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Review Articles

Role and potential of the semi-classical/-quantum mechanism of the extracellular environment and cell envelope in Direct Interspecies Electron Transfer (DIET)-driven biomethanation

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Pages 581-601 | Published online: 09 Nov 2023

References

  • Abken, H.-J., Tietze, M., Brodersen, J., Bäumer, S., Beifuss, U., & Deppenmeier, U. (1998). Isolation and characterization of methanophenazine and function of phenazines in membrane-bound electron transport of methanosarcina mazei Gö1. Journal of Bacteriology, 180(8), 2027–2032. https://doi.org/10.1128/JB.180.8.2027-2032.1998
  • Albers, S.-V., Kappler, U., Dahl, C., Kletzin, A., Heimerl, T., Flechsler, J., van Niftrik, L., Rachel, R., & Klingl, A. (2015). Cytochromes c in Archaea: Distribution, maturation, cell architecture, and the special case of Ignicoccus hospitalis. Frontiers in Microbiology, 6, 439. https://doi.org/10.3389/fmicb.2015.00439
  • Albers, S.-V., & Meyer, B. H. (2011). The archaeal cell envelope. Nature Reviews. Microbiology, 9(6), 414–426. https://doi.org/10.1038/nrmicro2576
  • Amdursky, N., Marchak, D., Sepunaru, L., Pecht, I., Sheves, M., & Cahen, D. (2014). Electronic transport via proteins. Advanced Materials (Deerfield Beach, FL), 26(42), 7142–7161. https://doi.org/10.1002/adma.201402304
  • Amdursky, N., Sepunaru, L., Raichlin, S., Pecht, I., Sheves, M., & Cahen, D. (2015). Electron transfer proteins as electronic conductors: Signifi cance of the metal and its binding site in the blue Cu protein, azurin. Advanced Science, 2(4), 1400026. https://doi.org/10.1002/advs.201400026
  • Amit, M., Appel, S., Cohen, R., Cheng, G., Hamley, I. W., & Ashkenasy, N. (2014). Hybrid proton and electron transport in peptide fibrils. Advanced Functional Materials, 24(37), 5873–5880. https://doi.org/10.1002/adfm.201401111
  • Anderson, K. L., Apolinario, E. E., & Sowers, K. R. (2012). Desiccation as a long-term survival mechanism for the archaeon Methanosarcina barkeri. Applied and Environmental Microbiology, 78(5), 1473–1479. https://doi.org/10.1128/AEM.06964-11
  • Ankerhold, J., & Lehle, H. (2004). Low temperature electron transfer in strongly condensed phase. The Journal of Chemical Physics, 120(3), 1436–1449. https://doi.org/10.1063/1.1630297
  • Arbing, M. A., Chan, S., Shin, A., Phan, T., Ahn, C. J., Rohlin, L., & Gunsalus, R. P. (2012). Structure of the surface layer of the methanogenic archaean Methanosarcina acetivorans. Proceedings of the National Academy of Sciences of the United States of America, 109(29), 11812–11817. https://doi.org/10.1073/PNAS.1120595109
  • Ardoña, H. A. M., Besar, K., Togninalli, M., Katz, H. E., & Tovar, J. D. (2015). Sequence-dependent mechanical, photophysical and electrical properties of pi-conjugated peptide hydrogelators. Journal of Materials Chemistry C, 3(25), 6505–6514. https://doi.org/10.1039/C5TC00100E
  • Arikuma, Y., Nakayama, H., Morita, T., & Kimura, S. (2010). Electron hopping over 100 Å along an α helix. Angewandte Chemie (International ed. in English), 49(10), 1800–1804. https://doi.org/10.1002/anie.200905621
  • Aslam, M., Yang, P., Lee, P. H., & Kim, J. (2018). Novel staged anaerobic fluidized bed ceramic membrane bioreactor: Energy reduction, fouling control and microbial characterization. Journal of Membrane Science, 553, 200–208. https://doi.org/10.1016/j.memsci.2018.02.038
  • Barber, R. D., Zhang, L., Harnack, M., Olson, M. v., Kaul, R., Ingram-Smith, C., & Smith, K. D. (2011). Complete genome sequence of Methanosaeta concilii, a specialist in aceticlastic methanogenesis. Journal of Bacteriology, 193(14), 3668–3669. https://doi.org/10.1128/JB.05031-11
  • Beifuss, U., Tietze, M., Bäumer, S., & Deppenmeier, U. (2000). Methanophenazine: Structure, total synthesis, and function of a new cofactor from Methanogenic Archaea. Angewandte Chemie International Edition, 39(14), 2470–2472. https://doi.org/10.1002/1521-3773(20000717)39:14 < 2470::AID-ANIE2470 > 3.0.CO;2-R
  • Bendall, D. S. (Ed.). (1996). Protein electron transfer. (D. S. Bendall, ed.; 1st ed.). Garland Science. https://doi.org/10.1201/9781003076803
  • Beratan, D. N. (2019). Why are DNA and protein electron transfer so different? Annual Review of Physical Chemistry, 70(1), 71–97. https://doi.org/10.1146/annurev-physchem-042018
  • Beratan, D. N., Betts, J. N., & Onuchic, J. N. (1991). Protein electron transfer rates set by the bridging secondary and tertiary structure. Science (New York, NY), 252(5010), 1285–1288. https://doi.org/10.1126/science.1656523
  • Bond, D. R., & Lovley, D. R. (2002). Reduction of Fe(III) oxide by methanogens in the presence and absence of extracellular quinones. Environmental Microbiology, 4(2), 115–124. https://doi.org/10.1046/j.1462-2920.2002.00279.x
