Diffusional Interactions among Marine Phytoplankton and Bacterioplankton: Modelling H2O2 as a Case Study

Abstract

Marine phytoplankton vary widely in size across taxa, and in cell suspension densities across habitats and growth states. Cell suspension density and total biovolume determine the bulk influence of a phytoplankton community upon its environment. Cell suspension density also determines the intercellular spacings separating phytoplankton cells from each other, or from co-occurring bacterioplankton. Intercellular spacing then determines the mean diffusion paths for exchanges of solutes among co-occurring cells. Marine phytoplankton and bacterioplankton both produce and scavenge reactive oxygen species (ROS), to maintain intracellular ROS homeostasis to support their cellular processes, while limiting damaging reactions. Among ROS, hydrogen peroxide (H₂O₂) has relatively low reactivity, long intracellular and extracellular lifetimes, and readily crosses cell membranes. Our objective was to quantify how cells can influence other cells via diffusional interactions, using H₂O₂ as a case study. To visualize and constrain potentials for cell-to-cell exchanges of H₂O₂, we simulated the decrease of [H₂O₂] outwards from representative phytoplankton taxa maintaining internal [H₂O₂] above representative seawater [H₂O₂]. [H₂O₂] gradients outwards from static cell surfaces were dominated by volumetric dilution, with only a negligible influence from decay. The simulated [H₂O₂] fell to background [H₂O₂] within ~3.1 µm from a Prochlorococcus cell surface, but extended outwards 90 µm from a diatom cell surface. More rapid decays of other, less stable ROS, would lower these threshold distances. Bacterioplankton lowered simulated local [H₂O₂] below background only out to 1.₂ µm from the surface of a static cell, even though bacterioplankton collectively act to influence seawater ROS. These small diffusional spheres around cells mean that direct cell-to-cell exchange of H₂O₂ is unlikely in oligotrophic habits with widely spaced, small cells; moderate in eutrophic habits with shorter cell-to-cell spacing; but extensive within phytoplankton colonies.

Keywords: bacterioplankton; diffusional interactions; hydrogen peroxide; phytoplankton.

Figure 1

Phytoplankton and heterotrophic bacteria spacing from eutrophic or oligotrophic environments, with cell size on the same scaling as the 1 mm XY spatial axes. A 1 mm Z spatial axis is coded with fainter points farther back.

Figure 2

Estimates of concentration gradients of [H₂O₂] vs. distance outwards from ‘heterotrophic’ Bacterioplankton cell maintaining an internal [H₂O₂] below seawater background [H₂O₂] (blue band); or outwards from ‘Phytoplankton’ cells of different radii, maintaining an internal [H₂O₂] equal to 1/10 the cytotoxic threshold for [H₂O₂]. Orange indicates cytotoxic concentration range for [H₂O₂] (1 × 10⁻⁵ to 1 × 10⁻⁴ M). Black points show modelled [H₂O₂] under the influence of dilution alone. Red points show modelled [H₂O₂] under superimposed influences of dilution and (negligible) decay of H₂O₂. Vertical green lines indicate the cell surface. Vertical dashed lines indicate threshold radii out from cells, where [H₂O₂] around the cell falls or rises to seawater background levels. Beyond that threshold, the cell has no specific, local influence upon seawater [H₂O₂].

Figure 3

Simulations of [H₂O₂] above seawater [H₂O₂] (pale blue) out from Phytoplankton cells (green spheres, spanning a size range), or [H₂O₂] below seawater [H₂O₂] out from Bacterioplankton cells (red spheres, single nominal cell size). Cell position along a third Z axis is simulated by the ‘alpha’ with lighter cells further back.

Figure 4

Simulation of [H₂O₂] above seawater [H₂O₂] within a Phaeocystis colony. Note the expansion of the axes scales to 0.1 mm. Cell position along a third Z axis is simulated by the ‘alpha’ with lighter cells further back.

Figure 5

Thresholds for direct phytoplankton cell-to-cell interaction through [H₂O₂] above seawater background. The X axis shows a range of cell m⁻³ (which in turn governs cell-to-cell distances), while the Y axis shows radii for cell-specific spheres of influence upon [H₂O₂] (a function of cell size, intracellular [H₂O₂] and seawater [H₂O₂]). The areas below the threshold lines show combinations where phytoplankton cell-to-cell distance exceeds the cell-specific [H₂O₂] distance, so direct cell-to-cell interactions mediated by [H₂O₂] are unlikely. The area above the threshold lines show combinations where phytoplankton cell-to-cell distance is less than the cell-specific [H₂O₂] distance, so direct cell-to-cell interactions mediated by [H₂O₂] are feasible. The four threshold lines refer to a range of ratios of phytoplankton intracellular to extracellular [H₂O₂]. Data points from different habitats show that direct phytoplankton cell-to-cell interactions are likely only within the Phaeocystis colony, whereas single phytoplankton cells are generally too small or too distant for direct interactions.

Figure 6

Thresholds for direct bacterioplankton cell-to-cell interaction through [H₂O₂] above seawater background. The X axis shows a range of cell m⁻³ (which in turn governs cell-to-cell distances), while the Y axis shows radii for cell-specific spheres of influence upon [H₂O₂] (a function of cell size, intracellular [H₂O₂] and seawater [H₂O₂]). The areas below the threshold lines show combinations where bacterioplankton cell-to-cell distance exceeds the cell-specific [H₂O₂] distance, so direct cell-to-cell interactions mediated by [H₂O₂] are unlikely. The area above the threshold lines show combinations where bacterioplankton cell-to-cell distance is less than the cell-specific [H₂O₂] distance, so direct cell-to-cell interactions mediated by [H₂O₂] are feasible. The four threshold lines refer to a range of ratios of bacterioplankton intracellular to extracellular [H₂O₂]. Data points from different habitats show that direct bacterioplankton cell-to-cell interactions are likely, over a range of reasonable ratios of intracellular to extracellular [H₂O₂], at >10¹⁰ cells m⁻³.