Emergent ecology in a microscale model of the surface ocean

• Published in: mBio 2024-11, Vol.15 (11), p.e0237224
• Main Authors: Eigemann, Falk, Hoffmann, Jutta, Schampera, Charlotte, Liu, Shuting, Bolaños, Luis M, Heemeyer, Mats, Carlson, Craig A, Giovannoni, Stephen, Hellweger, Ferdi L
• Format: Article
• Language: English
• Subjects: agent-based model; attachment; Bacteria - genetics; Bacteria - metabolism; Bacterial Physiological Phenomena; biogeochemical model; Carbon - metabolism; Chemotaxis; Cyanobacteria - growth & development; Cyanobacteria - metabolism; Cyanobacteria - physiology; Ecology; Ecosystem; fitness; Microbial Ecology; Models, Biological; Oceans and Seas; Phytoplankton - metabolism; Phytoplankton - physiology; Research Article; Seawater - chemistry; Seawater - microbiology
• ISSN: 2150-7511; 2150-7511
• DOI: 10.1128/mbio.02372-24

Microbial processes operate at the microscale, which is not resolved by existing ecosystem models. Here, we present a novel model that simulates a 1 mL three-dimensional cube using a hybrid Lagrangian-Eulerian approach, at ecologically relevant timescales. The model simulates individual microbes, including three phytoplankton size classes with healthy, senescent, and dead lifecycle stages; copiotrophic and oligotrophic heterotrophic bacteria; and dissolved organic matter at 50 µm resolution. Diffusion, shear, sedimentation, chemotaxis, and attachment processes are explicitly resolved. The emerging quantitative representation of the ecosystem shows that (1) copiotrophs grow mostly attached to eukaryotic phytoplankters and get almost all of their carbon from them vs. oligotrophs that grow on exudates and lysates of cyanobacteria; (2) contrasting diel patterns in substrate appearance in the phycosphere vs. ambient water and growth of particle-associated copiotrophs vs. free-living oligotrophs; (3) attached bacteria reduce carbon flux from the phycosphere, lowering chemotactic efficiency toward eukaryotes below that toward cyanobacteria; (4) shear reduces chemotactic efficiency and fitness of the copiotroph; and (5) the main benefit of chemotaxis is to locate attachment partners. These patterns are consistent with available observations. Our study provides insights into the microscale ecology of marine bacteria, and the open-source code is a tool for further research in this area.IMPORTANCEA large amount of global CO fixation is performed by marine phytoplankton, and a substantial fraction of that is released as dissolved organic carbon and further processed by heterotrophic bacteria. The interaction between phytoplankton and bacteria, i.e., the carbon flux between them, is therefore an important process in the global carbon and climate system. Some bacteria have developed specialized behavioral traits, like swimming and attachment, to increase their carbon acquisition. These interactions occur at the micrometer scale, for example, the immediate vicinity of phytoplankters (the phycosphere), but existing biogeochemical models typically only simulate down to the 1 meter vertical or ~100 kilometer horizontal scale. We present a new microscale model and use it to predict fluxes and other features in the surface ocean. The model makes important predictions about the fluxes between various types of phytoplankton and bacteria and the role of behavioral traits, and it