  • Braun-Sand, S., Burykin, A., Tao Chu, Z., & Warshel, A. (2005). Realistic simulations of proton transport along the gramicidin channel: Demonstrating the importance of solvation effects. The Journal of Physical Chemistry. B, 109(1), 583–592. https://doi.org/10.1021/jp0465783
  • Cahen, D., Pecht, I., & Sheves, M. (2021). What can we learn from protein-based electron transport junctions? The Journal of Physical Chemistry Letters, 12(47), 11598–11603. https://doi.org/10.1021/acs.jpclett.1c02446
  • Chakrabarti, B., Park, J. W., & Stevens, E. S. (1980). Glycosaminoglycans: Structure and interaction. CRC Critical Reviews in Biochemistry, 8(3), 225–313. https://doi.org/10.3109/10409238009102572
  • Chattopadhyay, S., Bandyopadhyay, S., & Dey, A. (2021). Kinetic isotope effects on electron transfer across self-assembled monolayers on gold. Inorganic Chemistry, 60(2), 597–605. https://doi.org/10.1021/acs.inorgchem.0c02185
  • Chen, R., Konishi, Y., & Nomura, T. (2018). Enhancement of methane production by Methanosarcina barkeri using Fe3O4 nanoparticles as iron sustained release agent. Advanced Powder Technology, 29(10), 2429–2433. https://doi.org/10.1016/j.apt.2018.06.022
  • Chiu, U. T., & Chao, L. (2019). Electron transfer through protein-bound water and its bioelectronic application. Biosensors & Bioelectronics, 136, 16–22. https://doi.org/10.1016/J.BIOS.2019.04.012
  • Cordes, M., & Giese, B. (2009). Electron transfer in peptides and proteins. Chemical Society Reviews, 38(4), 892–901. https://doi.org/10.1039/b805743p
  • Costentin, C., Robert, M., & Savéant, J. M. (2010). Concerted proton-electron transfers: Electrochemical and related approaches. Accounts of Chemical Research, 43(7), 1019–1029. https://doi.org/10.1021/ar9002812
  • D’Acunto, M. (2022). Quantum biology. π–π entanglement signatures in protein-DNA interactions. Physical Biology, 19(3), 036003. https://doi.org/10.1088/1478-3975/ac5bda
  • de Bruin, S., Vasquez-Cardenas, D., Sarbu, S. M., Meysman, F. J. R., Sousa, D. Z., van Loosdrecht, M. C. M., & Lin, Y. (2022). Sulfated glycosaminoglycan-like polymers are present in an acidophilic biofilm from a sulfidic cave. The Science of the Total Environment, 829, 154472. https://doi.org/10.1016/J.SCITOTENV.2022.154472
  • de Vrieze, J., Hennebel, T., Boon, N., & Verstraete, W. (2012). Methanosarcina: The rediscovered methanogen for heavy duty biomethanation. Bioresource Technology, 112, 1–9. https://doi.org/10.1016/J.BIORTECH.2012.02.079
  • Duan, L., Jiang, W., Song, Y., Xia, S., & Hermanowicz, S. W. (2013). The characteristics of extracellular polymeric substances and soluble microbial products in moving bed biofilm reactor-membrane bioreactor. Bioresource Technology, 148, 436–442. https://doi.org/10.1016/J.BIORTECH.2013.08.147
  • Dubé, C.-D., & Guiot, S. R. (2019). Characterization of the protein fraction of the extracellular polymeric substances of three anaerobic granular sludges. AMB Express, 9(1), 23. https://doi.org/10.1186/s13568-019-0746-0
  • Duszenko, N., & Buan, N. R. (2017). Physiological evidence for isopotential tunneling in the electron transport chain of methane-producing Archaea. Applied and Environmental Microbiology, 83(18), e0095017. https://doi.org/10.1128/AEM.00950-17
  • Edwards, S. J., Soudackov, A. v., & Hammes-Schiffer, S. (2009). Analysis of kinetic isotope effects for proton-coupled electron transfer reactions. The Journal of Physical Chemistry. A, 113(10), 2117–2126. https://doi.org/10.1021/jp809122y
  • Fereiro, J. A., Yu, X., Pecht, I., Sheves, M., Cuevas, J. C., & Cahen, D. (2018). Tunneling explains efficient electron transport via protein junctions. Proceedings of the National Academy of Sciences of the United States of America, 115(20), E4577–E4583. https://doi.org/10.1073/PNAS.1719867115
  • Flemming, H.-C., & Wingender, J. (2010). The biofilm matrix. Nature Reviews. Microbiology, 8(9), 623–633. https://doi.org/10.1038/nrmicro2415
  • Flemming, H.-C., Wingender, J., Szewzyk, U., Steinberg, P., Rice, S. A., & Kjelleberg, S. (2016). Biofilms: An emergent form of bacterial life. Nature Reviews. Microbiology, 14(9), 563–575. https://doi.org/10.1038/nrmicro.2016.94
  • França, C. G., Villalva, D. G., & Santana, M. H. A. (2021). Oxi-HA/ADH hydrogels: A novel approach in tissue engineering and regenerative medicine. Polysaccharides, 2(2), 477–496. https://doi.org/10.3390/polysaccharides2020029
  • Francoleon, D. R., Boontheung, P., Yang, Y., Kin, U., Ytterberg, A. J., Denny, P. A., Denny, P. C., Loo, J. A., Gunsalus, R. P., & Loo, R. R. O. (2009). S-layer, surface-accessible, and concanavalin A binding proteins of Methanosarcina acetivorans and Methanosarcina mazei. Journal of Proteome Research, 8(4), 1972–1982. https://doi.org/10.1021/pr800923e
