Single-cell genomics reveals features of a Colwellia species that was dominant during the Deepwater Horizon oil spill

Abstract

During the Deepwater Horizon (DWH) oil spill in the Gulf of Mexico a deep-sea hydrocarbon plume developed resulting in a rapid succession of bacteria. Colwellia eventually supplanted Oceanospirillales, which dominated the plume early in the spill. These successional changes may have resulted, in part, from the changing composition and abundance of hydrocarbons over time. Colwellia abundance peaked when gaseous and simple aromatic hydrocarbons increased, yet the metabolic pathway used by Colwellia in hydrocarbon disposition is unknown. Here we used single-cell genomics to gain insights into the genome properties of a Colwellia enriched during the DWH deep-sea plume. A single amplified genome (SAG) of a Colwellia cell isolated from a DWH plume, closely related (avg. 98% 16S rRNA gene similarity) to other plume Colwellia, was sequenced and annotated. The SAG was similar to the sequenced isolate Colwellia psychrerythraea 34H (84% avg. nucleotide identity). Both had genes for denitrification, chemotaxis, and motility, adaptations to cold environments and a suite of nutrient acquisition genes. The Colwellia SAG may be capable of gaseous and aromatic hydrocarbon degradation, which contrasts with a DWH plume Oceanospirillales SAG which encoded non-gaseous n-alkane and cycloalkane degradation pathways. The disparate hydrocarbon degradation pathways are consistent with hydrocarbons that were abundant at different times in the deep-sea plume; first, non-gaseous n-alkanes and cycloalkanes that could be degraded by Oceanospirillales, followed by gaseous, and simple aromatic hydrocarbons that may have been degraded by Colwellia. These insights into the genomic properties of a Colwellia species, which were supported by existing metagenomic sequence data from the plume and DWH contaminated sediments, help further our understanding of the successional changes in the dominant microbial players in the plume over the course of the DWH spill.

Diverse, rare microbial taxa responded to the Deepwater Horizon deep-sea hydrocarbon plume

“…The bar represents 10% estimated sequence divergence. oxidize methane (Lai et al, 2012;Mason et al, 2014). However, the positive correlation of these oligotypes with methane oxidation rates implies either their indirect involvement in this process (for example, through oxidation of co-metabolites or reaction byproducts) or their coexistence with methane oxidizers (for example, in plume samples, where methane, alkanes and PAHs coexisted) or possibly an unrecognized potential to oxidize methane.…”

Syntrophic Interactions Within a Butane-Oxidizing Bacterial Consortium Isolated from Puguang Gas Field in China

“…4). This pathway was the same as estimated in P. butanovora [17] and in a Colwellia species [29]. It was clear that the butane oxidization was inhibited by butanol accumulation, known as intermediate metabolite feedback inhibition that is a common mechanism for organisms to control the biosynthetic pathways [30][31][32].…”

Atmospheric aerosol deposition influences marine microbial communities in oligotrophic surface waters of the western Pacific Ocean

“…Members of Colwelliaceae are also known to degrade organic matter, such as aromatic hydrocarbons, which are stable in aquatic environments (Mason et al, 2014). Moreover, the bacterial species belonging to the families Rhodobacteraceae (Wagner-Döbler and Biebl, 2006) and Colwelliaceae (Mason et al, 2014) have been reported to consume nitrate via denitrification pathways.…”

“…Members of Colwelliaceae are also known to degrade organic matter, such as aromatic hydrocarbons, which are stable in aquatic environments (Mason et al, 2014). Moreover, the bacterial species belonging to the families Rhodobacteraceae (Wagner-Döbler and Biebl, 2006) and Colwelliaceae (Mason et al, 2014) have been reported to consume nitrate via denitrification pathways. Therefore, in the snow solution-treated seawater, increased nitrate and organic matter leading to more yellow particles and microalgal cells, would induce the growth of heterotrophic bacteria (including representatives from the Colwelliaceae and Rhodobacteraceae), implying consequences for the carbon cycle in these aerosol-affected waters.…”