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.

Knowledge of Earth's microbiomes' capacity to degrade aromatic compounds is limited by the lack of accurate tools for identifying degrading genes and their associated taxa. Additionally, these estimates are hardly compared to in situ background concentrations of polycyclic aromatic hydrocarbons (PAHs), particularly in oceanic waters. This knowledge is important for assessing the persistence of the widespread and abundant PAHs in the environment and their interactions with microbes. Here, we present a new tool to identify aromatic ringhydroxylating dioxygenase alpha-subunit (arhdA) gene sequences by combining profile-based search with phylogenetic placement in a reference phylogeny. We identified arhdA-harboring taxa in both the Genome Taxonomy Database and the Malaspina Vertical Profiles Gene Database, a gene catalog derived from metagenomes collected during the Malaspina expedition. We found that multiple ubiquitous taxa in tropical and temperate oceans harbor arhdA. The comparison of arhdA gene abundances in seawater metagenomes with the field PAH concentrations showed that higher abundances of arhdA gene copies per cell were negatively correlated with 2-4 ring PAHs, consistent with the known degradation of lighter PAHs. Gene abundances were significantly higher in the particle-associated fraction than in the free-living fraction, suggesting particulate matter as a relevant reservoir of PAH degraders. Finally, we show that PAHs, together with other environmental variables, modulate the structure of oceanic microbial communities.

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.

A few genera of diatoms that form stable partnerships with N₂-fixing filamentous cyanobacteria Richelia spp. are widespread in the open ocean. A unique feature of the diatom-Richelia symbioses is the symbiont cellular location spans a continuum of integration (epibiont, periplasmic, and endobiont) that is reflected in the symbiont genome size and content. In this study, we analyzed genomes derived from cultures and environmental metagenome-assembled genomes of Richelia symbionts, focusing on characters indicative of genome evolution. Our results show an enrichment of short-length transposases and pseudogenes in the periplasmic symbiont genomes, suggesting an active and transitionary period in genome evolution. By contrast, genomes of endobionts exhibited fewer transposases and pseudogenes, reflecting advanced stages of genome reduction. Pangenome analyses identified that endobionts streamline their genomes and retain most genes in the core genome, whereas periplasmic symbionts and epibionts maintain larger flexible genomes, indicating higher genomic plasticity compared with the genomes of endobionts. Functional gene comparisons with other N₂-fixing cyanobacteria revealed that Richelia endobionts have similar patterns of metabolic loss but are distinguished by the absence of specific pathways (e.g., cytochrome bd ubiquinol oxidase and lipid A) that increase both dependency and direct interactions with their respective hosts. In conclusion, our findings underscore the dynamic nature of genome reduction in N₂-fixing cyanobacterial symbionts and demonstrate the diatom-Richelia symbioses as a valuable and rare model to study genome evolution in the transitional stages from a free-living facultative symbiont to a host-dependent endobiont.

All nitrogen-fixing root nodule symbioses of angiosperms-legume and actinorhizal symbioses-possess a common ancestor. Molecular processes for the induction of root nodules are modulated by phytohormones, as is the case of the first nodulation-related transcription factor NODULE INCEPTION (NIN), whose expression can be induced by exogenous cytokinin in legumes. The process of actinorhizal nodule organogenesis is less well understood. To study the changes exerted by phytohormones on the expression of the orthologs of CYCLOPS, NIN, and NF-YA1 in the actinorhizal host Datisca glomerata, an axenic hydroponic system was established and used to examine the transcriptional responses (RT-qPCR) in roots treated with the synthetic cytokinin 6-Benzylaminopurine (BAP), the natural auxin Phenylacetic acid (PAA), and the synthetic auxin 1-Naphthaleneacetic acid (NAA). The model legume Lotus japonicus was used as positive control. Molecular readouts for auxins and cytokinin were established: DgSAUR1 for PAA, DgGH3.1. for NAA, and DgARR9 for BAP. L. japonicus NIN was induced by BAP, PAA, and NAA in a dosage- and time-dependent manner. While expression of D. glomerata NIN2 could not be induced in roots, D. glomerata NIN1 was induced by PAA; this induction was abolished in the presence of exogenous BAP. Furthermore, the induction of DgNIN1 expression by PAA required ethylene and gibberellic acid. This study suggests that while cytokinin signaling is central for cortex-induced nodules of L. japonicus, it acts antagonistically to the induction of nodule primordia of D. glomerata by PAA in the root pericycle.

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.

Uptake hydrogenase (Hup) recycles H2 formed by nitrogenase during nitrogen fixation, thereby preserving energy. Among root nodule bacteria, most rhizobial strains examined are Hup-, while only one Hup- Frankia inoculum had been identified. Previous analyses had led to the identification of two different [NiFe] hydrogenase syntons. We analysed the distribution of different types of [NiFe] hydrogenase in the genomes of different Frankia species. Our results show that Frankia strains can contain four different [NiFe] hydrogenase syntons representing groups 1f, 1h, 2a, and 3b according to S & oslash;ndergaard, Pedersen, and Greening (HydDB: a web tool for hydrogenase classification and analysis. Sci Rep 2016;6:34212. https://doi.org/10.1038/srep34212.); no more than three types were found in any individual genome. The phylogeny of the structural proteins of groups 1f, 1h, and 2a follows Frankia phylogeny; the phylogeny of the accessory proteins does not consistently. An analysis of different [NiFe] hydrogenase types in Actinomycetia shows that under the most parsimonious assumption, all four types were present in the ancestral Frankia strain. Based on Hup activities analysed and the losses of syntons in different lineages of genome reduction, we can conclude that groups 1f and 2a are involved in recycling H2 formed by nitrogenase while group 1 h and group 3b are not. Different types of [NiFe] hydrogenases in the genus Frankia and their roles in nitrogen fixation deduced from losses in lineages of genome erosion.