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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.