Influence of headspace composition on product diversity by sulphate reducing bacteria biocathode
Graphical abstract
Introduction
Recently there has been an emerging class of study on microbes which are capable of taking up electrons from cathodic surfaces and utilizing them for a series of electrochemical transformations through which they reduce inorganic (e.g. CO2) or organic chemicals (e.g. volatile fatty acids) into extracellular organic compounds (Soussan et al., 2013, Schröder, 2011, Rabaey and Rozendal, 2010). Microbial electrosynthesis requires some external electrical input to drive the conversions and overcome cathodic over-potentials, since many of the coupled electrochemical reactions are usually not thermodynamically feasible (Harnisch and Schröder, 2010). This electrical enhancement manipulates the redox metabolism by generation of reduced NADH within the cell through microbial electrodic interface reactions (Pandit and Mahadevan, 2011). More recently, major advances have been made in this realm of microbial electrosynthesis signifying the urgent need of research in this sector for production of value added chemicals. The successful demonstration of directly feeding electrons to acetogens with electrodes and the concept of integration of photovoltaics with electricity driven microbial reduction to organics was pitched by Nevin et al. (2010). Besides, there have been reports where this process is used for the production of H2 (Rozendal et al., 2009, Sleutels et al., 2013), caustic soda (Rabaey et al., 2010), hydrogen peroxide (Rozendal et al., 2009), methane (Wagner et al., 2009, Villano et al., 2010, Cheng et al., 2009), caproate, caprylate (Van Eerten-Jansen et al., 2013) and combination of one or more of the above mentioned chemicals (Lovley and Nevin, 2013, Marshall et al., 2012, Angenent and Rosenbaum, 2013).
In our previous study, we reported the possibility of bioelectrochemically reducing acetic and butyric acids to a number of organic products such as alcohols and acetone by a mixed electroactive (EA) sulphate reducing bacteria (SRB, now designated as TERI-MS-003) based biocathode (Sharma et al., 2013a). Electrons used for such conversions are derived mainly from direct electron transfer (DET). Yet a minor role was attributed to H2 as energy carrier. Steinbusch et al. (2008) proved that increasing H2 partial pressure (HPP) by accumulation in the headspace would result in a metabolic shift from acidogenesis to alcohol production. Villano et al. (2010) showed that the product profile can be influenced by the gases present in the headspace mainly by hydrogen generation along with bioelectrochemical conversion of carbon dioxide to methane when cathode potential was poised more negative than −0.7 V vs. Ag/AgCl. However in our study, methane production was not observed, presumably due to high salinity and acidic pH of the electrolyte.
Following our earlier results and the rationale of such above mentioned citations, the effect of HPP is investigated here as a step further to elucidate the mechanistic features involved in SRB electrosynthesis in Bioelectrochemical systems (BES). This overall research aims to culminate in practical application to recycle and subsequently divert energy in the form of biochemicals, particularly from low grade organic carbon present in wastewaters like fermentation effluents.
Section snippets
Inoculum and electrolyte
Inoculum of a mixed EA-SRB, TERI-MS-003 consortium was taken from a previously running bioelectrochemical reactor (Sharma et al., 2013a).The inoculum (10% v/v) was added to the electrolyte used for reactor operation, that consisted of a synthetic feed composed of 572 mg NH4Cl, 416 mg KH2PO4, 8 mg CaCl2, 96 mg MgCl2·6H2O, 1.98 mg FeCl2·4H2O, 2.37 mg CoCl2·6H2O, 0.59 mg MnCl2·4H2O, 0.034 CuCl2·2H2O, 0.062 mg H3BO3, 0.073 mg Na2MoO4·2H2O, 0.069 mg Na2SeO3, 0.095 mg NiCl2·6H2O, 0.055 mg ZnCl2 and 10 g NaCl per
Result and discussion
One of the major bottlenecks for conversion of electrical energy into organic chemicals via microbial electrocatalytic systems has been the unavailability of biocathodes that can achieve selected transformations at relevant kinetic rates. In our recent study (Sharma et al., 2013a), the development of SRB biocathode was achieved. The same inoculum (TERI-MS-003) was used here to develop a biocathode in a low-cost, easy to assemble, single chambered reactor as shown in the schematic (ES 1),
Conclusions
Electroactive SRB biocathodes serve as efficient biocatalysts and the metabolic routes shifts with alteration of headspace environment. Though most of such metabolic interventions are generally carried out though metabolic engineering, this study demonstrates that a set of economically desirable (bio) chemicals can be bioelectrochemically synthesized without any genetic manipulations in the biocatalyst. Other bigger challenges like effective separation of these microbial electrosynthesized
Acknowledgements
This work was funded by the Department of Science and Technology, India (Sanction number DST/INTSPAIN/P-23/2009). M.S. also acknowledge Indo-Belgian scholarship from the Flemish Government (Vlaamse Gemeenschap). The authors thank Dr. R.K. Pachauri, Director General TERI for providing excellent infrastructure and research facility. The authors also thank Mr. Rambaran for his technical assistance and Mr. Pradeep from HEG Ltd. for providing electrode sample material.
References (35)
- et al.
Waste to bioproduct conversion with undefined mixed cultures: the carboxylate platform
Trends Biotechnol.
(2011) - et al.
Effect of hydrogen and carbon dioxide on carboxylic acids patterns in mixed culture fermentation
Bioresour. Technol.
(2012) - et al.
