Metatranscriptomic insights into the microbial electrosynthesis of acetate by Fe2+/Ni2+ addition

Agency IE (2021) Global Energy Review: CO2 Emissions in 2021. Internation Energy Agency. https://www.iea.org/reports/global-energy-review-co2-emissions-in-2021-2. Accessed March 2022 Aklujkar M, Leang C, Shrestha PM, Shrestha M, Lovley DR (2017) Transcriptomic profiles of Clostridium ljungdahlii during lithotrophic growth with syngas or H2 and CO2 compared to organotrophic growth with fructose. Sci Rep 7:14. https://doi.org/10.1038/s41598-017-12712-w Ammam F, Tremblay PL, Lizak DM, Zhang T (2016) Effect of tungstate on acetate and ethanol production by the electrosynthetic bacterium Sporomusa ovata. Biotechnol Biofuels 9:10. https://doi.org/10.1186/s13068-016-0576-0 Arends JBA, Patil SA, Roume H, Rabaey K (2017) Continuous long-term electricity-driven bioproduction of carboxylates and isopropanol from CO2 with a mixed microbial community. J CO2 Util 20:141–149. https://doi.org/10.1016/j.jcou.2017.04.014 Aryal N, Ammam F, Patil SA, Pant D (2017a) An overview of cathode materials for microbial electrosynthesis of chemicals from carbon dioxide. Green Chem 19(24):5748–5760. https://doi.org/10.1039/c7gc01801k Aryal N, Tremblay PL, Lizak DM, Zhang T (2017b) Performance of different Sporomusa species for the microbial electrosynthesis of acetate from carbon dioxide. Bioresour Technol 233:184–190. https://doi.org/10.1016/j.biortech.2017.02.128 Bajracharya S, ter Heijne A, Dominguez Benetton X, Vanbroekhoven K, Buisman CJN, Strik DPBTB, Pant D (2015) Carbon dioxide reduction by mixed and pure cultures in microbial electrosynthesis using an assembly of graphite felt and stainless steel as a cathode. Bioresour Technol 195:14–24. https://doi.org/10.1016/j.biortech.2015.05.081 Bajracharya S, Yuliasni R, Vanbroekhoven K, Buisman CJN, Strik D, Pant D (2017) Long-term operation of microbial electrosynthesis cell reducing CO2 to multi-carbon chemicals with a mixed culture avoiding methanogenesis. Bioelectrochemistry 113:26–34. https://doi.org/10.1016/j.bioelechem.2016.09.001 Bar-Even A, Flamholz A, Noor E, Milo R (2012) Thermodynamic constraints shape the structure of carbon fixation pathways. Biochim Biophys Acta-Bioenerg 1817(9):1646–1659. https://doi.org/10.1016/j.bbabio.2012.05.002 Batlle-Vilanova P, Ganigue R, Ramio-Pujol S, Baneras L, Jimenez G, Hidalgo M, Balaguer MD, Colprim J, Puig S (2017) Microbial electrosynthesis of butyrate from carbon dioxide: production and extraction. Bioelectrochemistry 117:57–64. https://doi.org/10.1016/j.bioelechem.2017.06.004 Boyington JC, Gladyshev VN, Khangulov SV, Stadtman TC, Sun PD (1997) Crystal structure of Formate dehydrogenase H: Catalysis Involving Mo, Molybdopterin, Selenocysteine, and an Fe4S4 cluster. Science 275(5304):1305–1308. https://doi.org/10.1126/science.275.5304.1305 Buckel W, Thauer RK (2018) Flavin-Based Electron Bifurcation, Ferredoxin, Flavodoxin, and anaerobic respiration with protons (ech) or NAD(+) (rnf) as Electron acceptors: a historical review. Front Microbiol 9:24. https://doi.org/10.3389/fmicb.2018.00401 Chiranjeevi P, Patil SA (2020) Strategies for improving the electroactivity and specific metabolic functionality of microorganisms for various microbial electrochemical