Abstract

Halomonas species are recognized for producing exopolysaccharides (EPS) exhibiting amphiphilic properties that allow these macromolecules to interface with hydrophobic substrates, such as hydrocarbons. There remains a paucity of knowledge, however, on the potential of Halomonas EPS to influence the biodegradation of hydrocarbons. In this study, the well-characterized amphiphilic EPS produced by Halomonas species strain TG39 was shown to effectively increase the solubilization of aromatic hydrocarbons and enhance their biodegradation by an indigenous microbial community from oil-contaminated surface waters collected during the active phase of the Deepwater Horizon oil spill. Three Halomonas strains were isolated from the Deepwater Horizon site, all of which produced EPS with excellent emulsifying qualities and shared high (97-100%) 16S rRNA sequence identity with strain TG39 and other EPS-producing Halomonas strains. Analysis of pyrosequence data from surface water samples collected during the spill revealed several distinct Halomonas phylotypes, of which some shared a high sequence identity (≥97%) to strain TG39 and the Gulf spill isolates. Other bacterial groups comprising members with well-characterized EPS-producing qualities, such as Alteromonas , Colwellia and Pseudoalteromonas , were also found enriched in surface waters, suggesting that the total pool of EPS in the Gulf during the spill may have been supplemented by these organisms. Roller bottle incubations with one of the Halomonas isolates from the Deepwater Horizon spill site demonstrated its ability to effectively produce oil aggregates and emulsify the oil. The enrichment of EPS-producing bacteria during the spill coupled with their capacity to produce amphiphilic EPS is likely to have contributed to the ultimate removal of the oil and to the formation of oil aggregates, which were a dominant feature observed in contaminated surface waters.

Highlights

  • Dissolved organic matter (DOM) in the ocean is the largest and possibly least understood pool of carbon - ca. 6.9 x 1017 g C, which is comparable in mass to the carbon in atmospheric CO2 [1]

  • We report on the isolation of three EPSproducing strains of Halomonas from oil-contaminated surface waters during the active phase of the Deepwater Horizon oil spill

  • Dissolution and biodegradation of hydrocarbons, with particular reference to the role that EPS-producing bacteria contributed to the fate of the oil released from the blowout of the Macondo well at Deepwater Horizon

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Summary

Introduction

Dissolved organic matter (DOM) in the ocean is the largest and possibly least understood pool of carbon - ca. 6.9 x 1017 g C, which is comparable in mass to the carbon in atmospheric CO2 [1]. A major fraction of marine DOM derives from the synthesis and release of extracellular polymeric substances or exopolysaccharides (EPS) by bacteria and eukaryotic phytoplankton [4,5]. These are high molecular weight polymers composed mainly of monosaccharides, some of which may contain noncarbohydrate substituents. The negative charge associated with carboxyl groups of uronic acids of EPS has been implicated in the capacity of these macromolecules to complex with transition metals [7,8]. There is a growing body of evidence to implicate uronic acids of EPS in conferring these macromolecules with an ability to interface with hydrophobic organic chemicals, such as hydrocarbons [11]–[13]. The potential significance of marine bacterial EPS to influencing the fate and ultimate degradation of hydrocarbon pollutants in the ocean, during oil spills, remains largely unknown

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