Metabolic network modeling of redox balancing and biohydrogen production in purple nonsulfur bacteria

Hädicke, Oliver; Grammel, Hartmut; Klamt, Steffen

doi:10.1186/1752-0509-5-150

Cited by 81 publications

(59 citation statements)

References 58 publications

(104 reference statements)

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“…A flux balance model predicted that the reverse TCA cycle could substitute for the Calvin cycle in maintaining electron balance in Rs. rubrum (13). Consistent with this possibility, fumarate reductase activity was previously detected in Rs.…”

Section: Figsupporting

confidence: 72%

“…A flux balance model predicted that an Rs. rubrum Calvin cycle mutant could grow photoheterotrophically with malate by producing formate but that formate production would not permit growth with succinate because there would still be excess reducing power (13). However, we did not detect formate in the supernatants of any Rs.…”

Section: Figmentioning

confidence: 41%

“…sphaeroides ⌬RubisCO mutants with acetate and NH 4 ϩ (9). However, the ethylmalonyl-CoA pathway is unlikely to permit photoheterotrophic growth of PNSB Calvin cycle mutants with malate since excessive reducing power would be made en route to the start of the pathway (9,13). Indeed, the Rb.…”

Section: Figmentioning

confidence: 99%

“…First, 13 C metabolic flux and flux balance analyses agree that disrupting Calvin cycle activity should lead to a lethal depletion of oxidized electron carriers or, in other terms, a lethal excess of reducing power (8,10,13,14). Electron balance must be maintained to support metabolic flow and cell viability.…”

mentioning

confidence: 99%

“…palustris), prevented photoheterotrophic growth, even with relatively oxidized substrates, unless an alternative electron acceptor was provided (5-7), or if electrons were disposed of as H 2 (8), or if an alternative reductive CO 2 -fixing pathway was available (9). 13 C-labeling experiments with Rp. palustris have since shown that the Calvin cycle is one of the most active pathways during photoheterotrophic growth, and it oxidizes 40 to 60% of the reducing power even during growth with relatively oxidized substrates (8,10).…”

mentioning

confidence: 99%

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Calvin Cycle Mutants of Photoheterotrophic Purple Nonsulfur Bacteria Fail To Grow Due to an Electron Imbalance Rather than Toxic Metabolite Accumulation

Gordon

McKinlay

2014

J Bacteriol

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Purple nonsulfur bacteria grow photoheterotrophically by using light for energy and organic compounds for carbon and electrons. Disrupting the activity of the CO 2 -fixing Calvin cycle enzyme, ribulose 1,5-bisphosphate carboxylase (RubisCO) However, we also demonstrate that Rs. rubrum and Rp. palustris Calvin cycle phosphoribulokinase mutants that cannot produce RuBP cannot grow photoheterotrophically on succinate unless an electron acceptor is provided or H 2 production is permitted. Thus, the Calvin cycle is still needed to oxidize electron carriers even in the absence of toxic RuBP. Surprisingly, Calvin cycle mutants of Rs. rubrum, but not of Rp. palustris, grew photoheterotrophically on malate without electron acceptors or H 2 production. The mechanism by which Rs. rubrum grows under these conditions remains to be elucidated. P urple nonsulfur bacteria (PNSB) are renowned for their ability to employ versatile metabolic modules to thrive under different growth conditions. PNSB can grow photoautotrophically using light for energy, inorganic compounds other than water (e.g., thiosulfate, Fe 2ϩ ) for electrons, and CO 2 for carbon. The Calvin cycle is well-known for permitting autotrophic growth by converting CO 2 into organic precursors for biosynthesis (Fig. 1). In this pathway phosphoribulokinase (PRK) expends ATP to generate ribulose 1,5-bisphosphate (RuBP). RuBP is then combined with CO 2 via ribulose 1,5-bisphosphate carboxylase (RubisCO), resulting in two molecules of 3-phosphoglycerate. CO 2 fixation generates relatively oxidized metabolites that accept electrons from NAD(P)H via glyceraldehyde-3-phosphate dehydrogenase.,PNSB can also grow photoheterotrophically using light for energy and organic compounds for carbon and electrons. Unlike the process in a respiring heterotroph, reducing power from oxidative pathways [e.g., NAD(P)H] is not used to reduce a terminal electron acceptor and generate ATP by oxidative phosphorylation. Rather, ATP generation is largely decoupled from the oxidative pathways of central metabolism as photoheterotrophs repeatedly energize electrons and shuttle them through a H ϩ -pumping electron transfer chain to generate ATP by cyclic photophosphorylation (Fig. 1). Nevertheless, photoheterotrophs generate ample reducing power that must be oxidized to replenish pools of oxidized electron carriers [e.g., NAD(P) ϩ ] and maintain metabolic flow. CO 2 fixation was first hypothesized to fulfill this essential role of maintaining oxidized electron carriers during photoheterotrophic growth in 1933 by Muller (1), prior to the elucidation of the Calvin cycle itself (2) (Fig. 1, model 1). Muller devised this hypothesis to explain why there was net CO 2 fixation when PNSB grew photoheterotrophically on compounds, like butyrate, that are more electron rich than the average carbon in biomass (1).Supporting this hypothesis, it was later shown that PNSB could be grown photoheterotrophically on butyrate without added CO 2 if an electron acceptor like dimethyl sulfoxide (DMSO) was provided (3) or i...

