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The ecology of bacterial attachment to phytoplankton
Abstract
Phytoplankton are responsible for approximately half of Earth’s net primary production and, together with heterotrophic bacteria—the main consumers of organic matter—play a pivotal role in biogeochemical cycles. Their key ecological importance has led to growing interest in the interactions between these two groups. Yet, our understanding of the microscale mechanisms driving these interactions remains limited. Recent work highlighted the contribution of bacterial motility and chemotaxis to promoting encounters and nutrient exchange between bacteria and phytoplankton. In contrast, the ecological role of bacterial attachment—an important adaptation enabling bacteria to establish the closest contact with their phytoplankton host and retain it over extended periods of time—remains less explored. Here we describe the current evidence and understanding of bacterial attachment to phytoplankton and highlight recent insights from single-cell studies. Motivated by the implications for large-scale ecosystem processes, we discuss promising research avenues to further unveil the ecological relevance of bacterial attachment to phytoplankton.
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A universal surface functionalization technique to chemically enhance live microbial cells
Abstract
Microbial surface functionalization is a powerful strategy for endowing microbes with novel, non-genetic functions. However, existing methods are often species-specific, limited in scope, and compromise cell viability. Here, we present a universal and modular platform for high-density, reproducible surface functionalization across diverse microbial species-including Gram-positive, Gram-negative, aerobic, and anaerobic bacteria-using multiple molecular classes such as fluorophores, enzymes, and nucleic acids. Our method preserves cell viability and achieves 50× higher functionalization efficiency than previous methods with a standardized protocol applicable to any azide-containing molecule. Applications of the method show reproducible and tunable phenotypic outcomes at the single-cell level: fluorophore labeling yielded adjustable fluorescence, β-lactamase conferred scalable antibiotic resistance, and DNA coatings modulated adhesion and aggregation. This platform provides quantitative, non-genetic control over microbial phenotypes and complements genetic engineering approaches. It enables new possibilities for microbial design in biotechnology, medicine, and environmental applications where genetic modification is impractical or undesirable.
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Stochastic resilience enables particle foraging in oligotrophic marine environments
Abstract
Heterotrophic bacteria play a central role in attenuating the sequestration of carbon to the deep ocean by degrading sinking marine particles. The role of certain copiotrophic adaptations such as surface attachment and motility in particle degradation has remained unclear outside of coastal regions, where the sparsity of particles would appear to preclude a foraging lifestyle based on particle hopping. We show here instead that many oligotrophic marine environments are much more amenable to copiotrophic particle foraging than would be inferred from average-based estimates, because the foraging process samples a broad distribution of particle–bacteria interactions, with large variation in encounter times, particle sizes, and associated survival outcomes, and due to the disproportionate benefit of a particle encounter. We develop a generalized branching process model for particle foraging to assess environment viability and population growth rates based on encounters with particles, for different oceanographic particle size spectra. The results indicate that even bathypelagic environments can support particle foraging bacteria without requiring long-term starvation tolerance or multiyear feast–famine cycles, because stochastic encounters generate sufficient short-interval, high-reward events to sustain population growth despite long mean encounter times. More generally, stochasticity can confer resilience to microbial populations in resource-scarce marine environments.
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Bacterial iron acquisition by Escherichia coli is facilitated by amino acid complexation in a rapid-renewal environment
Abstract
In natural environments, bacteria often encounter low concentrations of nutrient mixtures that are continuously replenished by physical processes such as fluid flow. Studying bacterial physiology under such conditions is experimentally challenging because it is difficult to maintain steady, low nutrient concentrations with rapid renewal. Most studies on nutrient limitation have used approaches such as the chemostat, which rely on long renewal times to sustain low concentrations. We developed a Millifluidic Continuous Culture Device (MCCD), inspired by microfluidics, that enables bacterial cultivation in nutrient mixtures at low micromolar concentrations with rapid renewal driven by fluid flow. Unlike microfluidic systems, the MCCD retains sufficient culture volume to support batch-scale ‘omic analyses. Using the MCCD, we cultured Escherichia coli in a mixture of amino acids and nucleobases at three concentration ranges spanning a fivefold difference in growth rates. Surprisingly, at the lowest concentration range, cells exhibited proteomic signatures of iron limitation despite equal total ferrous iron across conditions. Uptake experiments with labeled iron–histidine and iron–cysteine complexes confirmed that amino acids facilitated ferrous iron acquisition. Under continuous flow, siderophores were washed out, rendering this pathway ineffective and revealing a previously unrecognized mechanism of iron acquisition via soluble ferrous iron–amino acid complexes. These findings highlight the importance of studying bacterial physiology at low nutrient concentrations and also suggest a broader role for other organic substrates capable of complexing iron as potential iron sources in environments with rapid renewal.
