Physiology of resistant Deinococcus geothermalis bacterium aerobically cultivated in low-manganese medium

Christina Liedert (Corresponding Author), M. Peltola, J. Bernhardt, P. Neubauer, M. Salkinoja-Salonen (Corresponding Author)

Research output: Contribution to journalArticleScientificpeer-review

15 Citations (Scopus)

Abstract

This dynamic proteome study describes the physiology of growth and survival of Deinococcus geothermalis, in conditions simulating paper machine waters being aerobic, warm, and low in carbon and manganese. The industrial environment of this species differs from its natural habitats, geothermal springs and deep ocean subsurfaces, by being highly exposed to oxygen. Quantitative proteome analysis using two-dimensional gel electrophoresis and bioinformatic tools showed expression change for 165 proteins, from which 47 were assigned to a function. We propose that D. geothermalis grew and survived in aerobic conditions by channeling central carbon metabolism to pathways where mainly NADPH rather than NADH was retrieved from the carbon source. A major part of the carbon substrate was converted into succinate, which was not a fermentation product but likely served combating reactive oxygen species (ROS). Transition from growth to nongrowth resulted in downregulation of the oxidative phosphorylation observed as reduced expression of V-type ATPase responsible for ATP synthesis in D. geothermalis. The battle against oxidative stress was seen as upregulation of superoxide dismutase (Mn dependent) and catalase, as well as several protein repair enzymes, including FeS cluster assembly proteins of the iron-sulfur cluster assembly protein system, peptidylprolyl isomerase, and chaperones. Addition of soluble Mn reinitiated respiration and proliferation with concomitant acidification, indicating that aerobic metabolism was restricted by access to manganese. We conclude that D. geothermalis prefers to combat ROS using manganese-dependent enzymes, but when manganese is not available central carbon metabolism is used to produce ROS neutralizing metabolites at the expense of high utilization of carbon substrate.
Original languageEnglish
Pages (from-to)1552-1561
Number of pages10
JournalJournal of Bacteriology
Volume194
Issue number6
DOIs
Publication statusPublished - 2012
MoE publication typeA1 Journal article-refereed

Fingerprint

Deinococcus
Manganese
Carbon
Bacteria
Reactive Oxygen Species
Proteome
Iron-Sulfur Proteins
Hot Springs
Peptidylprolyl Isomerase
Vacuolar Proton-Translocating ATPases
Proteins
Oxidative Phosphorylation
Electrophoresis, Gel, Two-Dimensional
Succinic Acid
Enzymes
Growth
Computational Biology
NADP
Oceans and Seas
NAD

Cite this

Liedert, Christina ; Peltola, M. ; Bernhardt, J. ; Neubauer, P. ; Salkinoja-Salonen, M. / Physiology of resistant Deinococcus geothermalis bacterium aerobically cultivated in low-manganese medium. In: Journal of Bacteriology. 2012 ; Vol. 194, No. 6. pp. 1552-1561.
@article{eaad4312392c42dbbb65f3b7ef5e8dd6,
title = "Physiology of resistant Deinococcus geothermalis bacterium aerobically cultivated in low-manganese medium",
abstract = "This dynamic proteome study describes the physiology of growth and survival of Deinococcus geothermalis, in conditions simulating paper machine waters being aerobic, warm, and low in carbon and manganese. The industrial environment of this species differs from its natural habitats, geothermal springs and deep ocean subsurfaces, by being highly exposed to oxygen. Quantitative proteome analysis using two-dimensional gel electrophoresis and bioinformatic tools showed expression change for 165 proteins, from which 47 were assigned to a function. We propose that D. geothermalis grew and survived in aerobic conditions by channeling central carbon metabolism to pathways where mainly NADPH rather than NADH was retrieved from the carbon source. A major part of the carbon substrate was converted into succinate, which was not a fermentation product but likely served combating reactive oxygen species (ROS). Transition from growth to nongrowth resulted in downregulation of the oxidative phosphorylation observed as reduced expression of V-type ATPase responsible for ATP synthesis in D. geothermalis. The battle against oxidative stress was seen as upregulation of superoxide dismutase (Mn dependent) and catalase, as well as several protein repair enzymes, including FeS cluster assembly proteins of the iron-sulfur cluster assembly protein system, peptidylprolyl isomerase, and chaperones. Addition of soluble Mn reinitiated respiration and proliferation with concomitant acidification, indicating that aerobic metabolism was restricted by access to manganese. We conclude that D. geothermalis prefers to combat ROS using manganese-dependent enzymes, but when manganese is not available central carbon metabolism is used to produce ROS neutralizing metabolites at the expense of high utilization of carbon substrate.",
author = "Christina Liedert and M. Peltola and J. Bernhardt and P. Neubauer and M. Salkinoja-Salonen",
year = "2012",
doi = "10.1128/JB.06429-11",
language = "English",
volume = "194",
pages = "1552--1561",
journal = "Journal of Bacteriology",
issn = "0021-9193",
publisher = "American Society for Microbiology",
number = "6",