  • Galagedera, S. K. K., Flechsig, G.-U., Galagedera, K. K., & Flechsig, G.-U. (2019). Voltammetric H/D isotope effects on redox-active small molecules conjugated with DNA self-assembled monolayers. ChemElectroChem, 6(18), 4781–4788. https://doi.org/10.1002/celc.201901151
  • Gao, K., & Lu, Y. (2021). Putative extracellular electron transfer in Methanogenic Archaea. Frontiers in Microbiology, 12, 611739. https://doi.org/10.3389/fmicb.2021.611739
  • Gao, L. G., Zhang, R. M., Xu, X., & Truhlar, D. G. (2019). Quantum effects on H2 diffusion in zeolite RHO: Inverse kinetic isotope effect for sieving. Journal of the American Chemical Society, 141(34), 13635–13642. https://doi.org/10.1021/jacs.9b06506
  • Glover, S. D., Tyburski, R., Liang, L., Tommos, C., & Hammarström, L. (2018). Pourbaix diagram, proton-coupled electron transfer, and decay kinetics of a protein tryptophan radical: Comparing the redox properties of W32• and Y32• generated inside the structurally characterized α3W and α3Y proteins. Journal of the American Chemical Society, 140(1), 185–192. https://doi.org/10.1021/jacs.7b08032
  • Godbey, W. T. (2014). Cellular transport. In An introduction to biotechnology. The science, technology and medical applications (pp. 35–64). Woodhead Publishing. https://doi.org/10.1016/B978-1-907568-28-2.00003-4
  • Goddard, T. D., Huang, C. C., Meng, E. C., Pettersen, E. F., Couch, G. S., Morris, J. H., & Ferrin, T. E. (2018). UCSF ChimeraX: Meeting modern challenges in visualization and analysis. Protein Science: A Publication of the Protein Society, 27(1), 14–25. https://doi.org/10.1002/pro.3235
  • Gong, S., Zhu, Z. H., & Li, Z. (2017). Electron tunnelling and hopping effects on the temperature coefficient of resistance of carbon nanotube/polymer nanocomposites. Physical Chemistry Chemical Physics: PCCP, 19(7), 5113–5120. https://doi.org/10.1039/c6cp08115k
  • Gorby, Y. A., Yanina, S., McLean, J. S., Rosso, K. M., Moyles, D., Dohnalkova, A., Beveridge, T. J., Chang, I. S., Kim, B. H., Kim, K. S., Culley, D. E., Reed, S. B., Romine, M. F., Saffarini, D. A., Hill, E. A., Shi, L., Elias, D. A., Kennedy, D. W., Pinchuk, G., … Fredrickson, J. K. (2006). Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proceedings of the National Academy of Sciences of the United States of America, 103(30), 11358–11363. https://doi.org/10.1073/pnas.0604517103
  • Gray, H. B., & Winkler, J. R. (2003). Electron tunneling through proteins. Quarterly Reviews of Biophysics, 36(3), 341–372. https://doi.org/10.1017/S0033583503003913
  • Gray, H. B., & Winkler, J. R. (2009). Electron flow through proteins. Chemical Physics Letters, 483(1–3), 1–9. https://doi.org/10.1016/J.CPLETT.2009.10.051
  • Hammarström, L., & Styring, S. (2011). Proton-coupled electron transfer of tyrosines in Photosystem II and model systems for artificial photosynthesis: The role of a redox-active link between catalyst and photosensitizer. Energy & Environmental Science, 4(7), 2379–2388. https://doi.org/10.1039/c1ee01348c
  • Hines, T., Diez-Perez, I., Hihath, J., Liu, H., Wang, Z.-S., Zhao, J., Zhou, G., Müllen, K., & Tao, N. (2010). Transition from tunneling to hopping in single molecular junctions by measuring length and temperature dependence. Journal of the American Chemical Society, 132(33), 11658–11664. https://doi.org/10.1021/ja1040946
  • Holmes, D. E., Ueki, T., Tang, H.-Y., Zhou, J., Smith, J. A., Chaput, G., & Lovley, D. R. (2019). A membrane-bound cytochrome enables methanosarcina acetivorans to conserve energy from extracellular electron transfer. mBio, 10(4), e00789. https://doi.org/10.1128/mBio.00789-19
  • Holmes, D. E., Zhou, J., Ueki, T., Woodard, T., & Lovley, D. R. (2021). Mechanisms for electron uptake by methanosarcina acetivorans during direct interspecies electron transfer. mBio, 12(5), e02344. https://doi.org/10.1128/mBio.02344-21
  • Huang, L., Liu, X., Zhang, Z., Ye, J., Rensing, C., Zhou, S., & Nealson, K. H. (2022). Light-driven carbon dioxide reduction to methane by Methanosarcina barkeri in an electric syntrophic coculture. The ISME Journal, 16(2), 370–377. https://doi.org/10.1038/s41396-021-01078-7
  • Kumar, R. J., MacDonald, J. M., Birendra Singh, T. J., Waddington, L. B., & Holmes, A. (2011). Hierarchical self-assembly of semiconductor functionalized peptide α-helices and optoelectronic properties. Journal of the American Chemical Society, 133(22), 8564–8573. https://doi.org/10.1021/ja110858k
  • Jasso-Chávez, R., Santiago-Martínez, M. G., Lira-Silva, E., Pineda, E., Zepeda-Rodríguez, A., Belmont-Díaz, J., Encalada, R., Saavedra, E., & Moreno-Sánchez, R. (2015). Air-adapted methanosarcina acetivorans shows high methane production and develops resistance against oxygen stress. PloS One, 10(2), e0117331. https://doi.org/10.1371/journal.pone.0117331
