Snorkels enhance alkanes respiration at ambient and increased hydrostatic pressure (10 MPa) by either supporting the TCA cycle or limiting alternative routes for acetyl-CoA metabolism

Abstract

The impact of piezosensitive microorganisms is generally underestimated in the ecology of underwater environments exposed to increasing hydrostatic pressure (HP), including the biodegradation of crude oil components. Yet, no isolated pressure-loving (piezophile) microorganism grows optimally on hydrocarbons, and no isolated piezophile at all has a HP optimum <10 MPa (e.g. 1000 m below sea water level). Piezosensitive heterotrophs are thus largely accountable for oil clean up < 10 MPa, however, they are affected by such a mild HP increase in ways which are not completely clear. In a first study, the application of a bioelectrochemical system (called "oil-spill snorkel") enhanced the alkane oxidation capacity in sediments collected at surface water but tested up to 10 MPa. Here, the fingerprint left on transcript abundance was studied to explore which metabolic routes are 1) supported by snorkels application and 2) negatively impacted by HP increase. Transcript abundance was comparable for beta-oxidation across all treatments (also at a taxonomical level), while the metabolism of acetyl-CoA was highly impacted: at either 0.1 or 10 MPa, snorkels supported acetyl-CoA oxidation within the TCA cycle, while in negative controls using non-conductive rods several alternative routes for acetyl-CoA were stimulated (including those leading to internal carbon reserves e.g. 2,3 butanediol and dihydroxyacetone). In general, increased HP had opposite effects as compared to snorkels, thus indicating that snorkels could enhance hydrocarbons oxidation by alleviating in part the stressing effects imposed by increased HP on the anaerobic, respiratory electron transport chain. 16S rRNA gene analysis of sediments and biofilms on snorkels suggest a crosstalk between oil-degrading, sulfate-reducing microorganisms and sulfur oxidizers. In fact, no sulfur was deposited on snorkels, however, iron, aluminum and phosphorous were found to preferentially deposit on snorkels at 10 MPa. This data indicates that a passive BES such as the oil-spill snorkel can mitigate the stress imposed by increased HP on piezosensitive microorganisms (up to 10 MPa) without being subjected to passivation. An improved setup applying these principles can further support this deep-sea bioremediation strategy.

Keywords: BES; Crude oil; Deep sea; Metatranscriptomics; Oil spill; Petroleum.