}

Physiology of resistant Deinococcus geothermalis bacterium aerobically cultivated in low-manganese medium. / Liedert, Christina (Corresponding Author); Peltola, M.; Bernhardt, J.; Neubauer, P.; Salkinoja-Salonen, M. (Corresponding Author).

In: Journal of Bacteriology, Vol. 194, No. 6, 2012, p. 1552-1561.

Research output: Contribution to journalArticleScientificpeer-review

TY - JOUR

T1 - Physiology of resistant Deinococcus geothermalis bacterium aerobically cultivated in low-manganese medium

AU - Liedert, Christina

AU - Peltola, M.

AU - Bernhardt, J.

AU - Neubauer, P.

AU - Salkinoja-Salonen, M.

PY - 2012

Y1 - 2012

N2 - This dynamic proteome study describes the physiology of growth and survival of Deinococcus geothermalis, in conditions simulating paper machine waters being aerobic, warm, and low in carbon and manganese. The industrial environment of this species differs from its natural habitats, geothermal springs and deep ocean subsurfaces, by being highly exposed to oxygen. Quantitative proteome analysis using two-dimensional gel electrophoresis and bioinformatic tools showed expression change for 165 proteins, from which 47 were assigned to a function. We propose that D. geothermalis grew and survived in aerobic conditions by channeling central carbon metabolism to pathways where mainly NADPH rather than NADH was retrieved from the carbon source. A major part of the carbon substrate was converted into succinate, which was not a fermentation product but likely served combating reactive oxygen species (ROS). Transition from growth to nongrowth resulted in downregulation of the oxidative phosphorylation observed as reduced expression of V-type ATPase responsible for ATP synthesis in D. geothermalis. The battle against oxidative stress was seen as upregulation of superoxide dismutase (Mn dependent) and catalase, as well as several protein repair enzymes, including FeS cluster assembly proteins of the iron-sulfur cluster assembly protein system, peptidylprolyl isomerase, and chaperones. Addition of soluble Mn reinitiated respiration and proliferation with concomitant acidification, indicating that aerobic metabolism was restricted by access to manganese. We conclude that D. geothermalis prefers to combat ROS using manganese-dependent enzymes, but when manganese is not available central carbon metabolism is used to produce ROS neutralizing metabolites at the expense of high utilization of carbon substrate.

AB - This dynamic proteome study describes the physiology of growth and survival of Deinococcus geothermalis, in conditions simulating paper machine waters being aerobic, warm, and low in carbon and manganese. The industrial environment of this species differs from its natural habitats, geothermal springs and deep ocean subsurfaces, by being highly exposed to oxygen. Quantitative proteome analysis using two-dimensional gel electrophoresis and bioinformatic tools showed expression change for 165 proteins, from which 47 were assigned to a function. We propose that D. geothermalis grew and survived in aerobic conditions by channeling central carbon metabolism to pathways where mainly NADPH rather than NADH was retrieved from the carbon source. A major part of the carbon substrate was converted into succinate, which was not a fermentation product but likely served combating reactive oxygen species (ROS). Transition from growth to nongrowth resulted in downregulation of the oxidative phosphorylation observed as reduced expression of V-type ATPase responsible for ATP synthesis in D. geothermalis. The battle against oxidative stress was seen as upregulation of superoxide dismutase (Mn dependent) and catalase, as well as several protein repair enzymes, including FeS cluster assembly proteins of the iron-sulfur cluster assembly protein system, peptidylprolyl isomerase, and chaperones. Addition of soluble Mn reinitiated respiration and proliferation with concomitant acidification, indicating that aerobic metabolism was restricted by access to manganese. We conclude that D. geothermalis prefers to combat ROS using manganese-dependent enzymes, but when manganese is not available central carbon metabolism is used to produce ROS neutralizing metabolites at the expense of high utilization of carbon substrate.

U2 - 10.1128/JB.06429-11

DO - 10.1128/JB.06429-11

M3 - Article

VL - 194

SP - 1552

EP - 1561

JO - Journal of Bacteriology

JF - Journal of Bacteriology

SN - 0021-9193

IS - 6

ER -