Abstract
The deep ocean may be one of the largest microbial habitats on the planet. Hence, high hydrostatic pressure is a feature of microbial life. We know very little about the deep biosphere because simulating deep ocean conditions in the laboratory whilst simultaneously monitoring microbial processes is difficult. Changes in pressure can inhibit some reactions, whilst simultaneously accelerating others. Assumptions about how biochemical reactions proceed under ambient conditions may lack validity in the deep biosphere. In extreme environments, microbes often exploit metabolic strategies that yield slim energetic margins. How these occur under pressure is an interesting thermodynamic puzzle. Extracellular electron transfer (EET) is a process whereby microbes respire solid substrates in their surrounding environment. For an electron to move outside of the cell, it must transit the microbial envelope through a series of membrane bound electron carriers each of which will have a unique pressure response. EET most likely evolved in the deep biosphere and therefore makes an excellent model system for studying microbial energetics in high pressure environments. In this chapter, the reader can explore the fundamentals of thermodynamics, the discovery of EET, theoretical implications of pressure effects on the relevant biochemical apparatus, and learn about a proposed system for studying the interesting phenomenon of EET under high pressure.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abe F (2007) Exploration of the effects of high hydrostatic pressure on microbial growth, physiology and survival: Perspectives from piezophysiology. Biosci Biotechnol Biochem 71:2347–2357
Allen RM, Bennetto HP (1993) Microbial fuel-cells. Appl Biochem Biotechnol 39:27–40
Aparicio FL, Nieto-Cid M, Borrull E, Romero E, Stedmon CA, Sala MM, Gasol JM, Ríos AF, Marrasé C (2015) Microbially-mediated fluorescent organic matter transformations in the deep ocean. Do the chemical precursors matter? Front Marine Sci 2:106
Bartlett DH (1999) Microbial adaptations to the psychrosphere/piezosphere. J Mol Microbiol Biotechnol 1:93–100
Bartlett DH (2002) Pressure effects on in vivo microbial processes. Biochimica et Biophysica Acta (BBA)—Protein Struct Mol Enzymol 1595:367–381
Bird LJ, Bonnefoy V, Newman DK (2011) Bioenergetic challenges of microbial iron metabolisms. Trends Microbiol 19:330–340
Canfield DE, Thamdrup B, Hansen JW (1993) The anaerobic degradation of organic matter in Danish coastal sediments: iron reduction, manganese reduction, and sulfate reduction. Geochim Cosmochim Acta 57:3867–3883
Chikuma S, Kasahara R, Kato C, Tamegai H (2007) Bacterial adaptation to high pressure: a respiratory system in the deep-sea bacterium Shewanella violacea DSS12. FEMS Microbiol Lett 267:108–112
Coursolle D, Gralnick JA (2012) Reconstruction of extracellular respiratory pathways for Iron(III) reduction in Shewanella oneidensis strain MR-1. Front Microbiol 3:56
Cruanes MT, Rodgers KK, Sligar SG (1992) Protein electrochemistry at high pressure. J Am Chem Soc 114:9660–9661
Cruanes MT, Drickamer HG, Faulkner LR (1995) Characterization of charge transfer processes in self-assembled monolayers by high-pressure electrochemical techniques. Langmuir 11:4089–4097
Daniel I, Oger P, Winter R (2006) Origins of life and biochemistry under high-pressure conditions. Chem Soc Rev 35:858–875
Edwards MJ, White GF, Norman M, Tome-Fernandez A, Ainsworth E, Shi L, Fredrickson JK, Zachara JM, Butt JN, Richardson DJ (2015) Redox linked flavin sites in extracellular decaheme proteins involved in microbe-mineral electron transfer. Sci Rep 5
El-Naggar MY, Wanger G, Leung KM, Yuzvinsky TD, Southam G, Yang J, Lau WM, Nealson KH, Gorby YA (2010) Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. Proc Natl Acad Sci 107:18127–18131
