Chemotaxis toward phytoplankton drives organic matter partitioning among marine bacteria
Significance Microscale interactions between bacteria and phytoplankton underpin ocean biogeochemistry and frequently involve bacterial chemotaxis to phytoplankton dissolved organic matter (DOM) Yet, it remains unclear how the effects of this interaction propagate to ecosystem scales. We address this gap through a hybrid approach where high resolution observations of chemotaxis toward a diatom are directly used in a resource utilization model. We find that chemotactic bacteria consume most diatom DOM under resource rich or bacteria rich conditions, that DOM is partitioned among distinct populations based on diffusivity, and that consumption is skewed toward very few cells. Nonmotile oligotrophic bacteria dominate when productivity is low. Motile copiotrophs dominate during blooms. Ocean chemotaxis thus partitions resources spatially, by molecular size, and temporally through seasonal and episodic blooms. The microenvironment surrounding individual phytoplankton cells is often rich in dissolved organic matter (DOM) which can attract bacteria by chemotaxis. These "phycospheres" may be prominent sources of resource heterogeneity in the ocean, affecting the growth of bacterial populations and the fate of DOM. However, these effects remain poorly quantified due to a lack of quantitative ecological frameworks. Here, we used video microscopy to dissect with unprecedented resolution the chemotactic accumulation of marine bacteria around individual Chaetoceros affinis diatoms undergoing lysis. The observed spatiotemporal distribution of bacteria was used in a resource utilization model to map the conditions under which competition between different bacterial groups favors chemotaxis. The model predicts that chemotactic, copiotrophic populations outcompete nonmotile, oligotrophic populations during diatom blooms and bloom collapse conditions, resulting in an increase in the ratio of motile to nonmotile cells and in the succession of populations. Partitioning of DOM between the two populations is strongly dependent on the overall concentration of bacteria and the diffusivity of different DOM substances, and within each population, the growth benefit from phycospheres is experienced by only a small fraction of cells. By informing a DOM utilization model with highly resolved behavioral data, the hybrid approach used here represents a new path toward the elusive goal of predicting the consequences of microscale interactions in the ocean.
Proceedings of the National Academy of Sciences