Abstract
Deciphering the ecology of marine obligate hydrocarbonoclastic bacteria (MOHCB) is of crucial importance for understanding their success in occupying distinct niches in hydrocarbon-contaminated marine environments after oil spills. In marine coastal sediments, MOHCB are particularly subjected to extreme fluctuating conditions due to redox oscillations several times a day as a result of mechanical (tide, waves and currents) and biological (bioturbation) reworking of the sediment. The adaptation of MOHCB to the redox oscillations was investigated by an experimental ecology approach, subjecting a hydrocarbon-degrading microbial community to contrasting oxygenation regimes including permanent anoxic conditions, anoxic/oxic oscillations and permanent oxic conditions. The most ubiquitous MOHCB, Alcanivorax and Cycloclasticus, showed different behaviors, especially under anoxic/oxic oscillation conditions, which were more favorable for Alcanivorax than for Cycloclasticus. The micro-diversity of 16S rRNA gene transcripts from these genera revealed specific ecotypes for different oxygenation conditions and their dynamics. It is likely that such ecotypes allow the colonization of distinct ecological niches that may explain the success of Alcanivorax and Cycloclasticus in hydrocarbon-contaminated coastal sediments during oil-spills.
Highlights
Blooms of the marine obligate hydrocarbonoclastic bacteria (MOHCB) are usually observed after oil spills (Maruyama et al, 2003; Yakimov et al, 2007; Teramoto et al, 2013; Acosta-González et al, 2015; Duran and Cravo-Laureau, 2016; Yang et al, 2016a)
Previous studies demonstrated that anoxic/oxic oscillations promote organic matter biodegradation (Abril et al, 2010), and more hydrocarbon degradation (Cravo-Laureau et al, 2011; Vitte et al, 2011, 2013)
In our study the n-C17/pristane ratio (McKenna and Kallio, 1971) and phenanthrene/dimethylphenanthrene ratio (Michel and Hayes, 1999), used as indexes reporting the biodegradation for n-alkane and polyaromatic hydrocarbons (PAH) respectively, indicated that the most efficient biodegradation for n-alkanes was under anoxic/oxic oscillation condition while similar efficiency was observed for PAH biodegradation under permanent oxic and anoxic/oxic oscillation conditions at the end of incubation (Supplementary Figure 2)
Summary
Blooms of the marine obligate hydrocarbonoclastic bacteria (MOHCB) are usually observed after oil spills (Maruyama et al, 2003; Yakimov et al, 2007; Teramoto et al, 2013; Acosta-González et al, 2015; Duran and Cravo-Laureau, 2016; Yang et al, 2016a). Members of the genera Alcanivorax and Cycloclasticus are almost always detected in samples from marine environments around the world after oil input (Harayama et al, 2004; Yakimov et al, 2007; Brito et al, 2009; Said et al, 2010; Gutierrez et al, 2013; Louvado et al, 2015; Jeanbille et al, 2016; Kleindienst et al, 2016) Members of these ubiquitous genera occupy distinct trophic niches, where usually the aliphatic hydrocarbon degrader Alcanivorax blooms first, followed by the (poly-)aromatic hydrocarbon degrader Cycloclasticus, as polyaromatic hydrocarbons (PAH) are less amenable to degradation (Head et al, 2006). The microbial processes underlying the biodegradation of hydrocarbons within the anoxic/oxic transitional zone is not well understood (Cravo-Laureau et al, 2011; Cravo-Laureau and Duran, 2014), especially for MOHCB subjected to such extreme fluctuating conditions
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