Polysaccharide hydrolysis in the presence of oil and dispersants: Insights into potential degradation pathways of exopolymeric substances (EPS) from oil-degrading bacteria

Abstract

Oceanic oil-degrading bacteria produce copious amounts of exopolymeric substances (EPS) that facilitate their access to oil. The fate of EPS in the water column is in part determined by activities of heterotrophic microbes capable of utilizing EPS compounds as carbon and energy sources. To evaluate the potential of natural microbial communities to degrade EPS produced during oil degradation, we measured potential hydrolysis rates of six structurally distinct polysaccharides in two roller bottle experiments, using water from a natural oil seep in the northern Gulf of Mexico. The suite of polysaccharides used to measure the initial step in carbon degradation is indicative of polymers within microbial EPS. The treatments included (i) unamended surface or deep waters (whole water), and water amended with (ii) a water-accommodated fraction of oil (WAF), (iii) oil dispersant Corexit 9500, and (iv) WAF chemically-enhanced with Corexit (CEWAF). The oil and Corexit treatments were employed to simulate conditions during the Deepwater Horizon oil spill. Polysaccharide hydrolysis rates in the surface-water treatments were lowest in the WAF treatment, despite elevated levels of EPS in the form of transparent exopolymer particles (TEP). In contrast, the three deep-water treatments (WAF, Corexit, CEWAF) showed enhanced hydrolysis rates and TEP levels (WAF) compared to the whole water. We also observed variations in the spectrum of polysaccharide-hydrolyzing enzyme activities among the treatments. These substrate specificities were likely driven by activities of oil-degrading bacteria, shaping the pool of EPS and TEP as well as degradation products of hydrocarbons and Corexit compounds. A model calculation of potential turnover rates of organic carbon within the TEP pool suggests extended residence times of TEP in oil-contaminated waters, making them prone to serve as the sticky matrix for oily aggregates known as marine oil snow.

Bacteria-Oil Microaggregates Are an Important Mechanism for Hydrocarbon Degradation in the Marine Water Column

“…It also indicates that the rates of hydrocarbon degradation in BOMAs may be important in comparison to rates among free-living microorganisms. These findings are the first to link BOMAs to hydrocarbon degradation and are consistent with research showing marine snow and other biomass aggregates are hot spots for microbial activity ( 28 , 31 – 33 ).…”

“…Such organisms may be utilizing the degradation products of the hydrocarbons ( 29 ), the nutrient-rich EPS of the aggregates ( 32 ), or other cellular components. Indeed, high rates of polysaccharide degradation by heterotrophic species following the formation of oil aggregates have been observed in several studies (e.g., references 31 and 32 ) and were also observed during this experiment ( 33 ). This shift toward secondary consumers marks a successional cascade in the aggregated microbial community following the initial degradation of hydrocarbons and may serve as an indicator of oil spill recovery.…”

Marine Snow Aggregates are Enriched in Polycyclic Aromatic Hydrocarbons (PAHs) in Oil Contaminated Waters: Insights from a Mesocosm Study

“…Marine snow aggregates were reported to be hotspots of microbial activity being colonized by an abundant population of bacteria, with many known hydrocarbon degraders [48,80]. However, these bacteria might not be active in degrading PAHs, but utilizing alkanes and polysaccharides, the readily available carbon sources in the aggregates [39,81]. This is evident from our previous mesocosm experiments showing extracts from these aggregates showed characteristics of weathered oil depleted of n-alkanes and rich in oxygenated metabolites [47,51].…”

GoMRI Insights into Microbial Genomics and Hydrocarbon Bioremediation Response in Marine Ecosystems

“…One example is addition of nitrogen fertilizers, which has been proposed by GoMRI and other investigators to accelerate microbial bioremediation (Edwards et al, 2011;Kleindienst et al, 2015b;Fernández-Carrera et al, 2016). Additionally, enhancement of microbes that produce exopolymeric substances, which emulsify oil and act like dispersants, could preclude addition of man-made dispersants such as Corexit (Ziervogel et al, 2019). Strategies to promote growth of native microbial species or utilization of genetically engineered microbes for natural surfactant production would provide responders with biodegradable, nontoxic surfactant alternatives.…”