The geochemical fingerprint of microbial long-distance electron transport in the seafloor

Recently, a novel “electrogenic” type of sulfur oxidation has been documented in marine sediments, whereby long filamentous cable bacteria are generating electrical currents over centimeter-scale distances. Here we propose a numerical model description that is capable of quantitatively simulating the solute depth profiles and biogeochemical transformations in such electro-active marine sediments. The model is based on a conventional reactive transport description of marine sediments, which is extended with a new model formulation for the long-distance electron transport induced by the cable bacteria. The mechanism of electron hopping is implemented to describe the electron transport along the longitudinal axis of the microbial filaments. We demonstrate that this model is capable of reproducing the observed geochemical fingerprint of electrogenic sulfur oxidation, which consists of a characteristic set of O2, pH and H2S depth profiles. Our simulation results suggest that the cable bacteria must have a high affinity for both oxygen and sulfide, and that intensive cryptic sulfur cycling takes place within the suboxic zone. A sensitivity analysis shows how electrogenic sulfur oxidation strongly impacts the biogeochemical cycling of sulfur, iron, carbon and calcium in marine sediments.

[1]  Anthony Guiseppi-Elie,et al.  On the electrical conductivity of microbial nanowires and biofilms , 2011 .

[2]  R. Glud Oxygen dynamics of marine sediments , 2008 .

[3]  K. Nealson Geomicrobiology: Sediment reactions defy dogma , 2010, Nature.

[4]  G. Munhoven Mathematics of the total alkalinity-pH equation - pathway to robust and universal solution algorithms: the SolveSAPHE package v1.0.1 , 2013 .

[5]  E. Hill,et al.  Microbial nanowires: Is the subsurface “hardwired”? , 2007 .

[6]  J. Middelburg,et al.  Carbonate compensation dynamics , 2010 .

[7]  Leonard M. Tender,et al.  Reply to the ‘Comment on “On electrical conductivity of microbial nanowires and biofilms”’ by N. S. Malvankar, M. T. Tuominen and D. R. Lovley, Energy Environ. Sci., 2012, 5, DOI: 10.1039/c2ee02613a , 2012 .

[8]  David Archer,et al.  A data-driven model of the global calcite lysocline , 1996 .

[9]  D. Canfield,et al.  Systematics and Phylogeny , 2005 .

[10]  John M. Zachara,et al.  Structure of a bacterial cell surface decaheme electron conduit , 2011, Proceedings of the National Academy of Sciences.

[11]  Kazuya Watanabe,et al.  Respiratory interactions of soil bacteria with (semi)conductive iron-oxide minerals. , 2010, Environmental microbiology.

[12]  B. Jørgensen Mineralization of organic matter in the sea bed—the role of sulphate reduction , 1982, Nature.

[13]  David N Beratan,et al.  Physical constraints on charge transport through bacterial nanowires. , 2012, Faraday discussions.

[14]  E. Zetsche,et al.  Natural occurrence of microbial sulphur oxidation by long-range electron transport in the seafloor , 2014, The ISME Journal.

[15]  J. Middelburg,et al.  AquaEnv : An Aqua tic Acid – Base Modelling Env ironment in R , 2010 .

[16]  Bernard P. Boudreau,et al.  Modeling reactive transport in sediments subject to bioturbation and compaction , 2005 .

[17]  F. Besenbacher,et al.  Filamentous bacteria transport electrons over centimetre distances , 2012, Nature.

[18]  L. Nielsen,et al.  Impact of Bacterial NO3− Transport on Sediment Biogeochemistry , 2005, Applied and Environmental Microbiology.

[19]  N. Revsbech,et al.  Colorless Sulfur Bacteria, Beggiatoa spp. and Thiovulum spp., in O2 and H2S Microgradients , 1983, Applied and environmental microbiology.

[20]  Jessika Schulze,et al.  The Structure Of The Novel , 2016 .

[21]  Alice Dohnalkova,et al.  Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Nigel A. Surridge,et al.  Charge transport in electroactive polymers consisting of fixed molecular Redox sites , 1990 .

[23]  L. Nielsen,et al.  Electric potential microelectrode for studies of electrobiogeophysics , 2014 .

[24]  W. Davison,et al.  Soluble iron sulfide species in natural waters: Reappraisal of their stoichiometry and stability constants , 1999, Aquatic Sciences.

[25]  B. Boudreau Diagenetic models and their implementation , 1997 .

[26]  T. Mehta,et al.  Extracellular electron transfer via microbial nanowires , 2005, Nature.

[27]  C. Reimers,et al.  CaCO3 dissolution in California continental margin sediments: The influence of organic matter remineralization , 1997 .

[28]  J. Middelburg,et al.  A step-by-step procedure for pH model construction in aquatic systems (THESIS VERSION) ) , 2007 .

[29]  Karline Soetaert,et al.  AquaEnv: An Aquatic Acid–Base Modelling Environment in R , 2010 .

