cThis 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.
Deinococcus geothermalis belongs to the deeply branched bacterial phylum Deinococcus-Thermus (19), which is known for its extremophilic species. D. geothermalis and D. radiodurans are extremely resistance against infrared (IR) and UV radiation and desiccation (12,42). D. geothermalis was first described as an aerobic bacterium found in geothermal springs (17) and later in deep-ocean subsurfaces (34), showing that it can grow in the absence of oxygen. D. geothermalis is able to reduce Fe(III), U(VI), and Cr(VI) and was genetically modified to reduce Hg(II) at elevated temperatures (7). These characteristics make the species a potential candidate for biotechnical applications such as the remediation of nuclear waste lands. The members of the Deinococcus family are also screened for biofuel, green chemistry, and antibiotics production purposes.D. geothermalis has found an industrial niche in paper industry, where it forms biofilms on warm air-exposed splash surfaces (33,35,44,45,58), showing that this species is able to fight oxidative stress caused by aerobic lifestyle and by oxidizing biocides. The genome of D. geothermalis was sequenced (42), but it did not reveal unique defense systems which could be responsible for the extr...