BACKGROUND: Marine microalgae (phytoplankton) mediate almost half of the worldwide photosynthetic carbon dioxide fixation and therefore play a pivotal role in global carbon cycling, most prominently during massive phytoplankton blooms. Phytoplankton biomass consists of considerable proportions of polysaccharides, substantial parts of which are rapidly remineralized by heterotrophic bacteria. We analyzed the diversity, activity, and functional potential of such polysaccharide-degrading bacteria in different size fractions during a diverse spring phytoplankton bloom at Helgoland Roads (southern North Sea) at high temporal resolution using microscopic, physicochemical, biodiversity, metagenome, and metaproteome analyses.
RESULTS: Prominent active 0.2-3 µm free-living clades comprised Aurantivirga, \"Formosa\", Cd. Prosiliicoccus, NS4, NS5, Amylibacter, Planktomarina, SAR11 Ia, SAR92, and SAR86, whereas BD1-7, Stappiaceae, Nitrincolaceae, Methylophagaceae, Sulfitobacter, NS9, Polaribacter, Lentimonas, CL500-3, Algibacter, and Glaciecola dominated 3-10 µm and > 10 µm particles. Particle-attached bacteria were more diverse and exhibited more dynamic adaptive shifts over time in terms of taxonomic composition and repertoires of encoded polysaccharide-targeting enzymes. In total, 305 species-level metagenome-assembled genomes were obtained, including 152 particle-attached bacteria, 100 of which were novel for the sampling site with 76 representing new species. Compared to free-living bacteria, they featured on average larger metagenome-assembled genomes with higher proportions of polysaccharide utilization loci. The latter were predicted to target a broader spectrum of polysaccharide substrates, ranging from readily soluble, simple structured storage polysaccharides (e.g., laminarin, α-glucans) to less soluble, complex structural, or secreted polysaccharides (e.g., xylans, cellulose, pectins). In particular, the potential to target poorly soluble or complex polysaccharides was more widespread among abundant and active particle-attached bacteria.
CONCLUSIONS: Particle-attached bacteria represented only 1% of all bloom-associated bacteria, yet our data suggest that many abundant active clades played a pivotal gatekeeping role in the solubilization and subsequent degradation of numerous important classes of algal glycans. The high diversity of polysaccharide niches among the most active particle-attached clades therefore is a determining factor for the proportion of algal polysaccharides that can be rapidly remineralized during generally short-lived phytoplankton bloom events. Video Abstract.

Weathered oil, that is, tar, forms hotspots of hydrocarbon degradation by complex biota in marine environment. Here, we used marker gene sequencing and metagenomics to characterize the communities of bacteria, archaea and eukaryotes that colonized tar patties and control samples (wood, plastic), collected in the littoral following an offshore spill in the warm, oligotrophic southeastern Mediterranean Sea (SEMS). We show potential aerobic and anaerobic hydrocarbon catabolism niches on tar interior and exterior, linking carbon, sulfur and nitrogen cycles. Alongside aromatics and larger alkanes, short-chain alkanes appear to fuel dominant populations, both the aerobic clade UBA5335 (Macondimonas), anaerobic Syntropharchaeales, and facultative Mycobacteriales. Most key organisms, including the hydrocarbon degraders and cyanobacteria, have the potential to fix dinitrogen, potentially alleviating the nitrogen limitation of hydrocarbon degradation in the SEMS. We highlight the complexity of these tar-associated communities, where bacteria, archaea and eukaryotes co-exist, likely exchanging metabolites and competing for resources and space.

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Seawalls are important in protecting coastlines from currents, erosion, sea-level rise, and flooding. They are, however, associated with reduced biodiversity, due to their steep orientation, lack of microhabitats, and the materials used in their construction. Hence, there is considerable interest in modifying seawalls to enhance the settlement and diversity of marine organisms, as microbial biofilms play a critical role facilitating algal and invertebrate colonization. We assessed how different stone materials, ranging from aluminosilicates to limestone and concrete, affect biofilm formation. Metagenomic assessment of marine microbial communities indicated no significant impact of material on microbial diversity, irrespective of the diverse surface chemistry and topography. Based on KEGG pathway analysis, surface properties appeared to influence the community composition and function during the initial stages of biofilm development, but this effect disappeared by Day 31. We conclude that marine biofilms converged over time to a generic marine biofilm, rather than the underlying stone substrata type playing a significant role in driving community composition.