  • Jia, M., Kim, J., Nguyen, T., Duong, T., & Rolandi, M. (2021). Natural biopolymers as proton conductors in bioelectronics. Biopolymers, 112(7), e23433. https://doi.org/10.1002/bip.23433
  • Jiang, Y., Shi, M., & Shi, L. (2019). Molecular underpinnings for microbial extracellular electron transfer during biogeochemical cycling of earth elements. Science China. Life Sciences, 62(10), 1275–1286. https://doi.org/10.1007/s11427-018-9464-3
  • Jiang, Z., Shi, M., & Shi, L. (2020). Degradation of organic contaminants and steel corrosion by the dissimilatory metal-reducing microorganisms Shewanella and Geobacter spp. International Biodeterioration & Biodegradation, 147, 104842. https://doi.org/10.1016/j.ibiod.2019.104842
  • Jiang, Z., Yu, Q., Sun, C., Wang, Z., Jin, Z., Zhu, Y., Zhao, Z., & Zhang, Y. (2022). Additional electric field alleviates acidity suppression in anaerobic digestion of kitchen wastes via enriching electro-active methanogens in cathodic biofilms. Water Research, 212, 118118. https://doi.org/10.1016/J.WATRES.2022.118118
  • Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., Bridgland, A., Meyer, C., Kohl, S. A. A., Ballard, A. J., Cowie, A., Romera-Paredes, B., Nikolov, S., Jain, R., Adler, J., … Hassabis, D. (2021). Highly accurate protein structure prediction with AlphaFold. Nature, 596(7873), 583–589. https://doi.org/10.1038/s41586-021-03819-2
  • Kandler, O., & Hippe, H. (1977). Lack of peptidoglycan in the cell walls of Methanosarcina barkeri. Archives of Microbiology, 113(1–2), 57–60. https://doi.org/10.1007/BF00428580
  • Kang, F., Qu, X. J. J., Alvarez, P., & Zhu, D. (2017). Extracellular saccharide-mediated reduction of Au3+ to gold nanoparticles: New insights for heavy metals biomineralization on microbial surfaces. Environmental Science & Technology, 51(5), 2776–2785. https://doi.org/10.1021/acs.est.6b05930
  • Kato, S. (2016). Microbial extracellular electron transfer and its relevance to iron corrosion. Microbial Biotechnology, 9(2), 141–148. https://doi.org/10.1111/1751-7915.12340
  • Kaufmann, J., Möhle, K., Hofmann, H. J., & Arnold, K. (1999). Molecular dynamics of a tetrasaccharide subunit of chondroitin 4-sulfate in water. Carbohydrate Research, 318(1–4), 1–9. https://doi.org/10.1016/S0008-6215(99)00091-9
  • Kayser, B., Fereiro, J. A., Bhattacharyya, R., Cohen, S. R., Vilan, A., Pecht, I., Sheves, M., & Cahen, D. (2020). Solid-state electron transport via the protein azurin is temperature-independent down to 4 K. The Journal of Physical Chemistry Letters, 11(1), 144–151. https://doi.org/10.1021/acs.jpclett.9b03120
  • Kim, Y., Bertagna, F., D’Souza, E. M., Heyes, D. J., Johannissen, L. O., Nery, E. T., Pantelias, A., Sanchez-Pedreño Jimenez, A., Slocombe, L., Spencer, M. G., Al-Khalili, J., Engel, G. S., Hay, S., Hingley-Wilson, S. M., Jeevaratnam, K., Jones, A. R., Kattnig, D. R., Lewis, R., Sacchi, M., … McFadden, J. (2021). Quantum biology: An update and perspective. Quantum Reports, 3(1), 80–126.   https://doi.org/10.3390/quantum3010006
  • Koga, Y., & Morii, H. (2005). Recent advances in structural research on ether lipids from archaea including comparative and physiological aspects. Bioscience, Biotechnology, and Biochemistry, 69(11), 2019–2034. https://doi.org/10.1271/bbb.69.2019
  • Kopě, J., Maki, J. S., Nikolausz, M., Nagler, M., Podmirseg, S. M., Mayr, M., Ascher-Jenull, J., & Insam, H. (2020). Quantities of intra- and extracellular DNA reveal information about activity and physiological state of Methanogenic Archaea. Frontiers in Microbiology, 11, 1894. https://doi.org/10.3389/fmicb.2020.01894
  • Kreisl, P., & Kandler, O. (1986). Chemical structure of the cell wall polymer of methanosarcina. Systematic and Applied Microbiology, 7(2–3), 293–299. https://doi.org/10.1016/S0723-2020(86)80022-4
  • Kwon, D., Lam, T. Y. C., Kim, M., Tan, G.-Y. A., Lee, P.-H., & Kim, J. (2021). Combined effect of activated carbon particles and non-adsorptive spherical beads as fluidized media on fouling, organic removal and microbial communities in anaerobic membrane bioreactor. Membranes, 11(5), 365. https://doi.org/10.3390/membranes11050365
  • Larsson, B., Nilsson, M., & Tjälve, H. (1981). The binding of inorganic and organic cations and H + to cartilage in vitro. Biochemical Pharmacology, 30(21), 2963–2970. https://doi.org/10.1016/0006-2952(81)90260-4
  • Lei, L., Zhang, J., Guan, R., Liu, J., Chen, F., & Tao, Z. (2020). Energy storage and hydrogen production by proton conducting solid oxide electrolysis cells with a novel heterogeneous design. Energy Conversion and Management, 218, 113044. https://doi.org/10.1016/j.enconman.2020.113044