Fang J, Bazylinski DA (2008) Deep sea geomicrobiology. High-pressure microbiology ASM Press, Washington, DC, pp 237–264
Fang J, Zhang L, Bazylinski DA (2010) Deep-sea piezosphere and piezophiles: geomicrobiology and biogeochemistry. Trends Microbiol 18:413–422
Foustoukos DI, Pérez-Rodríguez I (2015) A continuous culture system for assessing microbial activities in the piezosphere. Appl Environ Microbiol 81:6850–6856
Giovanelli D, Lawrence NS, Compton RG (2004) Electrochemistry at high pressures: a review. Electroanalysis 16:789–810
Gorby YA, Lovley DR (1991) Electron transport in the dissimilatory iron reducer, GS-15. Appl Environ Microbiol 57:867–870
Gorby YA, Yanina S, McLean JS, Rosso KM, Moyles D, Dohnalkova A, Beveridge TJ, Chang IS, Kim BH, Kim KS (2006) Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc Natl Acad Sci 103:11358–11363
Harnisch F, Schröder U (2010) From MFC to MXC: chemical and biological cathodes and their potential for microbial bioelectrochemical systems. Chem Soc Rev 39:4433–4448
Heidelberg JF, Paulsen IT, Nelson KE, Gaidos EJ, Nelson WC, Read TD, Eisen JA, Seshadri R, Ward N, Methe B, Clayton RA, Meyer T, Tsapin A, Scott J, Beanan M, Brinkac L, Daugherty S, DeBoy RT, Dodson RJ, Durkin AS, Haft DH, Kolonay JF, Madupu R, Peterson JD, Umayam LA, White O, Wolf AM, Vamathevan J, Weidman J, Impraim M, Lee K, Berry K, Lee C, Mueller J, Khouri H, Gill J, Utterback TR, McDonald LA, Feldblyum TV, Smith HO, Venter JC, Nealson KH, Fraser CM (2002a) Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nat Biotech 20:1118–1123
Heidelberg JF, Paulsen IT, Nelson KE, Gaidos EJ, Nelson WC, Read TD, Eisen JA, Seshadri R, Ward N, Methe B (2002b) Genome sequence of the dissimilatory metal ion–reducing bacterium Shewanella oneidensis. Nat Biotechnol 20:1118–1123
Hinks J, Wang Y, Poh WH, Donose BC, Thomas AW, Wuertz S, Loo SC, Bazan GC, Kjelleberg S, Mu Y, Seviour T (2014) Modeling cell membrane perturbation by molecules designed for transmembrane electron transfer. Langmuir 30:2429–2440
Hinks J, Poh WH, Chu JJH, Loo JSC, Bazan GC, Hancock LE, Wuertz S (2015a) Oligopolyphenylenevinylene-conjugated oligoelectrolyte membrane insertion molecules selectively disrupt cell envelopes of gram-positive bacteria. Appl Environ Microbiol 81:1949–1958
Hinks J, Wang Y, Matysik A, Kraut R, Kjelleberg S, Mu Y, Bazan GC, Wuertz S, Seviour T (2015b) Increased microbial butanol tolerance by exogenous membrane insertion molecules. ChemSusChem 8:3718–3726
Hinks J, Han EJ, Wang VB, Seviour T, Marsili E, Loo J, Wuertz S (2016) Naphthoquinone glycosides for bioelectroanalytical enumeration of the faecal indicator Escherichia coli. Microb Biotechnol 9(6)
Jackson BE, McInerney MJ (2002) Anaerobic microbial metabolism can proceed close to thermodynamic limits. Nature 415:454–456
Jensen HM, Albers AE, Malley KR, Londer YY, Cohen BE, Helms BA, Weigele P, Groves JT, Ajo-Franklin CM (2010) Engineering of a synthetic electron conduit in living cells. Proc Natl Acad Sci 107:19213–19218
Kim HJ, Park HS, Hyun MS, Chang IS, Kim M, Kim BH (2002) A mediator-less microbial fuel cell using a metal reducing bacterium, Shewanella putrefaciens. Enzyme Microb Technol 30:145–152
Liao L, Xu X-W, Jiang X-W, Wang C-S, Zhang D-S, Ni J-Y, Wu M (2011) Microbial diversity in deep-sea sediment from the cobalt-rich crust deposit region in the Pacific Ocean. FEMS Microbiol Ecol 78:565–585
Logan BE (2008) Microbial fuel cells. Wiley, New York
Logan BE, Hamelers B, Rozendal R, Schröder U, Keller J, Freguia S, Aelterman P, Verstraete W, Rabaey K (2006) Microbial fuel cells: methodology and technology. Environ Sci Technol 40:5181–5192
Lovley DR, Phillips EJP (1988) Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microbiol 54:1472–1480
Lovley DR, Giovannoni SJ, White DC, Champine JE, Phillips E, Gorby YA, Goodwin S (1993) Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch Microbiol 159:336–344
