Emergent ecology in a microscale model of the surface ocean

ABSTRACT 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 mic...

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Main Authors: Falk Eigemann, Jutta Hoffmann, Charlotte Schampera, Shuting Liu, Luis M. Bolaños, Mats Heemeyer, Craig A. Carlson, Stephen Giovannoni, Ferdi L. Hellweger
Format: Article
Language:English
Published: American Society for Microbiology 2024-11-01
Series:mBio
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Online Access:https://journals.asm.org/doi/10.1128/mbio.02372-24
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author Falk Eigemann
Jutta Hoffmann
Charlotte Schampera
Shuting Liu
Luis M. Bolaños
Mats Heemeyer
Craig A. Carlson
Stephen Giovannoni
Ferdi L. Hellweger
author_facet Falk Eigemann
Jutta Hoffmann
Charlotte Schampera
Shuting Liu
Luis M. Bolaños
Mats Heemeyer
Craig A. Carlson
Stephen Giovannoni
Ferdi L. Hellweger
author_sort Falk Eigemann
collection DOAJ
description ABSTRACT 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 CO2 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 provides a basis and tool for further research in this area.
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spelling doaj-art-7344bc82337f4db2afbfa97f8c727df72024-11-13T14:03:28ZengAmerican Society for MicrobiologymBio2150-75112024-11-01151110.1128/mbio.02372-24Emergent ecology in a microscale model of the surface oceanFalk Eigemann0Jutta Hoffmann1Charlotte Schampera2Shuting Liu3Luis M. Bolaños4Mats Heemeyer5Craig A. Carlson6Stephen Giovannoni7Ferdi L. Hellweger8Water Quality Engineering, Technical University of Berlin, Berlin, GermanyWater Quality Engineering, Technical University of Berlin, Berlin, GermanyWater Quality Engineering, Technical University of Berlin, Berlin, GermanyMarine Science Institute/Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, California, USASchool of Biosciences, University of Exeter, Exeter, United KingdomWater Quality Engineering, Technical University of Berlin, Berlin, GermanyMarine Science Institute/Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, California, USADepartment of Microbiology, Oregon State University, Corvallis, Oregon, USAWater Quality Engineering, Technical University of Berlin, Berlin, GermanyABSTRACT 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 CO2 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 provides a basis and tool for further research in this area.https://journals.asm.org/doi/10.1128/mbio.02372-24microbial ecologybiogeochemical modelagent-based modelattachmentchemotaxisfitness
spellingShingle Falk Eigemann
Jutta Hoffmann
Charlotte Schampera
Shuting Liu
Luis M. Bolaños
Mats Heemeyer
Craig A. Carlson
Stephen Giovannoni
Ferdi L. Hellweger
Emergent ecology in a microscale model of the surface ocean
mBio
microbial ecology
biogeochemical model
agent-based model
attachment
chemotaxis
fitness
title Emergent ecology in a microscale model of the surface ocean
title_full Emergent ecology in a microscale model of the surface ocean
title_fullStr Emergent ecology in a microscale model of the surface ocean
title_full_unstemmed Emergent ecology in a microscale model of the surface ocean
title_short Emergent ecology in a microscale model of the surface ocean
title_sort emergent ecology in a microscale model of the surface ocean
topic microbial ecology
biogeochemical model
agent-based model
attachment
chemotaxis
fitness
url https://journals.asm.org/doi/10.1128/mbio.02372-24
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AT luismbolanos emergentecologyinamicroscalemodelofthesurfaceocean
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