  • Li, L., Xu, Y., Dai, X., & Dai, L. (2021). Principles and advancements in improving anaerobic digestion of organic waste via direct interspecies electron transfer. Renewable and Sustainable Energy Reviews, 148, 111367. https://doi.org/10.1016/j.rser.2021.111367
  • Lindsay, S. (2020). Ubiquitous electron transport in non-electron transfer proteins. Life (Basel, Switzerland), 10(5), 72. https://doi.org/10.3390/life10050072
  • Liu, X., Walker, D. J. F., Nonnenmann, S. S., Sun, D., & Lovley, D. R. (2021). Direct observation of electrically conductive Pili emanating from geobacter sulfurreducens. mBio, 12(4), e02209. https://doi.org/10.1128/mBio.02209-21
  • Liu, D., Wang, H., Dong, H., Qiu, X., Dong, X., & Cravotta, C. A. (2011). Mineral transformations associated with goethite reduction by Methanosarcina barkeri. Chemical Geology, 288(1–2), 53–60. https://doi.org/10.1016/j.chemgeo.2011.06.013
  • Liu, Y., Wang, Z., Liu, J., Levar, C., Edwards, M. J., Babauta, J. T., Kennedy, D. W., Shi, Z., Beyenal, H., Bond, D. R., Clarke, T. A., Butt, J. N., Richardson, D. J., Rosso, K. M., Zachara, J. M., Fredrickson, J. K., & Shi, L. (2014). A trans-outer membrane porin-cytochrome protein complex for extracellular electron transfer by Geobacter sulfurreducens PCA. Environmental Microbiology Reports, 6(6), 776–785. https://doi.org/10.1111/1758-2229.12204
  • Sanders, A. M., Dawidczyk, T. J., Katz, H. E., & Tovar, J. (2012). Peptide-based supramolecular semiconductor nanomaterials via Pd-catalyzed solid-phase “dimerizations. ACS Macro Letters, 1(11), 1326–1329. https://doi.org/10.1021/mz3004665
  • Maleki, A., Kjøniksen, A. L., & Nyström, B. (2008). Effect of pH on the behavior of hyaluronic acid in dilute and semidilute aqueous solutions. Macromolecular Symposia, 274(1), 131–140. https://doi.org/10.1002/masy.200851418
  • Marcus, R. A., & Sutin, N. (1985). Electron transfers in chemistry and biology. Biochimica et Biophysica Acta (BBA) - Reviews on Bioenergetics, 811(3), 265–322. https://doi.org/10.1016/0304-4173(85)90014-X
  • McGlynn, S. E. (2017). Energy metabolism during anaerobic methane oxidation in ANME Archaea. Microbes and Environments, 32(1), 5–13. https://doi.org/10.1264/jsme2.ME16166
  • Meisner, J., & Kästner, J. (2016). Atom tunneling in chemistry. Angewandte Chemie (International ed. in English), 55(18), 5400–5413. https://doi.org/10.1002/anie.201511028
  • Meysman, F. J. R., Cornelissen, R., Trashin, S., Bonné, R., Martinez, S. H., van der Veen, J., Blom, C. J., Karman, C., Hou, J.-L., Eachambadi, R. T., Geelhoed, J. S., Wael, K. D., Beaumont, H. J. E., Cleuren, B., Valcke, R., van der Zant, H. S. J., Boschker, H. T. S., & Manca, J. V. (2019). A highly conductive fibre network enables centimetre-scale electron transport in multicellular cable bacteria. Nature Communications, 10(1), 4120. https://doi.org/10.1038/s41467-019-12115-7
  • Michele, C., Alessandra, M., Ivano, T., Paolo, C., & Ursula, R. (2006). Role of protein frame and solvent for the redox properties of azurin from Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences of the United States of America, 103(52), 19641–19646. https://doi.org/10.1073/pnas.0607890103
  • Milkevych, V., & Batstone, D. J. (2014). Controlling mechanisms in directional growth of aggregated archaeal cells. Soft Matter, 10(48), 9615–9625. https://doi.org/10.1039/C4SM01870B
  • Milkevych, V., Donose, B. C., Juste-Poinapen, N., & Batstone, D. J. (2015). Mechanical and cell-to-cell adhesive properties of aggregated Methanosarcina. Colloids and Surfaces. B, Biointerfaces, 126, 303–312. https://doi.org/10.1016/J.COLSURFB.2014.12.035
  • Munro, A. W., & McLean, K. J. (2013). Electron transfer cofactors. In G. C. K. Roberts (Ed.), Encyclopedia of biophysics (pp. 601–606). Springer Berlin Heidelberg. https://doi.org/10.1007/978-3-642-16712-6_41
  • Nakamura, K., Hatakeyama, T., & Hatakeyama, H. (1983). Relationship between hydrogen bonding and bound water in polyhydroxystyrene derivatives. Polymer, 24(7), 871–876. https://doi.org/10.1016/0032-3861(83)90206-9
  • Newberry, R. W., & Raines, R. T. (2017). The n→π* interaction. Accounts of Chemical Research, 50(8), 1838–1846. https://doi.org/10.1021/acs.accounts.7b00121
  • Nguyen, V., Karunakaran, E., Collins, G., & Biggs, C. A. (2016). Physicochemical analysis of initial adhesion and biofilm formation of Methanosarcina barkeri on polymer support material. Colloids and Surfaces. B, Biointerfaces, 143, 518–525. https://doi.org/10.1016/J.COLSURFB.2016.03.042
  • Nguyen, V. T. (2016). Biofilm formation of methanosarcina barkeri on different support materials: applications for anaerobic digestion [PhD dissertation]. The University of Sheffield. ProQuest Dissertations Publishing.
