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

Alberto Scoma, Robert Heyer, Ridwan Rifai, Christian Dandyk, Ian Marshall, Frederiek-Maarten Kerchhop, Angeliki Marietou, Henricus Boshker, Filip Meysman, Kirsten Malmos, Thomas Vosegaard, Pieter Vermeir, Ibrahim Banat, Dirk Benndorf, Nico Boon

Research output: Contribution to journalArticle

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Abstract

Petroleum hydrocarbons reach the deep-sea following natural and anthropogenic factors. The process by which they enter deepsea 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 1000m below sea surface level) than at ambient pressure. In longterm enrichments, increased HP selectively inhibited obligate hydrocarbon-degraders and downregulated the expression of betaoxidation-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.
LanguageEnglish
JournalThe ISME journal
Publication statusPublished - 12 Dec 2018

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Hydrostatic Pressure
hydrostatic pressure
Hydrocarbons
Oceans and Seas
microbial communities
deep sea
hydrocarbons
microbial community
Oils
hydrocarbon
oils
degradation
oil
Dihydroxyacetone
Citric Acid
citrates
rate
Food Chain
Petroleum
beta oxidation

Cite this

Scoma, Alberto ; Heyer, Robert ; Rifai, Ridwan ; Dandyk, Christian ; Marshall, Ian ; Kerchhop, Frederiek-Maarten ; Marietou, Angeliki ; Boshker, Henricus ; Meysman, Filip ; Malmos, Kirsten ; Vosegaard, Thomas ; Vermeir, Pieter ; Banat, Ibrahim ; Benndorf, Dirk ; Boon, Nico. / Reduced TCA cycle rates at high hydrostatic pressure hinder hydrocarbon degradation and obligate oil degraders in natural, deep-sea microbial communities. In: The ISME journal. 2018.
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abstract = "Petroleum hydrocarbons reach the deep-sea following natural and anthropogenic factors. The process by which they enter deepsea 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 activityof 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 1000m below sea surface level) than at ambient pressure. In longterm enrichments, increased HP selectively inhibited obligate hydrocarbon-degraders and downregulated the expression of betaoxidation-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 cellmetabolism 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.",
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Scoma, A, Heyer, R, Rifai, R, Dandyk, C, Marshall, I, Kerchhop, F-M, Marietou, A, Boshker, H, Meysman, F, Malmos, K, Vosegaard, T, Vermeir, P, Banat, I, Benndorf, D & Boon, N 2018, 'Reduced TCA cycle rates at high hydrostatic pressure hinder hydrocarbon degradation and obligate oil degraders in natural, deep-sea microbial communities', The ISME journal.

Reduced TCA cycle rates at high hydrostatic pressure hinder hydrocarbon degradation and obligate oil degraders in natural, deep-sea microbial communities. / Scoma, Alberto; Heyer, Robert; Rifai, Ridwan ; Dandyk, Christian; Marshall, Ian ; Kerchhop, Frederiek-Maarten; Marietou, Angeliki; Boshker, Henricus; Meysman, Filip; Malmos, Kirsten; Vosegaard, Thomas ; Vermeir, Pieter ; Banat, Ibrahim; Benndorf, Dirk; Boon, Nico.

In: The ISME journal, 12.12.2018.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Reduced TCA cycle rates at high hydrostatic pressure hinder hydrocarbon degradation and obligate oil degraders in natural, deep-sea microbial communities

AU - Scoma, Alberto

AU - Heyer, Robert

AU - Rifai, Ridwan

AU - Dandyk, Christian

AU - Marshall, Ian

AU - Kerchhop, Frederiek-Maarten

AU - Marietou, Angeliki

AU - Boshker, Henricus

AU - Meysman, Filip

AU - Malmos, Kirsten

AU - Vosegaard, Thomas

AU - Vermeir, Pieter

AU - Banat, Ibrahim

AU - Benndorf, Dirk

AU - Boon, Nico

PY - 2018/12/12

Y1 - 2018/12/12

N2 - Petroleum hydrocarbons reach the deep-sea following natural and anthropogenic factors. The process by which they enter deepsea 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 activityof 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 1000m below sea surface level) than at ambient pressure. In longterm enrichments, increased HP selectively inhibited obligate hydrocarbon-degraders and downregulated the expression of betaoxidation-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 cellmetabolism 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.

AB - Petroleum hydrocarbons reach the deep-sea following natural and anthropogenic factors. The process by which they enter deepsea 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 activityof 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 1000m below sea surface level) than at ambient pressure. In longterm enrichments, increased HP selectively inhibited obligate hydrocarbon-degraders and downregulated the expression of betaoxidation-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 cellmetabolism 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.

UR - https://doi.org/10.1038/s41396-018-0324-5

M3 - Article

JO - ISME Journal

T2 - ISME Journal

JF - ISME Journal

SN - 1751-7362

ER -