Si quotas between dSi-enriched treatments and controls, emphasizing that not all phytoplanktons without an obligate Si requirement accumulate this element. The Si-accumulating marine and brackish picocyanobacteria clustered within the Synechococcus clade, whereas their freshwater counterparts formed a distinct sister group, suggesting a link between phylogeny and silicification. Rapid culture growth caused increased pH and led to dSi precipitation, influencing apparent dSi uptake; this was mitigated by pH control through bubbling. This phenomenon has significant implications for natural systems affected by phytoplankton blooms. In such environments, pH-induced silicon precipitation may reduce dSi availability impacting Si-dependent populations like diatoms. Our findings suggest brackish picocyanobacteria could significantly influence the Si cycle through at least two mechanisms: cellular Si accumulation and biologically induced changes in dSi concentrations.IMPORTANCEThis work provides the first evidence of biogenic silica accumulation in brackish picocyanobacteria and uncovers a link between phylogeny and biosilicification patterns. Our findings demonstrate that picocyanobacterial growth induces pH-dependent silica precipitation, which could lead to overestimations of cellular Si quotas by up to 85%. This process may drive substantial silica precipitation in highly productive freshwater and coastal marine systems, with potential effects on silica cycling and the population dynamics of Si-dependent phytoplankton. The extent of biosilicification in modern picocyanobacteria offers insights into the rock record, shedding light on the evolutionary and ecological dynamics that influence sedimentary processes and the preservation of biosilicification signatures in geological formations. Overall, this research adds to the significant impact that microorganisms lacking an obligate silica requirement may have on silica dynamics.

Coastal upwelling areas are extraordinarily productive environments where prokaryotic communities, the principal remineralizers of dissolved organic matter (DOM), rapidly respond to phytoplankton bloom and decay dynamics. Nevertheless, the extent of variability of key microbial functions in such dynamic waters remains largely unconstrained. Our metatranscriptomics analyses of 162 marker genes encoding ecologically relevant prokaryotic functions showed distinct spatial-temporal patterns in the NW Iberian Peninsula upwelling area. Short-term (daily) changes in specific bacterial functions associated with changes in biotic and abiotic factors were superimposed on seasonal variability. Taxonomic and functional specialization of prokaryotic communities, based mostly on different resource acquisition strategies, was observed. Our results uncovered the potential influence of prokaryotic functioning on phytoplankton bloom composition and development (e.g., Cellvibrionales and Flavobacteriales increased relative gene expression related to vitamin B12 and siderophore metabolisms during Chaetoceros and Dinophyceae summer blooms). Notably, bacterial adjustments to C- or N-limitation and DMSP availability during summer phytoplankton blooms and different spatial-temporal patterns of variability in the expression of genes with different phosphate affinity indicated a complex role of resource availability in structuring bacterial communities in this upwelling system. Also, a crucial role of Cellvibrionales in the degradation of DOM (carbohydrate metabolism, TCA cycle, proteorhodopsin, ammonium, and phosphate uptake genes) during the summer phytoplankton bloom was found. Overall, this dataset revealed an intertwined mosaic of microbial interactions and nutrient utilization patterns along a spatial-temporal gradient that needs to be considered if we aim to understand the biogeochemical processes in some of the most productive ecosystems in the world ' s oceans.

Skin microbiomes provide vital functions, yet knowledge about the drivers and processes structuring their species assemblages is limited-especially for non-model organisms. In this study, fish skin microbiome was assessed by high throughput sequencing of amplicon sequence variants from metabarcoding of V3-V4 regions in the 16S rRNA gene on fish hosts subjected to the following experimental manipulations: (i) translocation between fresh and brackish water habitats to investigate the role of environment; (ii) treatment with an antibacterial disinfectant to reboot the microbiome and investigate community assembly and priority effects; and (iii) maintained alone or in pairs to study the role of social environment and inter-host dispersal of microbes. The results revealed that fish skin microbiomes harbour a highly dynamic microbial composition that was distinct from bacterioplankton communities in the ambient water. Microbiome composition first diverged as an effect of translocation to either the brackish or freshwater habitat. When the freshwater individuals were translocated back to brackish water, their microbiome composition converged towards the fish microbiomes in the brackish habitat. In summary, external environmental conditions and individual-specific factors jointly determined the community composition dynamics, whereas inter-host dispersal had negligible effects. The dynamics of the microbiome composition was seemingly non-affected by reboot treatment, pointing towards high resilience to disturbance. The results emphasised the role of inter-individual variability for the unexplained variation found in many host-microbiome systems, although the mechanistic underpinnings remain to be identified.