  • Ouellette, R. J., & Rawn, J. D. (2015). Amino acids, peptides, and proteins. In Principles of organic chemistry (pp. 371–396). Elsevier. https://doi.org/10.1016/b978-0-12-802444-7.00014-8
  • Paddock, M. L., Feher, G., & Okamura, M. Y. (2000). Identification of the proton pathway in bacterial reaction centers: Replacement of Asp-M17 and Asp-L210 with Asn reduces the proton transfer rate in the presence of Cd2+. Proceedings of the National Academy of Sciences of the United States of America, 97(4), 1548–1553. https://doi.org/10.1073/pnas.97.4.1548
  • Park, J. H., Kang, H. J., Park, K. H., & Park, H. D. (2018). Direct interspecies electron transfer via conductive materials: A perspective for anaerobic digestion applications. Bioresource Technology, 254, 300–311. https://doi.org/10.1016/J.BIORTECH.2018.01.095
  • Patil, S. A., Harnisch, F., Kapadnis, B., & Schröder, U. (2010). Electroactive mixed culture biofilms in microbial bioelectrochemical systems: The role of temperature for biofilm formation and performance. Biosensors & Bioelectronics, 26(2), 803–808. https://doi.org/10.1016/J.BIOS.2010.06.019
  • Pettersen, E. F., Goddard, T. D., Huang, C. C., Meng, E. C., Couch, G. S., Croll, T. I., Morris, J. H., & Ferrin, T. E. (2021). UCSF ChimeraX: Structure visualization for researchers, educators, and developers. Protein Science: A Publication of the Protein Society, 30(1), 70–82. https://doi.org/10.1002/pro.3943
  • Polo, F., Antonello, S., Formaggio, F., Toniolo, C., & Maran, F. (2005). Evidence against the hopping mechanism as an important electron transfer pathway for conformationally constrained oligopeptides. Journal of the American Chemical Society, 127(2), 492–493. https://doi.org/10.1021/ja043607e
  • Rao, R., Hu, I., & Lee, P.-H. (2022). Theoretical characterisation of electron tunnelling from granular activated carbon to electron accepting organisms in direct interspecies electron transfer. Scientific Reports, 12(1), 12426. https://doi.org/10.1038/s41598-022-15606-8
  • Reguera, G., McCarthy, K. D., Mehta, T., Nicoll, J. S., Tuominen, M. T., & Lovley, D. R. (2005). Extracellular electron transfer via microbial nanowires. Nature, 435(7045), 1098–1101. https://doi.org/10.1038/nature03661
  • Roca, C., Alves, V. D., Freitas, F., & Reis, M. A. M. (2015). Exopolysaccharides enriched in rare sugars: Bacterial sources, production, and applications. Frontiers in Microbiology, 6, 288. https://doi.org/10.3389/fmicb.2015.00288
  • Rohlin, L., Leon, D. R., Kim, U., Loo, J. A., Ogorzalek Loo, R. R., & Gunsalus, R. P. (2012). Identification of the major expressed S-layer and cell surface-layer-related proteins in the model methanogenic Archaea: Methanosarcina barkeri fusaro and Methanosarcina acetivorans C2A. Archaea (Vancouver, BC), 2012, 873589–873510. https://doi.org/10.1155/2012/873589
  • Rowe, A. R., Salimijazi, F., Trutschel, L., Sackett, J., Adesina, O., Anzai, I., Kugelmass, L. H., Baym, M. H., & Barstow, B. (2021). Identification of a pathway for electron uptake in Shewanella oneidensis. Communications Biology, 4(1), 957. https://doi.org/10.1038/s42003-021-02454-x
  • Santos, F. M., Barbosa, P. C., Pereira, R. F. P., Silva, M. M., Gonçalves, H. M. R., Nunes, S. C., Figueiredo, F. L., Valente, A. J. M., & de Zea Bermudez, V. (2020). Proton conducting electrolytes composed of chondroitin sulfate polysaccharide and citric acid. European Polymer Journal, 124, 109453. https://doi.org/10.1016/j.eurpolymj.2019.109453
  • Sattelle, B. M., Shakeri, J., Roberts, I. S., & Almond, A. (2010). A 3D-structural model of unsulfated chondroitin from high-field NMR: 4-sulfation has little effect on backbone conformation. Carbohydrate Research, 345(2), 291–302. https://doi.org/10.1016/J.CARRES.2009.11.013
  • Saunders, S. H., Tse, E. C. M., Yates, M. D., Otero, F. J., Trammell, S. A., Stemp, E. D. A., Barton, J. K., Tender, L. M., & Newman, D. K. (2020). Extracellular DNA promotes efficient extracellular electron transfer by pyocyanin in Pseudomonas aeruginosa biofilms. Cell, 182(4), 919–932.e19. https://doi.org/10.1016/J.CELL.2020.07.006
  • Selberg, J., Jia, M., & Rolandi, M. (2019). Proton conductivity of glycosaminoglycans. PloS One, 14(3), e0202713. https://doi.org/10.1371/journal.pone.0202713
  • Selyanchyn, O., Selyanchyn, R., & Lyth, S. M. (2006). A review of proton conductivity in cellulosic materials. Frontiers in Energy Research, 8. https://doi.org/10.3389/fenrg.2020.596164
  • Sepunaru, L., Friedman, N., Pecht, I., Sheves, M., & Cahen, D. (2012). Temperature-dependent solid-state electron transport through bacteriorhodopsin: Experimental evidence for multiple transport paths through proteins. Journal of the American Chemical Society, 134(9), 4169–4176. https://doi.org/10.1021/ja2097139
  • Shang, H., Daye, M., Sivan, O., Borlina, C. S., Tamura, N., Weiss, B. P., & Bosak, T. (2020). Formation of zerovalent iron in iron-reducing cultures of Methanosarcina barkeri. Environmental Science & Technology, 54(12), 7354–7365. https://doi.org/10.1021/acs.est.0c01595
  • Shi, L., Dong, H., Reguera, G., Beyenal, H., Lu, A., Liu, J., Yu, H.-Q., & Fredrickson, J. K. (2016). Extracellular electron transfer mechanisms between microorganisms and minerals. Nature Reviews. Microbiology, 14(10), 651–662. https://doi.org/10.1038/nrmicro.2016.93
