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Reduced TCA cycle rates at high hydrostatic pressure hinder hydrocarbon degradation and obligate oil degraders in natural, deep-sea microbial communities

(2019) ISME JOURNAL. 13(4). p.1004-1018
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Abstract
Petroleum hydrocarbons reach the deep-sea following natural and anthropogenic factors. The process by which they enter deep-sea microbial food webs and impact the biogeochemical cycling of carbon and other elements is unclear. Hydrostatic pressure (HP) is a distinctive parameter of the deep sea, although rarely investigated. Whether HP alone affects the assembly and activity of oil-degrading communities remains to be resolved. Here we have demonstrated that hydrocarbon degradation in deep-sea microbial communities is lower at native HP (10 MPa, about 1000 m below sea surface level) than at ambient pressure. In long-term enrichments, increased HP selectively inhibited obligate hydrocarbon-degraders and downregulated the expression of beta-oxidation-related proteins (i.e., the main hydrocarbon-degradation pathway) resulting in low cell growth and CO2 production. Short-term experiments with HP-adapted synthetic communities confirmed this data, revealing a HP-dependent accumulation of citrate and dihydroxyacetone. Citrate accumulation suggests rates of aerobic oxidation of fatty acids in the TCA cycle were reduced. Dihydroxyacetone is connected to citrate through glycerol metabolism and glycolysis, both upregulated with increased HP. High degradation rates by obligate hydrocarbon-degraders may thus be unfavourable at increased HP, explaining their selective suppression. Through lab-scale cultivation, the present study is the first to highlight a link between impaired cell metabolism and microbial community assembly in hydrocarbon degradation at high HP. Overall, this data indicate that hydrocarbons fate differs substantially in surface waters as compared to deep-sea environments, with in situ low temperature and limited nutrients availability expected to further prolong hydrocarbons persistence at deep sea.
Keywords
GEN. NOV., LACTOCOCCUS-LACTIS, MARINE BACTERIUM, INTRACELLULAR PH, WATER, GROWTH, SPILL, BIODEGRADATION, MECHANISMS, PATHWAYS

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MLA
Scoma, Alberto, et al. “Reduced TCA Cycle Rates at High Hydrostatic Pressure Hinder Hydrocarbon Degradation and Obligate Oil Degraders in Natural, Deep-Sea Microbial Communities.” ISME JOURNAL, vol. 13, no. 4, 2019, pp. 1004–18.
APA
Scoma, A., Heyer, R., Rifai, R. M., Dandyk, C., Marshall, I., Kerckhof, F.-M., … Boon, N. (2019). Reduced TCA cycle rates at high hydrostatic pressure hinder hydrocarbon degradation and obligate oil degraders in natural, deep-sea microbial communities. ISME JOURNAL, 13(4), 1004–1018.
Chicago author-date
Scoma, Alberto, Robert Heyer, Ridwan Muhamad Rifai, Christian Dandyk, Ian Marshall, Frederiek-Maarten Kerckhof, Angeliki Marietou, et al. 2019. “Reduced TCA Cycle Rates at High Hydrostatic Pressure Hinder Hydrocarbon Degradation and Obligate Oil Degraders in Natural, Deep-Sea Microbial Communities.” ISME JOURNAL 13 (4): 1004–18.
Chicago author-date (all authors)
Scoma, Alberto, Robert Heyer, Ridwan Muhamad Rifai, Christian Dandyk, Ian Marshall, Frederiek-Maarten Kerckhof, Angeliki Marietou, Henricus TS Boshker, Filip JR Meysman, Kirsten G Malmos, Thomas Vosegaard, Pieter Vermeir, Ibrahim M Banat, Dirk Benndorf, and Nico Boon. 2019. “Reduced TCA Cycle Rates at High Hydrostatic Pressure Hinder Hydrocarbon Degradation and Obligate Oil Degraders in Natural, Deep-Sea Microbial Communities.” ISME JOURNAL 13 (4): 1004–1018.
Vancouver
1.
Scoma A, Heyer R, Rifai RM, Dandyk C, Marshall I, Kerckhof F-M, et al. Reduced TCA cycle rates at high hydrostatic pressure hinder hydrocarbon degradation and obligate oil degraders in natural, deep-sea microbial communities. ISME JOURNAL. 2019;13(4):1004–18.
IEEE
[1]
A. Scoma et al., “Reduced TCA cycle rates at high hydrostatic pressure hinder hydrocarbon degradation and obligate oil degraders in natural, deep-sea microbial communities,” ISME JOURNAL, vol. 13, no. 4, pp. 1004–1018, 2019.
@article{8590096,
  abstract     = {Petroleum hydrocarbons reach the deep-sea following natural and anthropogenic factors. The process by which they enter deep-sea microbial food webs and impact the biogeochemical cycling of carbon and other elements is unclear. Hydrostatic pressure (HP) is a distinctive parameter of the deep sea, although rarely investigated. Whether HP alone affects the assembly and activity of oil-degrading communities remains to be resolved. Here we have demonstrated that hydrocarbon degradation in deep-sea microbial communities is lower at native HP (10 MPa, about 1000 m below sea surface level) than at ambient pressure. In long-term enrichments, increased HP selectively inhibited obligate hydrocarbon-degraders and downregulated the expression of beta-oxidation-related proteins (i.e., the main hydrocarbon-degradation pathway) resulting in low cell growth and CO2 production. Short-term experiments with HP-adapted synthetic communities confirmed this data, revealing a HP-dependent accumulation of citrate and dihydroxyacetone. Citrate accumulation suggests rates of aerobic oxidation of fatty acids in the TCA cycle were reduced. Dihydroxyacetone is connected to citrate through glycerol metabolism and glycolysis, both upregulated with increased HP. High degradation rates by obligate hydrocarbon-degraders may thus be unfavourable at increased HP, explaining their selective suppression. Through lab-scale cultivation, the present study is the first to highlight a link between impaired cell metabolism and microbial community assembly in hydrocarbon degradation at high HP. Overall, this data indicate that hydrocarbons fate differs substantially in surface waters as compared to deep-sea environments, with in situ low temperature and limited nutrients availability expected to further prolong hydrocarbons persistence at deep sea.},
  author       = {Scoma, Alberto and Heyer, Robert and Rifai, Ridwan Muhamad and Dandyk, Christian and Marshall, Ian and Kerckhof, Frederiek-Maarten and Marietou, Angeliki and Boshker, Henricus TS and Meysman, Filip JR and Malmos, Kirsten G and Vosegaard, Thomas and Vermeir, Pieter and Banat, Ibrahim M and Benndorf, Dirk and Boon, Nico},
  issn         = {1751-7362},
  journal      = {ISME JOURNAL},
  keywords     = {GEN. NOV.,LACTOCOCCUS-LACTIS,MARINE BACTERIUM,INTRACELLULAR PH,WATER,GROWTH,SPILL,BIODEGRADATION,MECHANISMS,PATHWAYS},
  language     = {eng},
  number       = {4},
  pages        = {1004--1018},
  title        = {Reduced TCA cycle rates at high hydrostatic pressure hinder hydrocarbon degradation and obligate oil degraders in natural, deep-sea microbial communities},
  url          = {http://dx.doi.org/10.1038/s41396-018-0324-5},
  volume       = {13},
  year         = {2019},
}

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