Macdonald AG (1997) Hydrostatic pressure as an environmental factor in life processes. Comp Biochem Physiol A Physiol 116:291–297
Malvankar NS, Vargas M, Nevin KP, Franks AE, Leang C, Kim B-C, Inoue K, Mester T, Covalla SF, Johnson JP (2011) Tunable metallic-like conductivity in microbial nanowire networks. Nat Nanotechnol 6:573–579
Malvankar NS, Tuominen MT, Lovley DR (2012) Comment on “On electrical conductivity of microbial nanowires and biofilms” by SM Strycharz-Glaven, RM Snider, A. Guiseppi-Elie and LM Tender, Energy Environ. Sci., 2011, 4, 4366. Energy Environ Sci 5:6247–6249
Malvankar NS, Vargas M, Nevin K, Tremblay P-L, Evans-Lutterodt K, Nykypanchuk D, Martz E, Tuominen MT, Lovley DR (2015) Structural basis for metallic-like conductivity in microbial nanowires. mBio 6, e00084-15
Meersman F, Daniel I, Bartlett DH, Winter R, Hazael R, McMillain P (2013) High-pressure biochemistry and biophysics. Rev Mineral Geochem 75:607–648
Meyer TE, Tsapin AI, Vandenberghe I, De Smet L, Frishman D, Nealson KH, Cusanovich MA, Van Beeumen JJ (2004) Identification of 42 possible cytochrome c genes in the Shewanella oneidensis genome and characterization of six soluble cytochromes. Omics: J Integr Biol 8:57–77
Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191:144–148
Myers CR, Nealson KH (1988) Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 240
Nealson KH, Myers CR (1992) Microbial reduction of manganese and iron: new approaches to carbon cycling. Appl Environ Microbiol 58:439
Picard A, Daniel I (2013) Pressure as an environmental parameter for microbial life—a review. Biophys Chem 183:30–41
Picard A, Daniel I, Testemale D, Kieffer I, Bleuet P, Cardon H, Oger P (2011) Monitoring microbial redox transformations of metal and metalloid elements under high pressure using in situ X-ray absorption spectroscopy. Geobiology 9:196–204
Picard A, Testemale D, Hazemann J-L, Daniel I (2012) The influence of high hydrostatic pressure on bacterial dissimilatory iron reduction. Geochim Cosmochim Acta 88:120–129
Picard A, Testemale D, Wagenknecht L, Hazael R, Daniel I (2014) Iron reduction by the deep-sea bacterium Shewanella profunda LT13a under subsurface pressure and temperature conditions. Front Microbiol 5
Picard, A., Testemale, D., Wagenknecht, L., Hazael, R., and Daniel, I. (2015) Iron reduction by the deep-sea bacterium Shewanella profunda LT13a under subsurface pressure and temperature conditions, Front Microbiol 5:796
Pirbadian S, Barchinger SE, Leung KM, Byun HS, Jangir Y, Bouhenni RA, Reed SB, Romine MF, Saffarini DA, Shi L, Gorby YA, Golbeck JH, El-Naggar MY (2015) Bacterial Nanowires of Shewanella Oneidensis MR-1 are Outer Membrane and Periplasmic Extensions of the Extracellular Electron Transport Components. Biophys J 108:368a
Potter MC (1911) Electrical effects accompanying the decomposition of organic compounds. Proc Royal Soc London Ser B, Containing Pap Biol Charac 84:260–276
Richardson DJ, Butt JN, Fredrickson JK, Zachara JM, Shi L, Edwards MJ, White G, Baiden N, Gates AJ, Marritt SJ (2012) The ‘porin–cytochrome’model for microbe-to-mineral electron transfer. Mol Microbiol 85:201–212
Roden EE (2003) Fe(III) oxide reactivity toward biological versus chemical reduction. Environ Sci Technol 37:1319–1324
Roller SD, Bennetto HP, Delaney GM, Mason JR, Stirling JL, Thurston CF (1984) Electron-transfer coupling in microbial fuel cells: 1. comparison of redox-mediator reduction rates and respiratory rates of bacteria. J Chem Technol Biotechnol 34:3–12
Roussel EG, Bonavita M-AC, Querellou J, Cragg BA, Webster G, Prieur D, Parkes RJ (2008) Extending the sub-sea-floor biosphere. Science 320:1046
Sachinidis JI, Shalders RD, Tregloan PA (1994) Measurement of redox reaction volumes for iron (III/II) complexes using high-pressure cyclic staircase voltammetry. Half-cell contributions to redox reaction volumes. Inorg Chem 33:6180–6186
