Dataset Information

Constrained optimal foraging by marine bacterioplankton on particulate organic matter.

ABSTRACT: Optimal foraging theory provides a framework to understand how organisms balance the benefits of harvesting resources within a patch with the sum of the metabolic, predation, and missed opportunity costs of foraging. Here, we show that, after accounting for the limited environmental information available to microorganisms, optimal foraging theory and, in particular, patch use theory also applies to the behavior of marine bacteria in particle seascapes. Combining modeling and experiments, we find that the marine bacterium Vibrio ordalii optimizes nutrient uptake by rapidly switching between attached and planktonic lifestyles, departing particles when their nutrient concentration is more than hundredfold higher than background. In accordance with predictions from patch use theory, single-cell tracking reveals that bacteria spend less time on nutrient-poor particles and on particles within environments that are rich or in which the travel time between particles is smaller, indicating that bacteria tune the nutrient concentration at detachment to increase their fitness. A mathematical model shows that the observed behavioral switching between exploitation and dispersal is consistent with foraging optimality under limited information, namely, the ability to assess the harvest rate of nutrients leaking from particles by molecular diffusion. This work demonstrates how fundamental principles in behavioral ecology traditionally applied to animals can hold right down to the scale of microorganisms and highlights the exquisite adaptations of marine bacterial foraging. The present study thus provides a blueprint for a mechanistic understanding of bacterial uptake of dissolved organic matter and bacterial production in the ocean-processes that are fundamental to the global carbon cycle.

SUBMITTER: Yawata Y

PROVIDER: S-EPMC7568300 | biostudies-literature | 2020 Oct

REPOSITORIES: biostudies-literature

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Constrained optimal foraging by marine bacterioplankton on particulate organic matter.

Yawata Yutaka Y Carrara Francesco F Menolascina Filippo F Stocker Roman R

Proceedings of the National Academy of Sciences of the United States of America 20200924 41

Optimal foraging theory provides a framework to understand how organisms balance the benefits of harvesting resources within a patch with the sum of the metabolic, predation, and missed opportunity costs of foraging. Here, we show that, after accounting for the limited environmental information available to microorganisms, optimal foraging theory and, in particular, patch use theory also applies to the behavior of marine bacteria in particle seascapes. Combining modeling and experiments, we find ...[more]

PMID: 32973087

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Project description:The biological carbon pump (BCP) in the Southern Ocean is driven by phytoplankton productivity and is a significant organic matter sink. However, the role of particle-attached (PA) and free-living (FL) prokaryotes (bacteria and archaea) and their diversity in influencing the efficiency of the BCP is still unclear. To investigate this, we analyzed the metagenomes linked to suspended and sinking marine particles from the Sub-Antarctic Southern Ocean Time Series (SOTS) by deploying a Marine Snow Catcher (MSC), obtaining suspended and sinking particulate material, determining organic carbon and nitrogen flux, and constructing metagenome-assembled genomes (MAGs). The suspended and sinking particle-pools were dominated by bacteria with the potential to degrade organic carbon. Bacterial communities associated with the sinking fraction had more genes related to the degradation of complex organic carbon than those in the suspended fraction. Archaea had the potential to drive nitrogen metabolism via nitrite and ammonia oxidation, altering organic nitrogen concentration. The data revealed several pathways for chemoautotrophy and the secretion of recalcitrant dissolved organic carbon (RDOC) from CO2, with bacteria and archaea potentially sequestering particulate organic matter (POM) via the production of RDOC. These findings provide insights into the diversity and function of prokaryotes in suspended and sinking particles and their role in organic carbon/nitrogen export in the Southern Ocean. IMPORTANCE The biological carbon pump is crucial for the export of particulate organic matter in the ocean. Recent studies on marine microbes have shown the profound influence of bacteria and archaea as regulators of particulate organic matter export. Yet, despite the importance of the Southern Ocean as a carbon sink, we lack comparable insights regarding microbial contributions. This study provides the first insights regarding prokaryotic contributions to particulate organic matter export in the Southern Ocean. We reveal evidence that prokaryotic communities in suspended and sinking particle fractions harbor widespread genomic potential for mediating particulate organic matter export. The results substantially enhance our understanding of the role played by microorganisms in regulating particulate organic matter export in suspended and sinking marine fractions in the Southern Ocean.

Dataset Information

Constrained optimal foraging by marine bacterioplankton on particulate organic matter.

Publications

Constrained optimal foraging by marine bacterioplankton on particulate organic matter.

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