technologies. Biotechnol Adv 39:16. https://doi.org/10.1016/j.biotechadv.2019.107468 Choi O, Um Y, Sang BI (2012) Butyrate production enhancement by Clostridium tyrobutyricum using electron mediators and a cathodic electron donor. Biotechnol Bioeng 109(10):2494–2502. https://doi.org/10.1002/bit.24520 Cui M, Nie H, Zhang T, Lovley D, Russell TP (2017) Three-dimensional hierarchical metal oxide-carbon electrode materials for highly efficient microbial electrosynthesis. Sustain Energ Fuels 1(5):1171–1176. https://doi.org/10.1039/c7se00073a Doukov TI, Blasiak LC, Seravalli J, Ragsdale SW, Drennan CL (2008) Xenon in and at the end of the tunnel of Bifunctional Carbon Monoxide Dehydrogenase/Acetyl-CoA synthase. Biochemistry 47(11):3474–3483. https://doi.org/10.1021/bi702386t Drake HL, Gossner AS, Daniel SL (2008) Old acetogens, new light. In: Wiegel J, Maier RJ, Adams MWW (eds) Incredible Anaerobes: from physiology to Genomics to Fuels. Annals of the New York Academy of Sciences, vol 1125. Wiley-Blackwell, Malden, pp 100–128. doi:https://doi.org/10.1196/annals.1419.016 Dross F, Geisler V, Lenger R, Theis F, Krafft T, Fahrenholz F, Kojro E, Duchene A, Tripier D, Juvenal K, Kroger A (1992) The quinone-reactive Ni/Fe-hydrogenase of Wolinella succinogenes. Eur J Biochem 206(1):93–102. https://doi.org/10.1111/j.1432-1033.1992.tb16905.x Feng X, Schut GJ, Haja DK, Adams MWW, Li HL (2022) Structure and electron transfer pathways of an electron-bifurcating NiFe-hydrogenase. Sci Adv 8(8):13. https://doi.org/10.1126/sciadv.abm7546 Fontmorin JM, Izadi P, Li D, Lim SS, Farooq S, Bilal SS, Cheng SA, Yu EH (2021) Gas diffusion electrodes modified with binary doped polyaniline for enhanced CO2 conversion during microbial electrosynthesis. Electrochim Acta 372:9. https://doi.org/10.1016/j.electacta.2021.137853 Guo Q, Majeed S, Xu R, Zhang K, Kakade A, Khan A, Hafeez FY, Mao C, Liu P, Li X (2019) Heavy metals interact with the microbial community and affect biogas production in anaerobic digestion: a review. J Environ Manage 240:266–272. https://doi.org/10.1016/j.jenvman.2019.03.104 Hirose A, Kasai T, Aoki M, Umemura T, Watanabe K, Kouzuma A (2018) Electrochemically active bacteria sense electrode potentials for regulating catabolic pathways. Nat Commun 9. https://doi.org/10.1038/s41467-018-03416-4 Hreha TN, Mezic KG, Herce HD, Duffy EB, Bourges A, Pryshchep S, Juarez O, Barquera B (2015) Complete topology of the RNF Complex from Vibrio cholerae. Biochemistry 54(15):2443–2455. https://doi.org/10.1021/acs.biochem.5b00020 Ismail WM, Ye Y, Tang H (2014) Gene finding in metatranscriptomic sequences. BMC Bioinformatics 15(9):S8. https://doi.org/10.1186/1471-2105-15-S9-S8 Izadi P, Fontmorin J-M, Godain A, Yu EH, Head IM (2020) Parameters influencing the development of highly conductive and efficient biofilm during microbial electrosynthesis: the importance of applied potential and inorganic carbon source. npj Biofilms and Microbiomes 6(1):40. https://doi.org/10.1038/s41522-020-00151-x Jourdin L, Freguia S, Donose BC, Keller J (2015) Autotrophic hydrogen-producing biofilm growth sustained by a cathode as the sole electron and energy source. Bioelectrochemistry 102:56–63. https://doi.org/10.1016/j.bioelechem.2014.12.001 Kopylova E, Noé L, Touzet H (2012) SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28(24):3211–3217. https://doi.org/10.1093/bioinformatics/bts611 Kracke F, Vassilev I, Krömer JO (2015) Microbial electron transport and energy conservation - the foundation for optimizing bioelectrochemical systems. Front Microbiol 6:575. https://doi.org/10.3389/fmicb.2015.00575 Lemaire ON, Wagner T (2021) Gas channel rerouting in a primordial enzyme: structural insights of the carbon-monoxide dehydrogenase/acetyl-CoA synthase complex from the acetogen Clostridium autoethanogenum. Biochim Biophys Acta-Bioenerg 1862(1):14. https://doi.org/10.1016/j.bbabio.2020.148330 Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12(1):323. https://doi.org/10.1186/1471-2105-12-323 Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22(13):1658–1659. https://doi.org/10.1093/bioinformatics/btl158 Liang TT, Zhou L, Irfan M, Bai Y, Liu XZ, Zhang JL, Wu ZY, Wang WZ, Liu JF, Cheng L, Yang SZ, Ye RQ, Gu JD, Mu BZ (2020) Assessment of five Electron-shuttling molecules in the Extracellular Electron transfer of Electromethanogenesis by using Methanosarcina barkeri. ChemElectroChem 7(18):3783–3789. https://doi.org/10.1002/celc.202000918 Liu H, Wang J, Wang AJ, Chen JA (2011) Chemical inhibitors of methanogenesis and putative applications. Appl Microbiol Biotechnol 89(5):1333–1340. https://doi.org/10.1007/s00253-010-3066-5 Liu JK, Lloyd C, Al-Bassam MM, Ebrahim A, Kim JN, Olson C, Aksenov A, Dorrestein P, Zengler K (2019) Predicting proteome allocation, overflow metabolism, and metal requirements in a model acetogen. PLoS Comput Biol 15(3):16. https://doi.org/10.1371/journal.pcbi.1006848 Lohner ST, Deutzmann JS, Logan BE, Leigh J, Spormann AM (2014) Hydrogenase-independent uptake and metabolism of electrons by the archaeon Methanococcus maripaludis. Isme J 8(8):1673–1681. https://doi.org/10.1038/ismej.2014.82 Maier T, Böck A (1996) Generation of active [NiFe] Hydrogenase in Vitro from a nickel-free Precursor Form. Biochemistry 35(31):10089–10093. https://doi.org/10.1021/bi960567l Maier T, Binder U, Böck A (1996) Analysis of the hydA locus of Escherichia coli: two genes (hydN and hypF) involved in formate and hydrogen metabolism. Arch Microbiol 165(5):333–341. https://doi.org/10.1007/s002030050335 Marshall CW, Ross DE, Handley KM, Weisenhorn PB, Edirisinghe JN, Henry CS, Gilbert JA, May HD, Norman RS (2016) Metabolic Reconstruction and Modeling Microbial Electrosynthesis. bioRxiv:059410. doi:https://doi.org/10.1101/059410 Martens JA, Bogaerts A, De Kimpe N, Jacobs PA, Marin GB, Rabaey K, Saeys M, Verhelst S (2017) The Chemical Route to a Carbon Dioxide Neutral World. Chemsuschem 10(6):1039–1055. https://doi.org/10.1002/cssc.201601051 Mateos R, Sotres A, Alonso RM, Escapa A, Moran A (2018) Impact of the start-up process on the microbial communities in biocathodes for electrosynthesis. Bioelectrochemistry 121:27–37. https://doi.org/10.1016/j.bioelechem.2018.01.002 Mayer F, Muller V (2014) Adaptations of anaerobic archaea to life under extreme energy limitation. Fems Microbiol Rev 38(3):449–472. https://doi.org/10.1111/1574-6976.12043 Mohanakrishna G, Vanbroekhoven K, Pant D (2018) Impact of dissolved carbon dioxide concentration on the process parameters during its conversion to acetate through microbial electrosynthesis. React