Hydrocarbon-degradation and MOS-formation capabilities of the dominant bacteria enriched in sea surface oil slicks during the Deepwater Horizon oil spill

Gutiérrez, Tony; Morris, Gordon A.; Ellis, Dave; Bowler, Bernard; Jones, Martin; Sałek, Karina; Mulloy, Barbara; Teske, Andreas

doi:10.1016/j.marpolbul.2018.07.027

Cited by 34 publications

(43 citation statements)

References 71 publications

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“…This pattern agrees with our previous work on polysaccharide hydrolysis in Gulf of Mexico surface waters (Ziervogel et al, 2011;Steen et al, 2012). The ability to degrade laminarin (glucose polymer) and xylan (xylose polymer) is widespread among marine bacteria (Arnosti et al, 2011), as glucose and xylose polymers are among the most abundant components of the marine DOM pool (McCarthy et al, 1996), including microbial EPS (Bhaskar et al, 2005;Alderkamp et al, 2007;Casillo et al, 2018;Gutierrez et al, 2018;Xu et al, 2018). In contrast, low or near-zero hydrolysis of arabinogalactan (i.e., a mixed polymers of galactose and arabinose; Table 1), as observed in our treatments, has been reported in different marine environments (Arnosti et al, 2011), emphasizing that chemical complexity may impede enzymatic degradation of specific substrates.…”

Section: Polysaccharide Hydrolysis Patterns In the Surface-water Rollsupporting

confidence: 90%

“…Enzymes that specifically hydrolyze these substrates have been identified in a variety of marine environments (Arnosti et al, 2011) as well as in the genomes of recently sequenced marine bacterial isolates (Glöckner et al, 2003;Bauer et al, 2006;Weiner et al, 2008). Moreover, most of the structural monosaccharides of the six polysaccharides used here were found in the EPS pool from Gulf of Mexico surfacewater microbial assemblages experimentally exposed to oil and Corexit (Xu et al, 2018), and from bacteria isolates associated with oil slicks from the 2010 Gulf of Mexico spill (Gutierrez et al, 2018).…”

Section: Research Articlementioning

confidence: 93%

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

Ziervogel

Joye

Kleindienst

et al. 2019

Elementa: Science of the Anthropocene

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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.

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Section: Polysaccharide Hydrolysis Patterns In the Surface-water Rollsupporting

confidence: 90%

Section: Research Articlementioning

confidence: 93%

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

Ziervogel

Joye

Kleindienst

et al. 2019

Elementa: Science of the Anthropocene

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“…In oil‐contaminated seawaters, hydrocarbons aggregate with suspended organic matter, forming marine oil snow (MOS). Field and laboratory studies have indicated that MOS constitutes hot spots of oil‐degrading and extracellular polymeric substance (EPS)‐producing bacteria (Sun and Zheng, ; Baelum et al ., ; Ziervogel et al ., ; Decho and Gutierrez, ; Gutierrez et al ., ). Likewise, cultures of hydrocarbonoclastic strains on pure hydrocarbons often result in the formation of oleolytic biofilms at the water–hydrocarbon interface (Fig.…”

Section: Biofilm Formation On Organic Particles Is a Widespread Stratmentioning

confidence: 97%

“…The observation that bacteria growing on the surface of chitin (Margolis et al ., ), cellulose (Miron et al ., ; Weimer et al ., ) or hydrocarbons (Baldi et al ., ; Whyte et al ., ; Gutierrez et al ., ) produce EPSs suggesting a general role for EPSs in adhesion to nutritive surfaces or between cells. In MOS, EPSs secreted by bacteria are thought to mediate the interaction of bacteria with oil (Gutierrez et al ., ). EPSs could be common molecular mediators of the adhesion to hydrocarbons in different bacterial species.…”

Section: Mechanisms Of Adhesion To Nutritive Surfacesmentioning

confidence: 97%

“…A series of studies on the EPSs produced by bacteria inhabiting MOS revealed their amphiphilic character and emulsifying activity and demonstrated that they were able to stimulate the biodegradation of hydrocarbons. Together, these data suggest that MOS EPS could interact with hydrocarbons to increase mass transfer to the cells (Gutierrez et al ., ).…”

Section: The Eps Matrix As An External Digestion Systemmentioning

confidence: 97%

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Biofilm formation as a microbial strategy to assimilate particulate substrates

Sivadon

Barnier

Urios

et al. 2019

Environmental Microbiology Reports

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Summary In most ecosystems, a large part of the organic carbon is not solubilized in the water phase. Rather, it occurs as particles made of aggregated hydrophobic and/or polymeric natural or man‐made organic compounds. These particulate substrates are degraded by extracellular digestion/solubilization implemented by heterotrophic bacteria that form biofilms on them. Organic particle‐degrading biofilms are widespread and have been observed in aquatic and terrestrial natural ecosystems, in polluted and man‐driven environments and in the digestive tracts of animals. They have central ecological functions as they are major players in carbon recycling and pollution removal. The aim of this review is to highlight bacterial adhesion and biofilm formation as central mechanisms to exploit the nutritive potential of organic particles. It focuses on the mechanisms that allow access and assimilation of non‐dissolved organic carbon, and considers the advantage provided by biofilms for gaining a net benefit from feeding on particulate substrates. Cooperative and competitive interactions taking place in biofilms feeding on particulate substrates are also discussed.

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