Salas EC, Bhartia R, Anderson L, Hug W, Reid RD, Iturrino G, Edwards K (2015) In-situ detection of microbial life in the deep biosphere in igneous ocean crust. Front Microbiol 6:1620
Sato S, Kurihara T, Kawamoto J, Hosokawa M, Sato S, Esaki N (2008) Cold adaptation of eicosapentaenoic acid-less mutant of Shewanella livingstonensis Ac10 involving uptake and remodeling of synthetic phospholipids containing various polyunsaturated fatty acids. Extremophiles 12:753–761
Seviour T, Doyle L, Lauw S, Hinks J, Rice S, Nesatyy V, Webster R, Kjelleberg S, Marsili E (2015) Voltammetric profiling of redox-active metabolites expressed by Pseudomonas aeruginosa for diagnostic purposes. Chem Commun (Cambridge, UK) 51:3789–3792
Slichter C, Drickamer H (1972) Pressure-induced electronic changes in compounds of iron. J Chem Phys 56:2142–2160
Strandberg E, Esteban-Martín S, Ulrich AS, Salgado J (2012) Hydrophobic mismatch of mobile transmembrane helices: merging theory and experiments. Biochim Biophys Acta 1818:1242–1249
Strycharz-Glaven SM, Tender LM (2012) Reply to the ‘Comment on “On electrical conductivity of microbial nanowires and biofilms”’by NS Malvankar, MT Tuominen and DR Lovley, Energy Environ. Sci., 2012, 5. doi:10.1039/c2ee02613a. Energy & Environ Sci 5:6250–6255
Strycharz-Glaven SM, Snider RM, Guiseppi-Elie A, Tender LM (2011) On the electrical conductivity of microbial nanowires and biofilms. Energy Environ Sci 4:4366–4379
Usui K, Hiraki T, Kawamoto J, Kurihara T, Nogi Y, Kato C, Abe F (2012) Eicosapentaenoic acid plays a role in stabilizing dynamic membrane structure in the deep-sea piezophile Shewanella violacea: a study employing high-pressure time-resolved fluorescence anisotropy measurement. Biochimica Et Biophysica Acta-Biomembranes 1818:574–583
Venkateswaran K, Moser DP, Dollhopf ME, Lies DP, Saffarini DA, MacGregor BJ, Ringelberg DB, White DC, Nishijima M, Sano H (1999) Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov. Int J Syst Bacteriol 49:705–724
Wang G, Spivack AJ, D’Hondt S (2010) Gibbs energies of reaction and microbial mutualism in anaerobic deep subseafloor sediments of ODP Site 1226. Geochim Cosmochim Acta 74:3938–3947
Wang VB, Du J, Chen X, Thomas AW, Kirchhofer ND, Garner LE, Maw MT, Poh WH, Hinks J, Wuertz S, Kjelleberg S, Zhang Q, Loo JS, Bazan GC (2013) Improving charge collection in Escherichia coli-carbon electrode devices with conjugated oligoelectrolytes. Phys Chem Chem Phys 15:5867–5872
Watanabe K, Manefield M, Lee M, Kouzuma A (2009) Electron shuttles in biotechnology. Curr Opin Biotechnol 20:633–641
Willey J (2014) Prescott’s microbiology-/Joanne M. Willey, Linda M. Sherwood, Christopher J. Woolverton. MacGraw-Hill, New York
Winter R, Jeworrek C (2009) Effect of pressure on membranes. Soft Matter 5:3157–3173
Wu W, Wang F, Li J, Yang X, Xiao X, Pan Y (2013) Iron reduction and mineralization of deep-sea iron reducing bacterium Shewanella piezotolerans WP3 at elevated hydrostatic pressures. Geobiology 11:593–601
Yan H, Chuang C, Zhugayevych A, Tretiak S, Dahlquist F, Bazan G. 2015. Inter-aromatic distances in Geobacter sulfurreducens pili relevant to biofilm charge transport. Adv Mater (Weinheim, Ger). doi:10.1002/adma.201404167
Yayanos AA, Dietz AS, Van Boxtel R (1981) Obligately barophilic bacterium from the Mariana Trench. Proc Natl Acad Sci 78:5212–5215
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Hinks, J., Zhou, M., Dolfing, J. (2017). Microbial Electron Transport in the Deep Subsurface. In: Chénard, C., Lauro, F. (eds) Microbial Ecology of Extreme Environments. Springer, Cham. https://doi.org/10.1007/978-3-319-51686-8_4
Download citation
DOI: https://doi.org/10.1007/978-3-319-51686-8_4
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-51684-4
Online ISBN: 978-3-319-51686-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)