Chem Eng 3(3):371–378. https://doi.org/10.1039/c7re00220c Muller V, Imkamp F, Biegel E, Schmidt S, Dilling S (2008) Discovery of a Ferredoxin: NAD(+)-Oxidoreductase (rnf) in Acetobacterium woodii - A novel potential coupling site in acetogens. In: Wiegel J, Maier RJ, Adams MWW (eds) Incredible Anaerobes: from physiology to Genomics to Fuels. Annals of the New York Academy of Sciences, vol 1125. Blackwell Publishing, Oxford, pp 137–146. doi:https://doi.org/10.1196/annals.1419.011 Nevin KP, Woodard TL, Franks AE, Summers ZM, Lovley DR (2010) Microbial Electrosynthesis: feeding Microbes Electricity to convert Carbon Dioxide and Water to Multicarbon Extracellular Organic Compounds. mBio 1(2):4. https://doi.org/10.1128/mBio.00103-10 Niks D, Hille R (2019) Molybdenum- and tungsten-containing formate dehydrogenases and formylmethanofuran dehydrogenases: structure, mechanism, and cofactor insertion. Protein Sci 28(1):111–122. https://doi.org/10.1002/pro.3498 Nimbalkar PR, Khedkar MA, Parulekar RS, Chandgude VK, Sonawane KD, Chavan PV, Bankar SB (2018) Role of Trace Elements as Cofactor: an efficient strategy toward enhanced Biobutanol Production. ACS Sustain Chem Eng 6(7):9304–9313. https://doi.org/10.1021/acssuschemeng.8b01611 Perona-Vico E, Feliu-Paradeda L, Puig S, Baneras L (2020) Bacteria coated cathodes as an in-situ hydrogen evolving platform for microbial electrosynthesis. Sci Rep 10(1):11. https://doi.org/10.1038/s41598-020-76694-y Prevoteau A, Carvajal-Arroyo JM, Ganigue R, Rabaey K (2020) Microbial electrosynthesis from CO2: forever a promise? Curr Opin Biotechnol 62:48–57. https://doi.org/10.1016/j.copbio.2019.08.014 Ragsdale SW (2009) Nickel-based enzyme Systems*. J Biol Chem 284(28):18571–18575. https://doi.org/10.1074/jbc.R900020200 Saxena J, Tanner RS (2011) Effect of trace metals on ethanol production from synthesis gas by the ethanologenic acetogen, Clostridium ragsdalei. J Ind Microbiol Biotechnol 38(4):513–521. https://doi.org/10.1007/s10295-010-0794-6 Schuchmann K, Muller V (2012) A bacterial Electron-bifurcating hydrogenase. J Biol Chem 287(37):31165–31171. https://doi.org/10.1074/jbc.M112.395038 Schuchmann K, Muller V (2014) Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria. Nat Rev Microbiol 12(12):809–821. https://doi.org/10.1038/nrmicro3365 Schuchmann K, Müller V (2013) Direct and reversible hydrogenation of CO2 to Formate by a bacterial Carbon Dioxide Reductase. Science 342(6164):1382–1385. https://doi.org/10.1126/science.1244758 Sena AMP, Brázdová V, Bowler DR (2009) Density functional theory study of the iron-based porphyrin haem(b) on the Si(111):H surface. Phys Rev B 79(24):245404. https://doi.org/10.1103/PhysRevB.79.245404 Seravalli J, Zhao SY, Ragsdale SW (1999) Mechanism of transfer of the methyl group from (6S)-methyltetrahydrofolate to the corrinoid/iron-sulfur protein catalyzed by the methyltransferase from Clostridium thermoaceticum: a key step in the Wood-Ljungdahl pathway of acetyl-CoA synthesis. Biochemistry 38(18):5728–5735. https://doi.org/10.1021/bi982473c Spero MA, Aylward FO, Currie CR, Donohue TJ (2015) Phylogenomic analysis and predicted physiological role of the Proton-Translocating NADH:Quinone Oxidoreductase (Complex I) across Bacteria. mBio 6(2):e00389–e00315. https://doi.org/10.1128/mBio.00389-15 