The effect of hydrostatic pressure on the activity and community composition of hydrocarbon-degrading bacteria in Arctic seawater

Angeliki Marietou; Jennie Spicker Schmidt; Martin R Rasmussen; Alberto Scoma; Søren Rysgaard; Leendert Vergeynst

doi:10.1128/aem.00987-23

The effect of hydrostatic pressure on the activity and community composition of hydrocarbon-degrading bacteria in Arctic seawater

Angeliki Marietou, Jennie Spicker Schmidt, Martin R Rasmussen, Alberto Scoma, Søren Rysgaard, Leendert Vergeynst

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

Abstract

There is a renewed interest in hydrocarbon biodegradation in Arctic seawaters due to increasing ship traffic and risk for oil spills. Most studies, however, fail to address the effect of increasing pressure as an environmental parameter. Here, we conducted a series of pressurized enrichments (0.1–30 MPa, 4°C) inoculated with a 100-day-old hydrocarbon-degrading biofilm collected from 615 m deep in Arctic seawater. Cell-specific CO₂ production rates provided a clear summary of the observed microbial activity: a bloom of a hydrocarbon degrading-biofilm generating 0.82–0.90 fmol CO₂⋅bacterial gene⁻¹⋅day⁻¹ at 0.1–8 MPa, but undetectable activity at 30 MPa until day 6. At 30 MPa, the microbial activity increased between days 6 and 34 with an average rate of 0.36 ± 0.08 fmol CO₂⋅bacterial gene⁻¹⋅day⁻¹. Amplicon sequencing revealed no differences in the microbial community composition at 0.1–12 MPa. While the typical Arctic alkane degraders Oleispira and Shewanella were abundant across all hydrostatic pressures and over time, Colwellia, Neptunomonas, and Kiloniella were significantly enriched solely at 30 MPa. Our results suggest that the physiological adaptations of psychrophilic bacteria to thrive at sub-zero temperature make Arctic oil degraders tolerant to mild hydrostatic pressures of up to 12 MPa, whereas temperate climate communities have shown hydrostatic pressure-induced inhibition at 10–15 MPa in comparable studies. The activity of hydrocarbon degraders in sinking marine oil snow in the Arctic may remain unaffected down to depths of about 1,200 m, after which hydrostatic pressure can significantly affect hydrocarbon degradation at increasing depths down to 3,000 m.

Originalsprog	Engelsk
Artikelnummer	e0098723
Tidsskrift	Applied and Environmental Microbiology
Vol/bind	89
Nummer	11
Antal sider	17
ISSN	0099-2240
DOI	https://doi.org/10.1128/aem.00987-23
Status	Udgivet - nov. 2023

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10.1128/aem.00987-23

https://pmc.ncbi.nlm.nih.gov/articles/PMC10686064/pdf/aem.00987-23.pdfLicens: Ikke-specificeret

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title = "The effect of hydrostatic pressure on the activity and community composition of hydrocarbon-degrading bacteria in Arctic seawater",

abstract = "There is a renewed interest in hydrocarbon biodegradation in Arctic seawaters due to increasing ship traffic and risk for oil spills. Most studies, however, fail to address the effect of increasing pressure as an environmental parameter. Here, we conducted a series of pressurized enrichments (0.1–30 MPa, 4°C) inoculated with a 100-day-old hydrocarbon-degrading biofilm collected from 615 m deep in Arctic seawater. Cell-specific CO2 production rates provided a clear summary of the observed microbial activity: a bloom of a hydrocarbon degrading-biofilm generating 0.82–0.90 fmol CO2⋅bacterial gene−1⋅day−1 at 0.1–8 MPa, but undetectable activity at 30 MPa until day 6. At 30 MPa, the microbial activity increased between days 6 and 34 with an average rate of 0.36 ± 0.08 fmol CO2⋅bacterial gene−1⋅day−1. Amplicon sequencing revealed no differences in the microbial community composition at 0.1–12 MPa. While the typical Arctic alkane degraders Oleispira and Shewanella were abundant across all hydrostatic pressures and over time, Colwellia, Neptunomonas, and Kiloniella were significantly enriched solely at 30 MPa. Our results suggest that the physiological adaptations of psychrophilic bacteria to thrive at sub-zero temperature make Arctic oil degraders tolerant to mild hydrostatic pressures of up to 12 MPa, whereas temperate climate communities have shown hydrostatic pressure-induced inhibition at 10–15 MPa in comparable studies. The activity of hydrocarbon degraders in sinking marine oil snow in the Arctic may remain unaffected down to depths of about 1,200 m, after which hydrostatic pressure can significantly affect hydrocarbon degradation at increasing depths down to 3,000 m.",

keywords = "Arctic, hydrocarbon biodegradation, hydrostatic pressure, microbial community, psychrophilic bacteria, Biodegradation, Environmental, Petroleum Pollution, Water Pollutants, Chemical, Hydrocarbons, Hydrostatic Pressure, Petroleum, Arctic Regions, Bacteria, Seawater/microbiology",

author = "Angeliki Marietou and Schmidt, {Jennie Spicker} and Rasmussen, {Martin R} and Alberto Scoma and S{\o}ren Rysgaard and Leendert Vergeynst",

year = "2023",

month = nov,

doi = "10.1128/aem.00987-23",

language = "English",

volume = "89",

journal = "Applied and Environmental Microbiology",

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publisher = "American Society for Microbiology",

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The effect of hydrostatic pressure on the activity and community composition of hydrocarbon-degrading bacteria in Arctic seawater. / Marietou, Angeliki ; Schmidt, Jennie Spicker ; Rasmussen, Martin R et al.
I: Applied and Environmental Microbiology, Bind 89, Nr. 11, e0098723, 11.2023.

