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Osmotic stress confers enhanced cell integrity to hydrostatic pressure but impairs growth in Alcanivorax borkumensis SK2

Alberto Scoma and Nico Boon UGent (2016) FRONTIERS IN MICROBIOLOGY. 7.
abstract
Alcanivorax is a hydrocarbonoclastic genus dominating oil spills worldwide. While its presence has been detected in oil-polluted seawaters, marine sediment and salt marshes under ambient pressure, its presence in deep-sea oil-contaminated environments is negligible. Recent laboratory studies highlighted the piezosensitive nature of some Alcanivorax species, whose growth yields are highly impacted by mild hydrostatic pressures (HPs). In the present study, osmotic stress was used as a tool to increase HP resistance in the type strain Alcanivorax borkumensis SK2. Control cultures grown under standard conditions of salinity and osmotic pressure with respect to seawater (35.6 ppt or 1136 mOsm kg(-1), respectively) were compared with cultures subjected to hypo- and hyperosmosis (330 and 1720 mOsm kg(-1), or 18 and 62 ppt in salinity, equivalent to brackish and brine waters, respectively), under atmospheric or increased HP (0.1 and 10 MPa). Osmotic stress had a remarkably positive impact on cell metabolic activity in terms of CO2 production (thus, oil bioremediation) and O-2 respiration under hyperosmosis, as acclimation to high salinity enhanced cell activity under 10 MPa by a factor of 10. Both osmotic shocks significantly enhanced cell protection by reducing membrane damage under HP, with cell integrities close to 100% under hyposmosis. The latter was likely due to intracellular water-reclamation as no trace of the piezolyte ectoine was found, contrary to hyperosmosis. Notably, ectoine production was equivalent at 0.1 MPa in hyperosmosis-acclimated cells and at 10 MPa under isosmotic conditions. While stimulating cell metabolism and enhancing cell integrity, osmotic stress had always a negative impact on culture growth and performance. No net growth was observed during 4-days incubation tests, and CO2:O-2 ratios and pH values indicated that culture performance in terms of hydrocarbon degradation was lowered by the effects of osmotic stress alone or combined with increased HP. These findings confirm the piezosensitive nature of A. borkumensis, which lacks proper resistance mechanisms to improve its metabolic efficiency under increased HP, thus explaining its limited role in oil-polluted deep-sea environments.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
piezolyte, osmolyte, hydrocarbons, oil, deep-sea, ectoine, Halomonas, petroleum, DEEP-WATER-HORIZON, COMPATIBLE SOLUTE ECTOINE, GULF-OF-MEXICO, OIL-SPILL, ESCHERICHIA-COLI, HALOMONAS-ELONGATA, BREVIBACTERIUM-EPIDERMIS, HALOPHILIC EUBACTERIA, DEGRADING BACTERIA, MODERATE HALOPHILE
journal title
FRONTIERS IN MICROBIOLOGY
Front. Microbiol.
volume
7
article number
729
pages
11 pages
Web of Science type
Article
Web of Science id
000376002100001
JCR category
MICROBIOLOGY
JCR impact factor
4.076 (2016)
JCR rank
25/124 (2016)
JCR quartile
1 (2016)
ISSN
1664-302X
DOI
10.3389/fmicb.2016.00729
project
41M08912W
language
English
UGent publication?
yes
classification
A1
copyright statement
I have retained and own the full copyright for this publication
id
8023252
handle
http://hdl.handle.net/1854/LU-8023252
date created
2016-07-01 14:42:04
date last changed
2017-05-10 13:05:13
@article{8023252,
  abstract     = {Alcanivorax is a hydrocarbonoclastic genus dominating oil spills worldwide. While its presence has been detected in oil-polluted seawaters, marine sediment and salt marshes under ambient pressure, its presence in deep-sea oil-contaminated environments is negligible. Recent laboratory studies highlighted the piezosensitive nature of some Alcanivorax species, whose growth yields are highly impacted by mild hydrostatic pressures (HPs). In the present study, osmotic stress was used as a tool to increase HP resistance in the type strain Alcanivorax borkumensis SK2. Control cultures grown under standard conditions of salinity and osmotic pressure with respect to seawater (35.6 ppt or 1136 mOsm kg(-1), respectively) were compared with cultures subjected to hypo- and hyperosmosis (330 and 1720 mOsm kg(-1), or 18 and 62 ppt in salinity, equivalent to brackish and brine waters, respectively), under atmospheric or increased HP (0.1 and 10 MPa). Osmotic stress had a remarkably positive impact on cell metabolic activity in terms of CO2 production (thus, oil bioremediation) and O-2 respiration under hyperosmosis, as acclimation to high salinity enhanced cell activity under 10 MPa by a factor of 10. Both osmotic shocks significantly enhanced cell protection by reducing membrane damage under HP, with cell integrities close to 100\% under hyposmosis. The latter was likely due to intracellular water-reclamation as no trace of the piezolyte ectoine was found, contrary to hyperosmosis. Notably, ectoine production was equivalent at 0.1 MPa in hyperosmosis-acclimated cells and at 10 MPa under isosmotic conditions. While stimulating cell metabolism and enhancing cell integrity, osmotic stress had always a negative impact on culture growth and performance. No net growth was observed during 4-days incubation tests, and CO2:O-2 ratios and pH values indicated that culture performance in terms of hydrocarbon degradation was lowered by the effects of osmotic stress alone or combined with increased HP. These findings confirm the piezosensitive nature of A. borkumensis, which lacks proper resistance mechanisms to improve its metabolic efficiency under increased HP, thus explaining its limited role in oil-polluted deep-sea environments.},
  articleno    = {729},
  author       = {Scoma, Alberto and Boon, Nico},
  issn         = {1664-302X},
  journal      = {FRONTIERS IN MICROBIOLOGY},
  keyword      = {piezolyte,osmolyte,hydrocarbons,oil,deep-sea,ectoine,Halomonas,petroleum,DEEP-WATER-HORIZON,COMPATIBLE SOLUTE ECTOINE,GULF-OF-MEXICO,OIL-SPILL,ESCHERICHIA-COLI,HALOMONAS-ELONGATA,BREVIBACTERIUM-EPIDERMIS,HALOPHILIC EUBACTERIA,DEGRADING BACTERIA,MODERATE HALOPHILE},
  language     = {eng},
  pages        = {11},
  title        = {Osmotic stress confers enhanced cell integrity to hydrostatic pressure but impairs growth in Alcanivorax borkumensis SK2},
  url          = {http://dx.doi.org/10.3389/fmicb.2016.00729},
  volume       = {7},
  year         = {2016},
}

Chicago
Scoma, Alberto, and Nico Boon. 2016. “Osmotic Stress Confers Enhanced Cell Integrity to Hydrostatic Pressure but Impairs Growth in Alcanivorax Borkumensis SK2.” Frontiers in Microbiology 7.
APA
Scoma, A., & Boon, N. (2016). Osmotic stress confers enhanced cell integrity to hydrostatic pressure but impairs growth in Alcanivorax borkumensis SK2. FRONTIERS IN MICROBIOLOGY, 7.
Vancouver
1.
Scoma A, Boon N. Osmotic stress confers enhanced cell integrity to hydrostatic pressure but impairs growth in Alcanivorax borkumensis SK2. FRONTIERS IN MICROBIOLOGY. 2016;7.
MLA
Scoma, Alberto, and Nico Boon. “Osmotic Stress Confers Enhanced Cell Integrity to Hydrostatic Pressure but Impairs Growth in Alcanivorax Borkumensis SK2.” FRONTIERS IN MICROBIOLOGY 7 (2016): n. pag. Print.