Bacterial use of choline to tolerate salinity shifts in sea-ice brines

E. Firth, S. D. Carpenter, H. L. Sørensen, R. E. Collins, J. W. Deming

Research output: Contribution to journalJournal articleResearchpeer-review

78 Downloads (Pure)

Abstract

Bacteria within the brine network of sea ice experience temperature-driven fluctuations in salinity on both short and long temporal scales, yet their means of osmoprotection against such fluctuations is poorly understood. One mechanism used to withstand the ion fluxes caused by salinity shifts, well-known in mesophilic bacteria, is the import and export of low molecular weight organic solutes that are compatible with intracellular functions. Working with the marine psychrophilic gammaproteobacterium, Colwellia psychrerythraea 34H, and with natural microbial assemblages present in sackhole brines drained from sea ice in Kanajorsuit Bay (2013) and Kobbefjord (2014), Greenland, we measured the utilization of 14C-choline (precursor to glycine betaine, a common compatible solute) at -1°C upon salinity shifts to double and to half the starting salinity. In all cases and across a range of starting salinities, when salinity was increased, 14C-solute (choline or derivatives) was preferentially retained as an intracellular osmolyte; when salinity was decreased, 14C-choline was preferentially respired to 14CO 2. Additional experiments with cold-adapted bacteria in culture indicated that an abrupt downshift in salinity prompted rapid (subsecond) expulsion of retained 14C-solute, but that uptake of 14C-choline and solute retention resumed when salinity was returned to starting value. Overall, the results indicate that bacteria in sea-ice brines use compatible solutes for osmoprotection, transporting, storing and cycling these molecules as needed to withstand naturally occurring salinity shifts and persist through the seasons. Because choline and many commonly used compatible solutes contain nitrogen, we suggest that when brines freshen and bacteria respire such compatible solutes, the corresponding regeneration of ammonium may enhance specific biogeochemical processes in the ice, possibly algal productivity but particularly nitrification. Measurements of potential nitrification rates in parallel sea-ice samples are consistent with a link between use of the compatible solute strategy and nitrification.

Original languageEnglish
Article number000120
JournalElementa: Science of the Anthropocene
Volume4
Number of pages15
ISSN2325-1026
DOIs
Publication statusPublished - 2016

Fingerprint

Brines
Sea ice
sea ice
Bacteria
solute
Nitrification
salinity
bacterium
Betaines
nitrification
Ice
Amino acids
Productivity
Molecular weight
Choline
Fluxes
Nitrogen
Derivatives
Molecules
Ions

Cite this

Firth, E., Carpenter, S. D., Sørensen, H. L., Collins, R. E., & Deming, J. W. (2016). Bacterial use of choline to tolerate salinity shifts in sea-ice brines. Elementa: Science of the Anthropocene, 4, [000120]. https://doi.org/10.12952/journal.elementa.000120
Firth, E. ; Carpenter, S. D. ; Sørensen, H. L. ; Collins, R. E. ; Deming, J. W. / Bacterial use of choline to tolerate salinity shifts in sea-ice brines. In: Elementa: Science of the Anthropocene. 2016 ; Vol. 4.
@article{a3fd3361d4b047fa881e08aaa0b47142,
title = "Bacterial use of choline to tolerate salinity shifts in sea-ice brines",
abstract = "Bacteria within the brine network of sea ice experience temperature-driven fluctuations in salinity on both short and long temporal scales, yet their means of osmoprotection against such fluctuations is poorly understood. One mechanism used to withstand the ion fluxes caused by salinity shifts, well-known in mesophilic bacteria, is the import and export of low molecular weight organic solutes that are compatible with intracellular functions. Working with the marine psychrophilic gammaproteobacterium, Colwellia psychrerythraea 34H, and with natural microbial assemblages present in sackhole brines drained from sea ice in Kanajorsuit Bay (2013) and Kobbefjord (2014), Greenland, we measured the utilization of 14C-choline (precursor to glycine betaine, a common compatible solute) at -1°C upon salinity shifts to double and to half the starting salinity. In all cases and across a range of starting salinities, when salinity was increased, 14C-solute (choline or derivatives) was preferentially retained as an intracellular osmolyte; when salinity was decreased, 14C-choline was preferentially respired to 14CO 2. Additional experiments with cold-adapted bacteria in culture indicated that an abrupt downshift in salinity prompted rapid (subsecond) expulsion of retained 14C-solute, but that uptake of 14C-choline and solute retention resumed when salinity was returned to starting value. Overall, the results indicate that bacteria in sea-ice brines use compatible solutes for osmoprotection, transporting, storing and cycling these molecules as needed to withstand naturally occurring salinity shifts and persist through the seasons. Because choline and many commonly used compatible solutes contain nitrogen, we suggest that when brines freshen and bacteria respire such compatible solutes, the corresponding regeneration of ammonium may enhance specific biogeochemical processes in the ice, possibly algal productivity but particularly nitrification. Measurements of potential nitrification rates in parallel sea-ice samples are consistent with a link between use of the compatible solute strategy and nitrification.",
author = "E. Firth and Carpenter, {S. D.} and S{\o}rensen, {H. L.} and Collins, {R. E.} and Deming, {J. W.}",
year = "2016",
doi = "10.12952/journal.elementa.000120",
language = "English",
volume = "4",
journal = "Elementa: Science of the Anthropocene",
issn = "2325-1026",
publisher = "BioOne",

}

Bacterial use of choline to tolerate salinity shifts in sea-ice brines. / Firth, E.; Carpenter, S. D.; Sørensen, H. L.; Collins, R. E.; Deming, J. W.

