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

Marta Barbato; Enza Palma; Ugo Marzocchi; Carolina Cruz Viggi; Simona Rossetti; Federico Aulenta; Alberto Scoma

doi:10.1016/j.jenvman.2022.115244

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

Marta Barbato
, Enza Palma
, Ugo Marzocchi
, Carolina Cruz Viggi
, Simona Rossetti
, Federico Aulenta^*
, Alberto Scoma^*

^*Corresponding author for this work

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

1 Citation (Scopus)

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.

Original language	English
Article number	115244
Journal	Journal of Environmental Management
Volume	316
Number of pages	16
ISSN	0301-4797
DOIs	https://doi.org/10.1016/j.jenvman.2022.115244
Publication status	Published - Aug 2022

Keywords

BES
Crude oil
Deep sea
Metatranscriptomics
Oil spill
Petroleum
sediments
Biodegradation, Environmental
Petroleum Pollution
RNA, Ribosomal, 16S/genetics
Alkanes
Hydrocarbons/metabolism
Hydrostatic Pressure
Acetyl Coenzyme A
Petroleum/metabolism
Geologic Sediments/chemistry
Respiration

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Barbato, M., Palma, E., Marzocchi, U., Cruz Viggi, C., Rossetti, S., Aulenta, F., & Scoma, A. (2022). 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. Journal of Environmental Management, 316, Article 115244. https://doi.org/10.1016/j.jenvman.2022.115244

@article{d12a4f4eaabf4be385ec1c6858ade5d8,

title = "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, sediments, Biodegradation, Environmental, Petroleum Pollution, RNA, Ribosomal, 16S/genetics, Alkanes, Hydrocarbons/metabolism, Hydrostatic Pressure, Acetyl Coenzyme A, Petroleum/metabolism, Geologic Sediments/chemistry, Respiration",

author = "Marta Barbato and Enza Palma and Ugo Marzocchi and \{Cruz Viggi\}, Carolina and Simona Rossetti and Federico Aulenta and Alberto Scoma",

year = "2022",

month = aug,

doi = "10.1016/j.jenvman.2022.115244",

language = "English",

volume = "316",

journal = "Journal of Environmental Management",

issn = "0301-4797",

publisher = "Academic Press",

}

Barbato, M, Palma, E, Marzocchi, U, Cruz Viggi, C, Rossetti, S, Aulenta, F & Scoma, A 2022, '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', Journal of Environmental Management, vol. 316, 115244. https://doi.org/10.1016/j.jenvman.2022.115244

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. / Barbato, Marta; Palma, Enza; Marzocchi, Ugo et al.
In: Journal of Environmental Management, Vol. 316, 115244, 08.2022.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

TY - JOUR

T1 - 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

AU - Barbato, Marta

AU - Palma, Enza

AU - Marzocchi, Ugo

AU - Cruz Viggi, Carolina

AU - Rossetti, Simona

AU - Aulenta, Federico

AU - Scoma, Alberto

PY - 2022/8

Y1 - 2022/8

N2 - 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.

AB - 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.

KW - BES

KW - Crude oil

KW - Deep sea

KW - Metatranscriptomics

KW - Oil spill

KW - Petroleum

KW - sediments

KW - Biodegradation, Environmental

KW - Petroleum Pollution

KW - RNA, Ribosomal, 16S/genetics

KW - Alkanes

KW - Hydrocarbons/metabolism

KW - Hydrostatic Pressure

KW - Acetyl Coenzyme A

KW - Petroleum/metabolism

KW - Geologic Sediments/chemistry

KW - Respiration

UR - https://www.scopus.com/pages/publications/85130834647

U2 - 10.1016/j.jenvman.2022.115244

DO - 10.1016/j.jenvman.2022.115244

M3 - Journal article

C2 - 35598451

SN - 0301-4797

VL - 316

JO - Journal of Environmental Management

JF - Journal of Environmental Management

M1 - 115244

ER -