A Model of Extracellular Enzymes in Free-Living Microbes: Which Strategy Pays Off?

Abstract

An initial modeling approach was applied to analyze how a single, nonmotile, free-living, heterotrophic bacterial cell may optimize the deployment of its extracellular enzymes. Free-living cells live in a dilute and complex substrate field, and to gain enough substrate, their extracellular enzymes must be utilized efficiently. The model revealed that surface-attached and free enzymes generate unique enzyme and substrate fields, and each deployment strategy has distinctive advantages. For a solitary cell, surface-attached enzymes are suggested to be the most cost-efficient strategy. This strategy entails potential substrates being reduced to very low concentrations. Free enzymes, on the other hand, generate a radically different substrate field, which suggests significant benefits for the strategy if free cells engage in social foraging or experience high substrate concentrations. Swimming has a slight positive effect for the attached-enzyme strategy, while the effect is negative for the free-enzyme strategy. The results of this study suggest that specific dissolved organic compounds in the ocean likely persist below a threshold concentration impervious to biological utilization. This could help explain the persistence and apparent refractory state of oceanic dissolved organic matter (DOM). Microbial extracellular enzyme strategies, therefore, have important implications for larger-scale processes, such as shaping the role of DOM in ocean carbon sequestration. Dissolved organic matter (DOM) in the oceans is one of the largest active reservoirs of organic carbon in the biosphere (1). An intricate web of biotic (e.g., photosynthesis, viral lysis, and grazing) and abiotic (e.g., photodegradation and aggregation) processes contribute to the physical and chemical complexity of DOM (2-4). However, DOM is almost exclusively exploited by the bacterioplankton (5, 6). Microbes face several challenges when consuming DOM. While small molecules approximately 600 to 800 Da in size can be taken up directly (7,8), larger compounds need to be enzymatically hydrolyzed outside the cell before uptake. This two-phase system of hydrolysis and subsequent uptake is a rate-limiting step of microbial enzymatic degradation (9-11), and a mechanistic understanding of these processes, therefore, is of global biogeochemical relevance. Furthermore, the bacterioplankton are faced with the challenges of spatial heterogeneity (12, 13) and individual compounds at extremely dilute concentrations (14-16). For a microbe, there is presumably a delicate balance between the substrate encounter rate and the energy cost associated with carrying and maintaining an enzymatic apparatus for substrate uptake.It has been proposed that bacteria have adapted to the "landscape" of marine DOM by two very different trophic strategies. Copiotrophs use a "feast and famine" strategy where they proliferate from low abundances upon exposure to high substrate levels (17), such as in association with detrital aggregates or phytoplankton blooms. Copiotrophs are distinguished...

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