Bacteria and archaea are central to the production, consumption, and remineralization of dissolved and particulate organic matter and contribute critically to carbon delivery, nutrient availability, and energy transformations in the deep ocean. To explore environmentally relevant genomic traits of sinking-particle-associated versus free-living microbes, we compared habitat-specific metagenome-assembled genomes recovered throughout the water column in the North Pacific Subtropical Gyre. The genomic traits of sinking-particle-associated versus free-living prokaryotes were compositionally, functionally, and phylogenetically distinct. Substrate-specific transporters and extracellular peptidases and carbohydrate-active enzymes were more enriched and diverse in particle-associated microbes at all depths than in free-living counterparts. These data indicate specific roles for particle-attached microbes in particle substrate hydrolysis, uptake, and remineralization. Shallow-water particle-associated microbes had elevated genomic GC content and proteome nitrogen content and reduced proteome carbon content in comparison to abyssal particle-associated microbes. An inverse trend was observed for their sympatric free-living counterparts. These different properties of attached microbes are postulated to arise in part due to elevated organic and inorganic nitrogen availability inside sinking particles. Particle-attached microbes also were enriched in genes for environmental sensing via two-component regulatory systems, and cell-cell interactions via extracellular secretion systems, reflecting their surface-adapted lifestyles. Finally, particle-attached bacteria had greater predicted maximal growth efficiencies than free-living bacterioplankton at all depths. All of these particle-associated specific genomic and proteomic features appear to be driven by microhabitat-specific elevated nutrient and energy availability as well as surface-associated competitive and synergistic ecological interactions. Although some of these characteristics have been previously postulated or observed individually, we report them together here in aggregate via direct comparisons of cooccurring free-living and sinking-particle-attached microbial genomes from the open ocean. IMPORTANCE Particle-attached microbes play large roles in the ocean carbon cycle and help to sequester atmospheric CO2 and to deliver nutrients and energy on sinking particles to the deep sea. Here, we report on the genomic traits of particle-attached versus free-living microbes throughout the ocean water column to better differentiate their specific metabolic and ecological roles in the sea. In general, the genomic properties and contents of particle-attached microbes reflected the physical and chemical compositions of their environment as well as their microhabitat-specific adaptive traits. In comparison to cooccurring free-living microbes, particle-attached microbes had larger genomes, greater capacity for extracellular polymer degradation, greater environmental sensing and response capacity, greater potential for motility and attachment, and higher growth efficiencies. Our results present an integrated new perspective on sinking-particle-attached microbial adaptive traits that contribute to their critical ecological and biogeochemical roles and activities in the sea.

Facultative multicellular behaviors expand the metabolic capacity and physiological resilience of bacteria. Despite their ubiquity in nature, we lack an understanding of how these behaviors emerge from cellular-scale phenomena. Here, we show how the coupling between growth and resource gradient formation leads to the emergence of multicellular lifecycles in a marine bacterium. Under otherwise carbon-limited growth conditions, Vibrio splendidus 12B01 forms clonal multicellular groups to collectively harvest carbon from soluble polymers of the brown-algal polysaccharide alginate. As they grow, groups phenotypically differentiate into two spatially distinct sub-populations: a static \"shell\" surrounding a motile, carbon-storing \"core.\" Differentiation of these two sub-populations coincides with the formation of a gradient in nitrogen-source availability within clusters. Additionally, we find that populations of cells containing a high proportion of carbon-storing individuals propagate and form new clusters more readily on alginate than do populations with few carbon-storing cells. Together, these results suggest that local metabolic activity and differential partitioning of resources leads to the emergence of reproductive cycles in a facultatively multicellular bacterium.

As the market size of the cosmetics industry increases, the safety and effectiveness of new products face higher requirements. The marine environment selects for species of micro-organisms with metabolic pathways and adaptation mechanisms different from those of terrestrial organisms, resulting in their natural products exhibiting unique structures, high diversity, and significant biological activities. Natural products are usually safe and non-polluting. Therefore, considerable effort has been devoted to searching for cosmetic ingredients that are effective, safe, and natural for marine micro-organisms. However, marine micro-organisms can be difficult, or impossible, to culture because of their special environmental requirements. Metagenomics technology can help to solve this problem. Moreover, using marine species to produce more green and environmentally friendly products through biotransformation has become a new choice for cosmetic manufacturers. In this study, the natural products of marine micro-organisms are reviewed and evaluated with respect to various cosmetic applications.