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

TY - JOUR

T1 - The effect of hydrostatic pressure on the activity and community composition of hydrocarbon-degrading bacteria in Arctic seawater

AU - Marietou, Angeliki

AU - Schmidt, Jennie Spicker

AU - Rasmussen, Martin R

AU - Scoma, Alberto

AU - Rysgaard, Søren

AU - Vergeynst, Leendert

PY - 2023/11

Y1 - 2023/11

N2 - There is a renewed interest in hydrocarbon biodegradation in Arctic seawaters due to increasing ship traffic and risk for oil spills. Most studies, however, fail to address the effect of increasing pressure as an environmental parameter. Here, we conducted a series of pressurized enrichments (0.1–30 MPa, 4°C) inoculated with a 100-day-old hydrocarbon-degrading biofilm collected from 615 m deep in Arctic seawater. Cell-specific CO2 production rates provided a clear summary of the observed microbial activity: a bloom of a hydrocarbon degrading-biofilm generating 0.82–0.90 fmol CO2⋅bacterial gene−1⋅day−1 at 0.1–8 MPa, but undetectable activity at 30 MPa until day 6. At 30 MPa, the microbial activity increased between days 6 and 34 with an average rate of 0.36 ± 0.08 fmol CO2⋅bacterial gene−1⋅day−1. Amplicon sequencing revealed no differences in the microbial community composition at 0.1–12 MPa. While the typical Arctic alkane degraders Oleispira and Shewanella were abundant across all hydrostatic pressures and over time, Colwellia, Neptunomonas, and Kiloniella were significantly enriched solely at 30 MPa. Our results suggest that the physiological adaptations of psychrophilic bacteria to thrive at sub-zero temperature make Arctic oil degraders tolerant to mild hydrostatic pressures of up to 12 MPa, whereas temperate climate communities have shown hydrostatic pressure-induced inhibition at 10–15 MPa in comparable studies. The activity of hydrocarbon degraders in sinking marine oil snow in the Arctic may remain unaffected down to depths of about 1,200 m, after which hydrostatic pressure can significantly affect hydrocarbon degradation at increasing depths down to 3,000 m.

AB - There is a renewed interest in hydrocarbon biodegradation in Arctic seawaters due to increasing ship traffic and risk for oil spills. Most studies, however, fail to address the effect of increasing pressure as an environmental parameter. Here, we conducted a series of pressurized enrichments (0.1–30 MPa, 4°C) inoculated with a 100-day-old hydrocarbon-degrading biofilm collected from 615 m deep in Arctic seawater. Cell-specific CO2 production rates provided a clear summary of the observed microbial activity: a bloom of a hydrocarbon degrading-biofilm generating 0.82–0.90 fmol CO2⋅bacterial gene−1⋅day−1 at 0.1–8 MPa, but undetectable activity at 30 MPa until day 6. At 30 MPa, the microbial activity increased between days 6 and 34 with an average rate of 0.36 ± 0.08 fmol CO2⋅bacterial gene−1⋅day−1. Amplicon sequencing revealed no differences in the microbial community composition at 0.1–12 MPa. While the typical Arctic alkane degraders Oleispira and Shewanella were abundant across all hydrostatic pressures and over time, Colwellia, Neptunomonas, and Kiloniella were significantly enriched solely at 30 MPa. Our results suggest that the physiological adaptations of psychrophilic bacteria to thrive at sub-zero temperature make Arctic oil degraders tolerant to mild hydrostatic pressures of up to 12 MPa, whereas temperate climate communities have shown hydrostatic pressure-induced inhibition at 10–15 MPa in comparable studies. The activity of hydrocarbon degraders in sinking marine oil snow in the Arctic may remain unaffected down to depths of about 1,200 m, after which hydrostatic pressure can significantly affect hydrocarbon degradation at increasing depths down to 3,000 m.

KW - Arctic

KW - hydrocarbon biodegradation

KW - hydrostatic pressure

KW - microbial community

KW - psychrophilic bacteria

KW - Biodegradation, Environmental

KW - Petroleum Pollution

KW - Water Pollutants, Chemical

KW - Hydrocarbons

KW - Hydrostatic Pressure

KW - Petroleum

KW - Arctic Regions

KW - Bacteria

KW - Seawater/microbiology

U2 - 10.1128/aem.00987-23

DO - 10.1128/aem.00987-23

M3 - Journal article

C2 - 37943057

SN - 0099-2240

VL - 89

JO - Applied and Environmental Microbiology

JF - Applied and Environmental Microbiology

IS - 11

M1 - e0098723

ER -

The effect of hydrostatic pressure on the activity and community composition of hydrocarbon-degrading bacteria in Arctic seawater

Abstract

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