In nature, the number of genome or chromosome copies within cells (ploidy) can vary between species and environmental conditions, potentially influencing how organisms adapt to changing environments. Although ploidy levels cannot be easily determined by standard genome sequencing, understanding ploidy is crucial for the quantitative interpretation of molecular data. Cyanobacteria are known to contain haploid, oligoploid, and polyploid species. The smallest cyanobacteria, picocyanobacteria (less than 2 μm in diameter), have a widespread distribution ranging from marine to freshwater environments, contributing significantly to global primary production. In this study, we determined the ploidy level of genetically and physiologically diverse brackish picocyanobacteria isolated from the Baltic Sea using a qPCR assay targeting the rbcL gene. The strains contained one to four genome copies per cell. The ploidy level was not linked with phylogeny based on the identity of the 16S rRNA gene. The variation of ploidy among the brackish strains was lower compared to what has been reported for freshwater strains and was more similar to what has been reported for marine strains. The potential ecological advantage of polyploidy among picocyanobacteria has yet to be described. Our study highlights the importance of considering ploidy to interpret the abundance and adaptation of brackish picocyanobacteria.

Prokaryotic maintenance respiration and associated metabolic activities constitute a considerable proportion of the total respiration of carbon to CO2 in the ocean's mixed layer. However, seasonal influences on prokaryotic maintenance activities in terms of morphological and metabolic adaptations at low (winter) and high productivity (summer) are still unclear. To address this, we examined the natural prokaryotic communities at the mesocosm scale to analyse the differences in their morphological features and gene expression at low and high maintenance respiration, experimentally manipulated with the specific growth rate. Here, we showed that morphological features including membrane blebbing, membrane vesicles, and cell-cell connections occurred under high productivity. Metabolic adaptations associated with maintenance activities were observed under low productivity. Several Kyoto Encyclopedia of Genes and Genomes categories related to signal transduction, energy metabolism, and translational machinery supported maintenance activities under simulated winter conditions. Differential abundances of genes related to transporters, osmoregulation, nitrogen metabolism, ribosome biogenesis, and cold stress were observed. Our results demonstrate how specific growth rate in different seasons can influence resource allocation at the levels of morphological features and metabolic adaptations. This motivates further study of morphological features and their ecological role during high productivity, while investigations of metabolic adaptations during low productivity can advance our knowledge about maintenance activities.

Unveiling the interactions among phytoplankton and bacteria at the level of species requires axenic isolates to experimentally demonstrate their mutual effects. In this study, we describe the interactions among the diatoms Pseudo-nitzschia granii and Chaetoceros tenuissimus and their associated bacterial species, isolated from surface water of a coastal upwelling system using coculture experiments. Microalgae growth was assessed in axenic monocultures or in coculture with each of their co-isolated bacteria in the presence or absence of B vitamins. Pseudo-nitzschia granii growth was limited by B-vitamin supply, except when cultured with the bacteria Jannaschia cystaugens, which seemed to provide adequate levels of B vitamins to the diatom. Chaetoceros tenuissimus growth was reduced in the absence of B vitamins. Moreover, the growth of C. tenuissimus was stimulated by Alteromonas sp. and Celeribacter baekdonensis during the exponential growth. These results show a diversity of specific interactions between the diatoms and co-isolated bacteria, ranging from allelopathy to commensalism. Understanding how interactions between phytoplankton and bacteria modulate the structure and function of marine microbial plankton communities will contribute to a greater knowledge of plankton ecology and improve our ability to predict nutrient fluxes in marine ecosystems or the formation of blooms in a context of global change.