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Section: Figsupporting

confidence: 72%

Section: Figmentioning

confidence: 41%

Section: Figmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Calvin Cycle Mutants of Photoheterotrophic Purple Nonsulfur Bacteria Fail To Grow Due to an Electron Imbalance Rather than Toxic Metabolite Accumulation

Gordon

McKinlay

2014

J Bacteriol

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Stepwise reduction of the culture redox potential allows the analysis of microaerobic metabolism and photosynthetic membrane synthesis in Rhodospirillum rubrum

Carius

Hädicke

Grammel

2012

Biotech & Bioengineering

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Bacterial growth under oxygen-limited (microaerobic) conditions is often accompanied by phenomena of great interest for fundamental research and industrial application. The microaerobic lifestyle of anoxygenic photosynthetic bacteria like Rhodospirillum rubrum harbors such a phenomenon, as it allows the formation of photosynthetic membranes and related interesting products without light. However, due to the technical difficulties in process control of microaerobic cultivations and the limited sensitivity of available oxygen sensors, the analysis of microaerobic growth and physiology is still underrepresented in current research. The main focus of the present study was to establish an experimental set-up for the systematic study of physiological processes, associated with the growth of R. rubrum under microaerobic conditions in the dark. For this purpose, we introduce a robust and reliable microaerobic process control strategy, which applies the culture redox potential (CRP) for assessing different degrees of oxygen limitation in bioreactor cultivations. To describe the microaerobic growth behavior of R. rubrum cultures for each of these defined CRP reduction steps, basic growth parameters were experimentally determined. Flux variability analysis provided an insight into the metabolic activity of the TCA cycle and implied its connection to the respiratory capacity of the cells. In this context, our results suggest that microaerobic growth of R. rubrum can be described as an oxygen-activated cooperative mechanism. The present study thus contributes to the investigation of metabolic and regulatory events responsible for the redox-sensitive formation of photosynthetic membranes in facultative photosynthetic bacteria. Furthermore, the introduced microaerobic cultivation setup should be generally applicable for any microbial system of interest which can be cultivated in common stirred-tank bioreactors.

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Application of Nanotechnology in the Production of Biohydrogen: A Review

2021

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Hydrogen is an outstanding source of energy that does not create any hostile carbon footprint as it produces only water during combustion. The application of nanotechnology is one of the recent advanced technologies used to enhance the rate of hydrogen production from biomass. The use of nanoparticles (NPs) in the conversion process enhances this rate. Biological methods such as dark fermentation and photobiological route of conversion of biomass to hydrogen are the most suitable and cost‐effective paths. Hydrogen production with nanotechnology in dark fermentation utilizes organic or inorganic NPs in the bioreactor membrane. The efficiency of biohydrogen production depends on the concentration and nature of the NPs used, and the kind of biowastes or biomass feed. The effectiveness of both processes is discussed.

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Metabolic network modeling of redox balancing and biohydrogen production in purple nonsulfur bacteria

Cited by 81 publications

References 58 publications

Calvin Cycle Mutants of Photoheterotrophic Purple Nonsulfur Bacteria Fail To Grow Due to an Electron Imbalance Rather than Toxic Metabolite Accumulation

Calvin Cycle Mutants of Photoheterotrophic Purple Nonsulfur Bacteria Fail To Grow Due to an Electron Imbalance Rather than Toxic Metabolite Accumulation

Stepwise reduction of the culture redox potential allows the analysis of microaerobic metabolism and photosynthetic membrane synthesis in Rhodospirillum rubrum

Application of Nanotechnology in the Production of Biohydrogen: A Review

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