  • Shi, Y., Liu, T., Chen, S., & Quan, X. (2022). Accelerating anaerobic hydrolysis acidification of dairy wastewater in integrated floating-film and activated sludge (IFFAS) by using zero-valent iron (ZVI) composite carriers. Biochemical Engineering Journal, 177, 108226. https://doi.org/10.1016/j.bej.2021.108226
  • Shin, C., & Bae, J. (2018). Current status of the pilot-scale anaerobic membrane bioreactor treatments of domestic wastewaters: A critical review. Bioresource Technology, 247, 1038–1046. https://doi.org/10.1016/J.BIORTECH.2017.09.002
  • Shipps, C., Kelly, R. H., Dahl, P. J., Yi, S. M., Vu, D., Boyer, D., Glynn, C., Sawaya, M. R., Eisenberg, D., Batista, V. S., & Malvankar, N. S. (2021). Intrinsic electronic conductivity of individual atomically resolved amyloid crystals reveals micrometer-long hole hopping via tyrosines. Proceedings of the National Academy of Sciences of the United States of America, 118(2), e2014139118. https://doi.org/10.1073/pnas.2014139118
  • Shmilovich, K., Yao, Y., Tovar, J. D., Katz, H. E., Schleife, A., & Ferguson, A. L. (2022). Computational discovery of high charge mobility self-assembling π-conjugated peptides. Molecular Systems Design & Engineering, 7(5), 447–459. https://doi.org/10.1039/D2ME00017B
  • Slocombe, L., Al-Khalili, J. S., & Sacchi, M. (2021). Quantum and classical effects in DNA point mutations: Watson-Crick tautomerism in AT and GC base pairs. Physical Chemistry Chemical Physics: PCCP, 23(7), 4141–4150. https://doi.org/10.1039/d0cp05781a
  • Snetkov, P., Zakharova, K., Morozkina, S., Baranov, M., Olekhnovich, R., & Uspenskaya, M. (2020). Electrosprayed nanoparticles based on hyaluronic acid: Preparation and characterization. Technologies, 8(4), 71. https://doi.org/10.3390/technologies8040071
  • Sowers, K. R., Boone, J. E., & Gunsalus, R. P. (1993). Disaggregation of Methanosarcina spp. and growth as single cells at elevated osmolarity. Applied and Environmental Microbiology, 59(11), 3832–3839. https://doi.org/10.1128/aem.59.11.3832-3839.1993
  • Sprott, D. G., Dicaire, C. J., Choquet, C. G., Patel, G. B., & Ekiel, I. (1993). Hydroxydiether lipid structures in Methanosarcina spp. and Methanococcus voltae. Applied and Environmental Microbiology, 59(3), 912–914. https://doi.org/10.1128/aem.59.3.912-914.1993
  • Storck, T., Virdis, B., & Batstone, D. J. (2016). Modelling extracellular limitations for mediated versus direct interspecies electron transfer. The ISME Journal, 10(3), 621–631. https://doi.org/10.1038/ismej.2015.139
  • Sundaresan, G., Abraham, R. J. J., Appa Rao, V., Narendra Babu, R., Govind, V., & Meti, M. F. (2018). Established method of chondroitin sulphate extraction from buffalo (Bubalus bubalis) cartilages and its identification by FTIR. Journal of Food Science and Technology, 55(9), 3439–3445. https://doi.org/10.1007/s13197-018-3253-4
  • Tang, W. K., Mu, X., Li, M., Martens, J., Berden, G., Oomens, J., Chu, I. K., & Siu, C.-K. (2020). Formation of n → π+ interaction facilitating dissociative electron transfer in isolated tyrosine-containing molecular peptide radical cations. Physical Chemistry Chemical Physics: PCCP, 22(37), 21393–21402. https://doi.org/10.1039/D0CP00533A
  • Tang, L., Yi, L., Jiang, T., Ren, R., Paulose Nadappuram, B., Zhang, B., Wu, J., Liu, X., Lindsay, S., Edel, J. B., & Ivanov, A. P. (2022). Measuring conductance switching in single proteins using quantum tunneling. Science Advances, 8(20), eabm8149. https://doi.org/10.1126/sciadv.abm8149
  • Tietze, M., Beuchle, A., Lamla, I., Orth, N., Dehler, M., Greiner, G., & Beifuss, U. (2003). Redox potentials of methanophenazine and CoB-S-S-CoM, factors involved in electron transport in Methanogenic Archaea. Chembiochem: A European Journal of Chemical Biology, 4(4), 333–335. https://doi.org/10.1002/cbic.200390053
  • Tokita, Y., & Okamoto, A. (1995). Hydrolytic degradation of hyaluronic acid. Polymer Degradation and Stability, 48(2), 269–273. https://doi.org/10.1016/0141-3910(95)00041-J
  • Tyburski, R., Liu, T., D. Glover, S., & Hammarström, L. (2021). Proton-coupled electron transfer guidelines, fair and square. Journal of the American Chemical Society, 143(2), 560–576. https://doi.org/10.1021/jacs.0c09106
  • Varadi, M., Anyango, S., Deshpande, M., Nair, S., Natassia, C., Yordanova, G., Yuan, D., Stroe, O., Wood, G., Laydon, A., Žídek, A., Green, T., Tunyasuvunakool, K., Petersen, S., Jumper, J., Clancy, E., Green, R., Vora, A., Lutfi, M., … Velankar, S. (2022). AlphaFold protein structure database: Massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Research, 50(D1), D439–D444. https://doi.org/10.1093/nar/gkab1061
  • Veiga, M. C., Jain, M. K., Wu, W., Hollingsworth, R. I., & Zeikus, J. G. (1997). Composition and role of extracellular polymers in methanogenic granules. Applied and Environmental Microbiology, 63(2), 403–407. https://doi.org/10.1128/aem.63.2.403-407.1997
  • Wagner, D., Schirmack, J., Ganzert, L., Morozova, D., & Mangelsdorf, K. (2013). Methanosarcina soligelidi sp. nov., a desiccation- and freeze-thaw-resistant methanogenic archaeon from a Siberian permafrost-affected soil. International Journal of Systematic and Evolutionary Microbiology, 63(Pt 8), 2986–2991. https://doi.org/10.1099/ijs.0.046565-0