In: Elementa: Science of the Anthropocene, Vol. 4, 000120, 2016.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Bacterial use of choline to tolerate salinity shifts in sea-ice brines

AU - Firth, E.

AU - Carpenter, S. D.

AU - Sørensen, H. L.

AU - Collins, R. E.

AU - Deming, J. W.

PY - 2016

Y1 - 2016

N2 - Bacteria within the brine network of sea ice experience temperature-driven fluctuations in salinity on both short and long temporal scales, yet their means of osmoprotection against such fluctuations is poorly understood. One mechanism used to withstand the ion fluxes caused by salinity shifts, well-known in mesophilic bacteria, is the import and export of low molecular weight organic solutes that are compatible with intracellular functions. Working with the marine psychrophilic gammaproteobacterium, Colwellia psychrerythraea 34H, and with natural microbial assemblages present in sackhole brines drained from sea ice in Kanajorsuit Bay (2013) and Kobbefjord (2014), Greenland, we measured the utilization of 14C-choline (precursor to glycine betaine, a common compatible solute) at -1°C upon salinity shifts to double and to half the starting salinity. In all cases and across a range of starting salinities, when salinity was increased, 14C-solute (choline or derivatives) was preferentially retained as an intracellular osmolyte; when salinity was decreased, 14C-choline was preferentially respired to 14CO 2. Additional experiments with cold-adapted bacteria in culture indicated that an abrupt downshift in salinity prompted rapid (subsecond) expulsion of retained 14C-solute, but that uptake of 14C-choline and solute retention resumed when salinity was returned to starting value. Overall, the results indicate that bacteria in sea-ice brines use compatible solutes for osmoprotection, transporting, storing and cycling these molecules as needed to withstand naturally occurring salinity shifts and persist through the seasons. Because choline and many commonly used compatible solutes contain nitrogen, we suggest that when brines freshen and bacteria respire such compatible solutes, the corresponding regeneration of ammonium may enhance specific biogeochemical processes in the ice, possibly algal productivity but particularly nitrification. Measurements of potential nitrification rates in parallel sea-ice samples are consistent with a link between use of the compatible solute strategy and nitrification.

AB - Bacteria within the brine network of sea ice experience temperature-driven fluctuations in salinity on both short and long temporal scales, yet their means of osmoprotection against such fluctuations is poorly understood. One mechanism used to withstand the ion fluxes caused by salinity shifts, well-known in mesophilic bacteria, is the import and export of low molecular weight organic solutes that are compatible with intracellular functions. Working with the marine psychrophilic gammaproteobacterium, Colwellia psychrerythraea 34H, and with natural microbial assemblages present in sackhole brines drained from sea ice in Kanajorsuit Bay (2013) and Kobbefjord (2014), Greenland, we measured the utilization of 14C-choline (precursor to glycine betaine, a common compatible solute) at -1°C upon salinity shifts to double and to half the starting salinity. In all cases and across a range of starting salinities, when salinity was increased, 14C-solute (choline or derivatives) was preferentially retained as an intracellular osmolyte; when salinity was decreased, 14C-choline was preferentially respired to 14CO 2. Additional experiments with cold-adapted bacteria in culture indicated that an abrupt downshift in salinity prompted rapid (subsecond) expulsion of retained 14C-solute, but that uptake of 14C-choline and solute retention resumed when salinity was returned to starting value. Overall, the results indicate that bacteria in sea-ice brines use compatible solutes for osmoprotection, transporting, storing and cycling these molecules as needed to withstand naturally occurring salinity shifts and persist through the seasons. Because choline and many commonly used compatible solutes contain nitrogen, we suggest that when brines freshen and bacteria respire such compatible solutes, the corresponding regeneration of ammonium may enhance specific biogeochemical processes in the ice, possibly algal productivity but particularly nitrification. Measurements of potential nitrification rates in parallel sea-ice samples are consistent with a link between use of the compatible solute strategy and nitrification.

U2 - 10.12952/journal.elementa.000120

DO - 10.12952/journal.elementa.000120

M3 - Journal article

VL - 4

JO - Elementa: Science of the Anthropocene

JF - Elementa: Science of the Anthropocene

SN - 2325-1026

M1 - 000120

ER -