[30]  Carlo H. R. Heip,et al.  Reactive transport in surface sediments. II. Media: an object-oriented problem-solving environment for early diagenesis , 2003 .

[31]  Yifeng Wang,et al.  Cycling of iron and manganese in surface sediments; a general theory for the coupled transport and reaction of carbon, oxygen, nitrogen, sulfur, iron, and manganese , 1996 .

[32]  R. Aller 8.11 – Sedimentary Diagenesis, Depositional Environments, and Benthic Fluxes , 2014 .

[33]  D. Rickard The solubility of FeS , 2006 .

[34]  A. Revil,et al.  Mapping electron sources and sinks in a marine biogeobattery , 2014 .

[35]  Bernard P. Boudreau,et al.  A method-of-lines code for carbon and nutrient diagenesis in aquatic sediments , 1996 .

[36]  Pierre Regnier,et al.  Quantitative interpretation of pH distributions in aquatic sediments: A reaction-transport modeling approach , 2005 .

[37]  Derek R. Lovley,et al.  Comment on “On electrical conductivity of microbial nanowires and biofilms” by S. M. Strycharz-Glaven, R. M. Snider, A. Guiseppi-Elie and L. M. Tender, Energy Environ. Sci., 2011, 4, 4366 , 2012 .

[38]  J. Savéant,et al.  Electron transfer through redox polymer films , 1980 .

[39]  Karline Soetaert,et al.  Reactive transport in aquatic ecosystems: Rapid model prototyping in the open source software R , 2012, Environ. Model. Softw..

[40]  B. Jørgensen,et al.  Succession of cable bacteria and electric currents in marine sediment , 2014, The ISME Journal.

[41]  H. Gray,et al.  Long-range electron transfer. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Korneel Rabaey,et al.  Conversion of Wastes into Bioelectricity and Chemicals by Using Microbial Electrochemical Technologies , 2012, Science.

[43]  Peter Berg,et al.  Dynamic Modeling of Early Diagenesis and Nutrient Cycling. A Case Study in an Artic Marine Sediment , 2003 .

[44]  D. Hammond,et al.  Early oxidation of organic matter in pelagic sediments of the eastern equatorial Atlantic: suboxic diagenesis , 1979 .

[45]  A. F. Hofmann A step-by-step procedure for pH model construction in aquatic systems (DATASET) , 2009 .

[46]  Derek R Lovley,et al.  Extracellular electron transfer: wires, capacitors, iron lungs, and more , 2008, Geobiology.

[47]  R. Aller,et al.  Complete oxidation of solid phase sulfides by manganese and bacteria in anoxic marine sediments , 1988 .

[48]  A. F. Hofmann,et al.  The effect of biogeochemical processes on pH , 2007 .

[49]  D. Canfield,et al.  Aquatic geomicrobiology. , 2005, Advances in marine biology.

[50]  F. Meysman,et al.  Alkalinity production in intertidal sands intensified by lugworm bioirrigation , 2014, Estuarine, coastal and shelf science.

[51]  Karline Soetaert,et al.  Solving Differential Equations in R , 2012 .

[52]  F. Millero,et al.  Dissociation constants of carbonic acid in seawater as a function of salinity and temperature , 2006 .

[53]  Bernard P. Boudreau,et al.  The diffusive tortuosity of fine-grained unlithified sediments , 1996 .

[54]  N. Duke,et al.  Structure of a novel dodecaheme cytochrome c from Geobacter sulfurreducens reveals an extended 12 nm protein with interacting hemes. , 2011, Journal of structural biology.

[55]  D. Canfield,et al.  Pathways of organic carbon oxidation in three continental margin sediments. , 1993, Marine geology.

[56]  Karline Soetaert,et al.  A model of early diagenetic processes from the shelf to abyssal depths , 1996 .

[57]  L. Nielsen,et al.  Electric currents couple spatially separated biogeochemical processes in marine sediment , 2010, Nature.

[58]  D. Lovley,et al.  Centimeter-long electron transport in marine sediments via conductive minerals , 2014, The ISME Journal.

[59]  B. Hales,et al.  Calcite dissolution in sediments of the Ontong‐Java Plateau: In situ measurements of pore water O2 and pH , 1996 .

[60]  A. Revil,et al.  Sulfur, iron-, and calcium cycling associated with natural electric currents running through marine sediment , 2012 .

[61]  I. McKelvie,et al.  The role of alkalinity generation in controlling the fluxes of CO 2 during exposure and inundation on tidal flats , 2012 .

[62]  T. D. Yuzvinsky,et al.  Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1 , 2010, Proceedings of the National Academy of Sciences.

[63]  B. Jørgensen The sulfur cycle of a coastal marine sediment (Limfjorden, Denmark)1 , 1977 .

[64]  A. Borges,et al.  Enhanced ocean carbon storage from anaerobic alkalinity generation in coastal sediments , 2008 .