A tradeoff between physical encounters and consumption determines an optimal droplet size for microbial degradation of dispersed oil

Abstract

Immiscible hydrocarbons occur in the ocean water column as droplets of varying diameters. Although microbial oil degradation is a central process in the remediation of hydrocarbon pollution in marine environments, the relationship between droplet size distribution and oil degradation rates by bacteria remains unclear, with a conflicting history of laboratory studies. Despite this knowledge gap, the use of chemical dispersants in oil spill response and mitigation is based on the rationale that increasing the surface-area-to-volume ratio of droplets will enhance net bacterial biodegradation rates. We demonstrate that this intuitive argument does not apply to most natural marine environments, where the abundance of oil droplets is much lower than in laboratory experiments and droplet-bacteria encounters are the limiting factor. We present a mechanistic encounter-consumption model to predict the characteristic time for oil degradation by marine bacteria as a function of the initial oil concentration, the distribution of droplet sizes, and the initial abundance of oil-degrading bacteria. We find that the tradeoff between the encounter time and the consumption time leads to an optimal droplet size larger than the average size generated by the application of dispersants. Reducing droplet size below this optimum can increase the persistence of oil droplets in the environment from weeks to years. The new perspective granted by this biophysical model of biodegradation that explicitly accounts for oil–microbe encounters changes our understanding of biodegradation particularly in the deep ocean, where droplets are often small and oil concentrations low, and explains degradation rate discrepancies between laboratory and field studies.