Tahir K, Miran W, Jang J, Woo SH, Lee DS (2021) Enhanced product selectivity in the microbial electrosynthesis of butyrate using a nickel ferrite-coated biocathode. Environ Res 196:9. https://doi.org/10.1016/j.envres.2021.110907 Tai HL, Hirota S, Stripp ST (2021) Proton transfer mechanisms in Bimetallic Hydrogenases. Acc Chem Res 54(1):232–241. https://doi.org/10.1021/acs.accounts.0c00651 Tremblay PL, Zhang T, Dar SA, Leang C, Lovley DR (2013) The Rnf Complex of Clostridium ljungdahlii is a Proton-Translocating Ferredoxin:NAD(+) oxidoreductase essential for Autotrophic Growth. mBio 4(1):8. https://doi.org/10.1128/mBio.00406-12 Vassilev I, Hernandez PA, Batlle-Vilanova P, Freguia S, Krömer JO, Keller J, Ledezma P, Virdis B (2018) Microbial Electrosynthesis of Isobutyric, Butyric, Caproic acids, and corresponding alcohols from Carbon Dioxide. ACS Sustain Chem Eng 6(7):8485–8493. https://doi.org/10.1021/acssuschemeng.8b00739 Velazquez I, Nakamaru-Ogiso E, Yano T, Ohnishi T, Yagi T (2005) Amino acid residues associated with cluster N3 in the NuoF subunit of the proton-translocating NADH-quinone oxidoreductase from Escherichia coli. FEBS Lett 579(14):3164–3168. https://doi.org/10.1016/j.febslet.2005.05.005 Wang GR, Huang Q, Song TS, Xie JJ (2020) Enhancing Microbial Electrosynthesis of acetate and butyrate from CO2 reduction Involving Engineered Clostridium ljungdahlii with a nickel-phosphide-modified electrode. Energy Fuels 34(7):8666–8675. https://doi.org/10.1021/acs.energyfuels.0c01710 Wenzel J, Fiset E, Batlle-Vilanova P, Cabezas A, Etchebehere C, Balaguer MD, Colprim J, Puig S (2018) Microbial Community Pathways for the production of volatile fatty acids from CO2 and electricity. Front Energy Res 6. https://doi.org/10.3389/fenrg.2018.00015 Wu RR, Song HY, Wang YM, Wang L, Zhu ZG (2020) Multienzyme co-immobilization-based bioelectrode: design of principles and bioelectrochemical applications. Chin J Chem Eng 28(8):2037–2050. https://doi.org/10.1016/j.cjche.2020.04.003 Xiang YB, Liu GL, Zhang RD, Lu YB, Luo HP (2017) Acetate production and electron utilization facilitated by sulfate-reducing bacteria in a microbial electrosynthesis system. Bioresour Technol 241:821–829. https://doi.org/10.1016/j.biortech.2017.06.017 Yamamoto I, Saiki T, Liu SM, Ljungdahl LG (1983) Purification and properties of NADP-dependent formate dehydrogenase from Clostridium thermoaceticum, a tungsten-selenium-iron protein. J Biol Chem 258(3):1826–1832. https://doi.org/10.1016/S0021-9258(18)33062-X Zhang T, Nie HR, Bain TS, Lu HY, Cui MM, Snoeyenbos-West OL, Franks AE, Nevin KP, Russell TP, Lovley DR (2013) Improved cathode materials for microbial electrosynthesis. Energy Environ Sci 6(1):217–224. https://doi.org/10.1039/c2ee23350a Zhang J, Liu H, Zhang Y, Wu P, Li J, Ding P, Jiang Q, Cui MH (2022) Heterotrophic precultivation is a better strategy than polarity reversal for the startup of acetate microbial electrosynthesis reactor. Biochem Eng J 179:10. https://doi.org/10.1016/j.bej.2021.108319 Zhu HF, Liu ZY, Zhou X, Yi JH, Lun ZM, Wang SN, Tang WZ, Li FL (2020) Energy Conservation and Carbon Flux distribution during fermentation of CO or H2/CO2 by Clostridium ljungdahlii. Front Microbiol 11:9. https://doi.org/10.3389/fmicb.2020.00416