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Phosphate deprivation restricts bacterial degradation of the marine polysaccharide fucoidan
Abstract
Brown algae and diatoms convert carbon dioxide into the polysaccharide fucoidan, which sequesters carbon in the ocean despite the prevalence of marine bacterial fucoidanase genes. Bacteria with fucoidanase genes also have high-affinity phosphate transporters, suggesting that phosphate could impact fucoidan degradation and subsequent carbon sequestration. Here, to test this hypothesis, we assembled a system consisting of a microalga that produces and a bacterium that degrades fucoidan. The fixation of carbon dioxide into fucoidan by the microalga Glossomastix sp. PLY432 occurred independent of the phosphate concentration. In contrast, the fucoidan-degrading Verrucomicrobiaceae bacterium 227 was inhibited by a lack of phosphate. Degradation of the structurally simpler polysaccharide laminarin was less affected by the phosphate concentration. Phosphate deprivation enabled the fixation of carbon dioxide in fucoidan and disabled its degradation. These conclusions suggest that phosphate deprivation could be a potential strategy to promote the fixation and sequestration of carbon dioxide as fucoidan.
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Phytoplankton community composition in the oligotrophic Argo Basin of the eastern Indian Ocean
Abstract
Phytoplankton, the foundational organisms in ocean food webs, have been little studied in the Indonesian Throughflow region of the eastern Indian Ocean, the spawning area of Southern Bluefin Tuna. Here, we assess phytoplankton abundance, biomass, size structure, pigment composition, taxonomic diversity and percent functional mixotrophs of that region based on complementary approaches of flow cytometry, microscopy, taxon-specific pigments and rRNA gene sequencing. During summer (January–February) 2022, the region was characterized by warm (up to 30.5 °C), stratified, oligotrophic (nitrogen-limited) waters, with integrated euphotic zone (EZ) chlorophyll a (CHLa) of 13 mg m−2. EZ mean CHLa was low in the upper layer (85 ng L−1) and 3.8 times higher (320 ng L−1) at the pronounced deep CHLa maximum. EZ-integrated phytoplankton carbon averaged 1229 mg C m−2. Prochlorococcus dominated throughout the EZ, but eukaryotic carbon biomass was ∼4-times greater in the lower than upper EZ, along with a distinct community. In the upper EZ, haptophytes, dinoflagellates and prasinophycean taxa without prasinoxanthin contributed most to monovinyl chlorophyll a (MV-CHLa). In the more diverse lower EZ, haptophytes, dinoflagellates, prasinophycean taxa with prasinoxanthin, pelagophytes, and cryptophytes were the main contributors to MV-CHLa. Diatoms were a minor part of the community. A higher percentage of the upper EZ community showed mixotrophy (35–84%) relative to the lower EZ (30–51%). Nitrogen-fixing organisms (as symbionts of diatoms and free-living cyanobacteria taxa) were ubiquitous, but low in abundance. Overall, community characteristics were similar to those at the Hawaii Ocean Time-series site and the central Gulf of Mexico.
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Dynamic reworking of marine diatom endometabolomes in response to temperature and a model bacterium
Abstract
A large annual carbon flux occurs through the surface ocean’s labile dissolved organic carbon (DOC) pool, with influx dominated by phytoplankton-derived metabolites and outflux by heterotrophic bacterioplankton uptake. We addressed the dynamics of this carbon flow between microbial primary and secondary producers through analysis of the Thalassiosira pseudonana CCMP1335 endometabolome, a proxy for the labile DOC released upon phytoplankton lysis, as temperature and bacterial presence were altered. Diatom strains acclimated at one of three different temperatures (14°C, 20°C, or 28°C) were cultured either axenically or with the bacterium Ruegeria pomeroyi DSS-3, and their endometabolites analyzed by NMR. Median concentration variation between conditions was ~1.5-fold across all identified endometabolites. Those with roles as osmolytes varied most, exhibiting concentration differences up to 170-fold across conditions with the largest variations triggered by the presence/absence of the heterotrophic bacterium. Differential expression observed for diatom metabolite synthesis pathways suggested changes in synthesis rates as a mechanism for endome tabolome remodeling. Consistent with expectations of high turnover by heterotrophic bacteria, endometabolite mean lifetimes in a DOC pool were <2 h to 12 h.