The simultaneous limitation of productivity by two or more nutrients, commonly referred to as nutrient co-limitation, affects microbial communities throughout the marine environment and is of profound importance because of its impacts on various biogeochemical cycles. Multiple types of co-limitation have been described, enabling distinctions based on the hypothesized mechanisms of co-limitation at a biochemical level. These definitions usually pertain to individuals and do not explicitly, or even implicitly, consider complex ecological dynamics found within a microbial community. However, limiting and co-limiting nutrients can be produced in situ by a subset of microbial community members, suggesting that interactions within communities can underpin co-limitation. To address this, we propose a new category of nutrient co-limitation, community interaction co-limitation (CIC). During CIC, one part of the community is limited by one nutrient, which results in the insufficient production or transformation of a biologically produced nutrient that is required by another part of the community, often primary producers. Using cobalamin (vitamin B12) and nitrogen fixation as our models, we outline three different ways CIC can arise based on current literature and discuss CIC\'s role in biogeochemical cycles. Accounting for the inherent and complex roles microbial community interactions play in generating this type of co-limitation requires an expanded toolset - beyond the traditional approaches used to identify and study other types of co-limitation. We propose incorporating processes and theories well-known in microbial ecology and evolution to provide meaningful insight into the controls of community-based feedback loops and mechanisms that give rise to CIC in the environment. Finally, we highlight the data gaps that limit our understanding of CIC mechanisms and suggest methods to overcome these and further identify causes and consequences of CIC. By providing this framework for understanding and identifying CIC, we enable systematic examination of the impacts this co-limitation can have on current and future marine biogeochemical processes.

With 4 to 12 million tons of plastic entering the marine environment each year, plastic pollution has become one of the most ubiquitous sources of pollution of the Anthropocene threatening the marine environment. Beyond the conspicuous physical damages, plastics may release a cocktail of harmful chemicals, i.e. monomers, additives and persistent organic pollutants. Although known to be highly toxic, plastic leachates seemingly appear, however, as the \"somewhat sickly child\" of the plastic pollution literature. We reviewed the only 26 studies investigating the impact of plastic leachates on marine microbes and invertebrates, and concluded that the observed effects essentially depend on the species, polymer type, plastic composition, accumulated contaminants and weathering processes. We identified several gaps that we believe may hamper progress in this emerging area of research and discussed how they could be bridged to further our understanding of the effects of the compounds released by plastic items on marine organisms. We first stress the lack of a consensus on the use of the term \'leachate\', and subsequently introduce the concepts of primary and secondary leachates, based on the intrinisic or extrinsic origin of the products released in bulk seawater. We discuss how methodological inconsistencies and the discrepancy between the polymers used in experiments and their abundance in the environment respectively limit comparison between studies and a comprehensive assessment of the effects leachate may actually have in the ocean. We also discuss how the imbalanced in the variety of both organisms and polymers considered, the mostly unrealistic concentrations used in laboratory experiments, and the lack of investigation on key ecosystem engineers may considerably narrow the spectrum of our understanding of the plastic leachates\' effects. We finally discuss how increasing multi-disciplinarity through collaborations between different research fields may benefit to an area of research which is still in its early infancy.

Ocean microbial communities are important contributors to the global biogeochemical reactions that sustain life on Earth. The factors controlling these communities are being increasingly explored using metatranscriptomic and metaproteomic environmental biomarkers. Using published proteomes and transcriptomes from the abundant colony-forming cyanobacterium Trichodesmium (strain IMS101) grown under varying Fe and/or P limitation in low and high CO2, we observed robust correlations of stress-induced proteins and RNAs (i.e., involved in transport and homeostasis) that yield useful information on the nutrient status under low and/or high CO2. Conversely, transcriptional and translational correlations of many other central metabolism pathways exhibit broad discordance. A cellular RNA and protein production/degradation model demonstrates how biomolecules with small initial inventories, such as environmentally responsive proteins, achieve large increases in fold-change units as opposed to those with a higher basal expression and inventory such as metabolic systems. Microbial cells, due to their immersion in the environment, tend to show large adaptive responses in both RNA and protein that result in transcript-protein correlations. These observations and model results demonstrate multi-omic coherence for environmental biomarkers and provide the underlying mechanism for those observations, supporting the promise for global application in detecting responses to environmental stimuli in a changing ocean.