  • Walker, D. J. F., Martz, E., Holmes, D. E., Zhou, Z., Nonnenmann, S. S., & Lovley, D. R. (2019). The archaellum of Methanospirillum hungatei is electrically conductive. mBio, 10(2), e00579. https://doi.org/10.1128/mBio.00579-19
  • Wall, B. D., Diegelmann, S. R., Zhang, S., Dawidczyk, T. J., Wilson, W. L., Katz, H. E., Mao, H.-Q., & Tovar, J. D. (2011). Aligned macroscopic domains of optoelectronic nanostructures prepared via shear-flow assembly of peptide hydrogels. Advanced Materials (Deerfield Beach, FL), 23(43), 5009–5014, 4967. https://doi.org/10.1002/adma.201102963
  • Wang, W., & Lee, D. J. (2021). Direct interspecies electron transfer mechanism in enhanced methanogenesis: A mini-review. Bioresource Technology, 330, 124980. https://doi.org/10.1016/J.BIORTECH.2021.124980
  • Wang, P., Li, X., Chu, S., Su, Y., Wu, D., & Xie, B. (2022). Metatranscriptomic insight into the effects of antibiotic exposure on performance during anaerobic co-digestion of food waste and sludge. Journal of Hazardous Materials, 423(Pt B), 127163. https://doi.org/10.1016/J.JHAZMAT.2021.127163
  • Wang, C., Qiao, W., Chen, H., Xu, X., & Zhu, L. (2019). A short-term stimulation of ethanol enhances the effect of magnetite on anaerobic digestion. Applied Microbiology and Biotechnology, 103(3), 1511–1522. https://doi.org/10.1007/s00253-018-9531-2
  • Watanabe, K., Manefield, M., Lee, M., & Kouzuma, A. (2009). Electron shuttles in biotechnology. Current Opinion in Biotechnology, 20(6), 633–641. https://doi.org/10.1016/J.COPBIO.2009.09.006
  • Winkler, J. R., & Gray, H. B. (2014). Long-Range Electron Tunneling. Journal of the American Chemical Society, 136(8), 2930–2939. https://doi.org/10.1021/ja500215j
  • Xiang, L., Palma, J. L., Bruot, C., Mujica, V., Ratner, M. A., & Tao, N. (2015). Intermediate tunnelling–hopping regime in DNA charge transport. Nature Chemistry, 7(3), 221–226. https://doi.org/10.1038/nchem.2183
  • Xiao, X., Xu, B., & Tao, N. (2004). Conductance titration of single-peptide molecules. Journal of the American Chemical Society, 126(17), 5370–5371. https://doi.org/10.1021/ja049469a
  • Xiao, Y., Zhang, E., Zhang, J., Dai, Y., Yang, Z., Christensen, H. E. M., Ulstrup, J., & Zhao, F. (2017). Extracellular polymeric substances are transient media for microbial extracellular electron transfer. Science Advances, 3(7), e1700623. https://doi.org/10.1126/sciadv.1700623
  • Xin, H., Sim, W. J., Namgung, B., Choi, Y., Li, B., & Lee, L. P. (2019). Quantum biological tunnel junction for electron transfer imaging in live cells. Nature Communications, 10(1), 3245. https://doi.org/10.1038/s41467-019-11212-x
  • Yardeni, J. L., Amit, M., Ashkenasy, G., & Ashkenasy, N. (2016). Sequence dependent proton conduction in self-assembled peptide nanostructures. Nanoscale, 8(4), 2358–2366. https://doi.org/10.1039/c5nr06750b
  • Ye, J., Yu, J., Zhang, Y., Chen, M., Liu, X., Zhou, S., & He, Z. (2019). Light-driven carbon dioxide reduction to methane by Methanosarcina barkeri-CdS biohybrid. Applied Catalysis B: Environmental, 257, 117916. https://doi.org/10.1016/j.apcatb.2019.117916
  • Yee, M. O., & Rotaru, A.-E. (2020). Extracellular electron uptake in Methanosarcinales is independent of multiheme c-type cytochromes. Scientific Reports, 10(1), 372. https://doi.org/10.1038/s41598-019-57206-z
  • Yee, M. O., Snoeyenbos-West, O. L., Thamdrup, B., Ottosen, L. D. M., & Rotaru, A.-E. (2019). Extracellular electron uptake by two methanosarcina species. Frontiers in Energy Research, 7, 29. https://doi.org/10.3389/fenrg.2019.00029
  • Young, C.-C., Rekha, P. D., Lai, W.-A., & Arun, A. B. (2006). Encapsulation of plant growth-promoting bacteria in alginate beads enriched with humic acid. Biotechnology and Bioengineering, 95(1), 76–83. https://doi.org/10.1002/bit.20957
  • Yu, L., He, D., Zhang, E., He, Q., Li, J., Jason Ren, Z., & Zhou, S. (2021). Electricity from anaerobic methane oxidation by a single methanogenic archaeon Methanosarcina barkeri. Chemical Engineering Journal, 405, 126691. https://doi.org/10.1016/j.cej.2020.126691
  • Yuan, Y., Zhou, L., Hou, R., Wang, Y., & Zhou, S. (2021). Centimeter-long microbial electron transport for bioremediation applications. Trends in Biotechnology, 39(2), 181–193. https://doi.org/10.1016/J.TIBTECH.2020.06.011
  • Zhang, J., Dong, H., Zhao, L., McCarrick, R., & Agrawal, A. (2014). Microbial reduction and precipitation of vanadium by mesophilic and thermophilic methanogens. Chemical Geology, 370, 29–39. https://doi.org/10.1016/j.chemgeo.2014.01.014
  • Zhang, F., Xu, H., Shelobolina, E., Konishi, H., & Roden, E. (2021). Precipitation of low-temperature disordered dolomite induced by extracellular polymeric substances of methanogenic Archaea Methanosarcina barkeri: Implications for sedimentary dolomite formation. American Mineralogist, 106(1), 69–81. https://doi.org/10.2138/am-2020-7381
  • Zhou, J., Holmes, D. E., Tang, H.-Y., & Lovley, D. R. (2021). Correlation of key physiological properties of methanosarcina isolates with environment of origin. Applied and Environmental Microbiology, 87(13), e00731. https://doi.org/10.1128/AEM.00731-21
  • Zimbovskaya, N. (2003). Low temperature electronic transport and electron transfer through organic macromolecules. The Journal of Chemical Physics, 118(1), 4–7. https://doi.org/10.1063/1.1533077

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