A sequential electron transfer from hydrogenases to cytochromes in sulfate-reducing bacteria
Biochim. Biophys. Acta
(2000) - et al.
Biocorrosion: towards understanding interactions between biofilms and metals
Curr. Opin. Biotechnol.
(2004) - et al.
Electroactive biofilms of sulphate reducing bacteria
Electrochim. Acta
(2008) - et al.
A shift in the current: new applications and concepts for microbe-electrode electron exchange
Curr. Opin. Biotechnol.
(2011) - et al.
Electrobiocommodities: powering microbial production of fuels and commodity chemicals from carbon dioxide with electricity
Curr. Opin. Biotechnol.
(2013) - et al.
Efficient hydrogen peroxide generation from organic matter in a bioelectrochemical system
Electrochem. Commun.
(2009) - et al.
Enhanced performance of sulfate reducing bacteria based biocathode using stainless steel mesh on activated carbon fabric electrode
Bioresour. Technol.
(2013) - et al.
Steady-state performance and chemical efficiency of microbial electrolysis cells
Int. J. Hydrogen Energy
(2013)
Electrochemical reduction of CO2 catalysed by Geobacter sulfurreducens grown on polarized stainless steel cathodes
Electrochem. Commun.
Alcohol production through volatile fatty acids reduction with hydrogen as electron donor by mixed cultures
Water Res.
Accelerated cathodic reaction in microbial corrosion of iron due to direct electron uptake by sulfate-reducing bacteria
Corros. Sci.
Bioelectrochemical reduction of CO(2) to CH(4) via direct and indirect extracellular electron transfer by a hydrogenophilic methanogenic culture
Bioresour. Technol.
Hydrogen and methane production from swine wastewater using microbial electrolysis cells
Water Res.
Microbial electrocatalysis to guide biofuel and biochemical bioprocessing
Biofuels
Direct biological conversion of electrical current into methane by electromethanogenesis
Environ. Sci. Technol.
Cited by (21)
Progress and perspectives on microbial electrosynthesis for valorisation of CO<inf>2</inf> into value-added products
2023, Journal of Environmental ManagementCopper ferrite supported reduced graphene oxide as cathode materials to enhance microbial electrosynthesis of volatile fatty acids from CO<inf>2</inf>
2021, Science of the Total EnvironmentCitation Excerpt :Therefore, MES systems showed high production rates in continuous or batch operations. The results of a study by Sharma et al. have shown the efficient conversion of CO2 into mixed products of VFAs with high production rates using mixed cultures [Sharma et al., 2014]. However, the function of individual species in mixed cultures is still unclear to the scientific community.
Carbon dioxide and organic waste valorization by microbial electrosynthesis and electro-fermentation
2019, Water ResearchCitation Excerpt :For example, using an electrode with a poised potential of −0.55 V, acetate was reduced to ethanol by mixed culture of bacteria using methyl viologen (MV) as a mediator (Steinbusch et al., 2010). Other studies reported that mixed culture such as sulfate-reducing bacteria (SRB) could also reduce acetic and butyric acids to alcohols (ethanol, butanol, methanol, and propanol) and acetone in MES without the addition of artificial mediators (Kondaveeti and Min, 2015; Sharma et al., 2013, 2014). Using the solid electrode as the electron donor with a working potential caproic acid, butyric acid, and caprylic acid were produced from acetic acid, likely through the H2 route of inward EET (Raes et al., 2017; Van Eerten-Jansen et al., 2013a).
Expanding the product spectrum of value added chemicals in microbial electrosynthesis through integrated process design—A review
2018, Bioresource TechnologyCitation Excerpt :A mixed culture of sulfate-reducing bacteria, was reported to achieve the reduction of acetic and butyric acids to alcohols (ethanol, butanol, methanol, and propanol) and acetone in MES without the addition of artificial mediators (Sharma et al., 2013). Further study indicated that the gases present in headspace environment could significantly affect the product profile from the reduction of VFAs (Sharma et al., 2014). Using a practical AD effluent as the substrate for the production of various alcohols by MES was also reported, and it pointed out that the accumulation of unexpected lactic acid might be the main reason of the limited biofuel production (Kondaveeti and Min, 2015).
Evaluation of key parameters on simultaneous sulfate reduction and sulfide oxidation in an autotrophic biocathode
2017, Water ResearchCitation Excerpt :Bioelectrosynthesis has opened a plethora of new applications. Among them, the use of SRB in a biocathode has been reported (Sharma et al., 2014, 2013), showing that SRB could use the electrons coming from the anode to convert acetic and butyric acids to alcohols and acetone presumably via direct electron transfer. Some authors have also shown how an SRB-enriched consortium can also reduce sulfate.
Bio-electro catalytic treatment of petroleum produced water: Influence of cathode potential upliftment
2016, Bioresource TechnologyCitation Excerpt :The performance was evaluated based on power output, substrate degradation, sulfate removal and electron discharge pattern. Mixed consortium (TERI-MS-003) rich in SRB, enriched from different petroleum refineries and formation sites across India, was used as inoculum (Sharma et al., 2014). The inoculum was enriched initially in API RP-38 medium (4 g sodium lactate, 1 g yeast extract, 0.1 g ascorbic acid, 0.2 g MgSO4, 0.01 g K2HPO4, 0.1 g KH2PO4, 0.2 g(NH4)2FeSO4 and 10 g NaCl, for 1 L, pH-7.4) and added to the BES anode (10% v/v) under anaerobic condition.
- 1
These authors contributed equally to this manuscript and should be considered as co-first authors.