Novel phenazine crystals enable direct electron transfer to methanogens in anaerobic digestion by redox potential modulation

Beckmann, Sabrina; Welte, Cornelia U.; Li, Xiaomin; Yee, Mon Oo; Kroeninger, Lena; Heo, Yooun; Zhang, Miaomiao; Ribeiro, Daniela; Lee, Matthew; Bhadbhade, Mohan; Marjo, Christopher E.; Seidel, Jan; Deppenmeier, Uwe; Manefield, Mike

doi:10.1039/c5ee03085d

Cited by 75 publications

(32 citation statements)

References 34 publications

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“…The effect of external compounds on the redox potential affecting methanogenesis was reported before. According to Beckmann et al (2016), synthetic phenazine neutral red crystals stimulate methanogenesis by transferring electrons to membrane bound proteins of methanogens. On the other hand, the soluble form of phenazine neutral red has a lower potential for reduction (444 mV lower) when compared with the crystal form and had no effect on methane production (Beckmann et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Carbon nanotubes accelerate methane production in pure cultures of methanogens and in a syntrophic coculture

Salvador

Martins

Melle‐Franco

et al. 2017

Environmental Microbiology

131

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Carbon materials have been reported to facilitate direct interspecies electron transfer (DIET) between bacteria and methanogens improving methane production in anaerobic processes. In this work, the effect of increasing concentrations of carbon nanotubes (CNT) on the activity of pure cultures of methanogens and on typical fatty acid-degrading syntrophic methanogenic coculture was evaluated. CNT affected methane production by methanogenic cultures, although acceleration was higher for hydrogenotrophic methanogens than for acetoclastic methanogens or syntrophic coculture. Interestingly, the initial methane production rate (IMPR) by Methanobacterium formicicum cultures increased 17 times with 5 g·L CNT. Butyrate conversion to methane by Syntrophomonas wolfei and Methanospirillum hungatei was enhanced (∼1.5 times) in the presence of CNT (5 g·L ), but indications of DIET were not obtained. Increasing CNT concentrations resulted in more negative redox potentials in the anaerobic microcosms. Remarkably, without a reducing agent but in the presence of CNT, the IMPR was higher than in incubations with reducing agent. No growth was observed without reducing agent and without CNT. This finding is important to re-frame discussions and re-interpret data on the role of conductive materials as mediators of DIET in anaerobic communities. It also opens new challenges to improve methane production in engineered methanogenic processes.

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Section: Discussionmentioning

confidence: 99%

Carbon nanotubes accelerate methane production in pure cultures of methanogens and in a syntrophic coculture

Salvador

Martins

Melle‐Franco

et al. 2017

Environmental Microbiology

131

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“…6a). Recent reports also show that the addition of phenol red and phenazines to anaerobic digesters and microbial fuel cells does in fact increase the growth of Methanosarcina species, demonstrating that this phenomenon is generally relevant to biotechnology (46).…”

Section: Resultsmentioning

confidence: 93%

Physiological Evidence for Isopotential Tunneling in the Electron Transport Chain of Methane-Producing Archaea

Duszenko

Buan

2017

Appl Environ Microbiol

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Many, but not all, organisms use quinones to conserve energy in their electron transport chains. Fermentative bacteria and methane-producing archaea (methanogens) do not produce quinones but have devised other ways to generate ATP. Methanophenazine (MPh) is a unique membrane electron carrier found in Methanosarcina species that plays the same role as quinones in the electron transport chain. To extend the analogy between quinones and MPh, we compared the MPh pool sizes between two well-studied Methanosarcina species, Methanosarcina acetivorans C2A and Methanosarcina barkeri Fusaro, to the quinone pool size in the bacterium Escherichia coli. We found the quantity of MPh per cell increases as cultures transition from exponential growth to stationary phase, and absolute quantities of MPh were 3-fold higher in M. acetivorans than in M. barkeri. The concentration of MPh suggests the cell membrane of M. acetivorans, but not of M. barkeri, is electrically quantized as if it were a single conductive metal sheet and near optimal for rate of electron transport. Similarly, stationary (but not exponentially growing) E. coli cells also have electrically quantized membranes on the basis of quinone content. Consistent with our hypothesis, we demonstrated that the exogenous addition of phenazine increases the growth rate of M. barkeri three times that of M. acetivorans. Our work suggests electron flux through MPh is naturally higher in M. acetivorans than in M. barkeri and that hydrogen cycling is less efficient at conserving energy than scalar proton translocation using MPh.IMPORTANCE Can we grow more from less? The ability to optimize and manipulate metabolic efficiency in cells is the difference between commercially viable and nonviable renewable technologies. Much can be learned from methane-producing archaea (methanogens) which evolved a successful metabolic lifestyle under extreme thermodynamic constraints. Methanogens use highly efficient electron transport systems and supramolecular complexes to optimize electron and carbon flow to control biomass synthesis and the production of methane. Worldwide, methanogens are used to generate renewable methane for heat, electricity, and transportation. Our observations suggest Methanosarcina acetivorans, but not Methanosarcina barkeri, has electrically quantized membranes. Escherichia coli, a model facultative anaerobe, has optimal electron transport at the stationary phase but not during exponential growth. This study also suggests the metabolic efficiency of bacteria and archaea can be improved using exogenously supplied lipophilic electron carriers. The enhancement of methanogen electron transport through methanophenazine has the potential to increase renewable methane production at an industrial scale.

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“…Literature emphasizes the role of Methanosarcina in methane production in the presence of acetate. Acetate can be converted into CH 4 via methyl‐H 4 SPT and via methyl‐S‐Com, in which CO 2 is finally released from the carboxylic group . The reduction of carbon dioxide, which comes from the oxidation of acetate to methane, leads to methane avoiding or not the production of hydrogen as an intermediate step .…”

Section: Resultsmentioning

confidence: 99%

Effect of sludge age on microbial consortia developed in MFCs

Mateo

Zamorano-López

Borrás

et al. 2017

J of Chemical Tech & Biotech

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BACKGROUND This work is focused on the assessment of the performance of mini‐scale air‐breathing microbial fuel cells (MFCs), by monitoring the evolution of the bio‐electrogenic activity for a period of 40 days and by comparing the microorganisms populations developed in each of the MFCs after this period. RESULTS Five MFCs were operated at sludge ages ranging from 1.4 to 10.0 days. Results showed the superb performance of the MFC operating under a sludge age of 2.5 days. Desulfuromonas, Syntrophothermus, Solitalea, Acholeplasma, Propionicimonas, Desulfobacula and Sphaerochaeta are proposed as potentially responsible for the bio‐electrogenic activity. CONCLUSIONS Microbial population analysis through Illumina amplicon sequencing demonstrated that despite all MFCs being seeded with the same mixed culture inoculum, the biological cultures developed in the suspension and the biofilm are completely different and depend strongly on sludge age. © 2017 Society of Chemical Industry

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Novel phenazine crystals enable direct electron transfer to methanogens in anaerobic digestion by redox potential modulation

Abstract: Phenazine crystals enhance methanogenesis by electron delivery to respiratory heterodisulfide reductase enzyme.

Cited by 75 publications

References 34 publications

Carbon nanotubes accelerate methane production in pure cultures of methanogens and in a syntrophic coculture

Carbon nanotubes accelerate methane production in pure cultures of methanogens and in a syntrophic coculture

Physiological Evidence for Isopotential Tunneling in the Electron Transport Chain of Methane-Producing Archaea

Effect of sludge age on microbial consortia developed in MFCs

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