Unravelling biocomplexity of electroactive biofilms for producing hydrogen from biomass

Lewis, Alex J.; Campa, Maria F.; Hazen, Terry C.; Borole, Abhijeet P.

doi:10.1111/1751-7915.12756

Title: Unravelling biocomplexity of electroactive biofilms for producing hydrogen from biomass

Abstract

Leveraging nature's biocomplexity for solving human problems requires better understanding of the syntrophic relationships in engineered microbiomes developed in bioreactor systems. Understanding the interactions between microbial players within the community will be key to enhancing conversion and production rates from biomass streams. Here we investigate a bioelectrochemical system employing an enriched microbial consortium for conversion of a switchgrass-derived bio-oil aqueous phase (BOAP) into hydrogen via microbial electrolysis (MEC). MECs offer the potential to produce hydrogen in an integrated fashion in biorefinery platforms and as a means of energy storage through decentralized production to supply hydrogen to fuelling stations, as the world strives to move towards cleaner fuels and electricity-mediated transportation. A unique approach combining differential substrate and redox conditions revealed efficient but rate-limiting fermentation of the compounds within BOAP by the anode microbial community through a division of labour strategy combined with multiple levels of syntrophy. Despite the fermentation limitation, the adapted abilities of the microbial community resulted in a high hydrogen productivity of 9.35 L per L-day. Using pure acetic acid as the substrate instead of the biomass-derived stream resulted in a three-fold improvement in productivity. This high rate of exoelectrogenesis signifies the potential commercial feasibility of MEC technology formore » integration in biorefineries.« less

Authors:

Lewis, Alex J. ^[1]; Campa, Maria F. ^[2]; Hazen, Terry C. ^[2];

^[2]

The University of Tennessee, Knoxville TN 37996 USA, Biosciences Division, Oak Ridge National Laboratory, Oak Ridge TN 37831-6226 USA, Bredesen Center for Interdisciplinary Research and Education, The University of Tennessee, Knoxville TN 37996 USA
The University of Tennessee, Knoxville TN 37996 USA, Biosciences Division, Oak Ridge National Laboratory, Oak Ridge TN 37831-6226 USA, Bredesen Center for Interdisciplinary Research and Education, The University of Tennessee, Knoxville TN 37996 USA, Institute for Secure and Sustainable Environments, The University of Tennessee, Knoxville TN 37996 USA

Publication Date:: Tue Jul 11 00:00:00 EDT 2017

Research Org.:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:: USDOE Office of Energy Efficiency and Renewable Energy (EERE), Sustainable Transportation Office. Bioenergy Technologies Office (BETO); USDOE Office of Science (SC)

OSTI Identifier:: 1369105

Alternate Identifier(s):: OSTI ID: 1369106; OSTI ID: 1408603; OSTI ID: 1479376

Grant/Contract Number:: AC05-00OR22725; AC02-05CH11231

Resource Type:: Published Article

Journal Name:: Microbial Biotechnology (Online)

Additional Journal Information:: Journal Name: Microbial Biotechnology (Online); Journal ID: ISSN 1751-7915

Publisher:: Wiley

Country of Publication:: United Kingdom

Language:: English

Subject:: 09 BIOMASS FUELS

Citation Formats


                    Lewis, Alex J., Campa, Maria F., Hazen, Terry C., and Borole, Abhijeet P. Unravelling biocomplexity of electroactive biofilms for producing hydrogen from biomass.  United Kingdom: N. p., 2017. 
Web.  doi:10.1111/1751-7915.12756.

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                    Lewis, Alex J., Campa, Maria F., Hazen, Terry C., & Borole, Abhijeet P. Unravelling biocomplexity of electroactive biofilms for producing hydrogen from biomass.  United Kingdom.  https://doi.org/10.1111/1751-7915.12756

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                    Lewis, Alex J., Campa, Maria F., Hazen, Terry C., and Borole, Abhijeet P. Tue .  
"Unravelling biocomplexity of electroactive biofilms for producing hydrogen from biomass".  United Kingdom.  https://doi.org/10.1111/1751-7915.12756.

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@article{osti_1369105,

  title        = {Unravelling biocomplexity of electroactive biofilms for producing hydrogen from biomass},

  author       = {Lewis, Alex J. and Campa, Maria F. and Hazen, Terry C. and Borole, Abhijeet P.},

  abstractNote = {Leveraging nature's biocomplexity for solving human problems requires better understanding of the syntrophic relationships in engineered microbiomes developed in bioreactor systems. Understanding the interactions between microbial players within the community will be key to enhancing conversion and production rates from biomass streams. Here we investigate a bioelectrochemical system employing an enriched microbial consortium for conversion of a switchgrass-derived bio-oil aqueous phase (BOAP) into hydrogen via microbial electrolysis (MEC). MECs offer the potential to produce hydrogen in an integrated fashion in biorefinery platforms and as a means of energy storage through decentralized production to supply hydrogen to fuelling stations, as the world strives to move towards cleaner fuels and electricity-mediated transportation. A unique approach combining differential substrate and redox conditions revealed efficient but rate-limiting fermentation of the compounds within BOAP by the anode microbial community through a division of labour strategy combined with multiple levels of syntrophy. Despite the fermentation limitation, the adapted abilities of the microbial community resulted in a high hydrogen productivity of 9.35 L per L-day. Using pure acetic acid as the substrate instead of the biomass-derived stream resulted in a three-fold improvement in productivity. This high rate of exoelectrogenesis signifies the potential commercial feasibility of MEC technology for integration in biorefineries.},

  doi          = {10.1111/1751-7915.12756},

  journal      = {Microbial Biotechnology (Online)},

  number       = ,

  volume       = ,

  place        = {United Kingdom},

  year         = {Tue Jul 11 00:00:00 EDT 2017},

  month        = {Tue Jul 11 00:00:00 EDT 2017}

}

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Title: Unravelling biocomplexity of electroactive biofilms for producing hydrogen from biomass

Abstract

Citation Formats

Engineering inhibitor tolerance for the production of biorenewable fuels and chemicals journal, October 2011

Enhanced H2 production from corn stalk by integrating dark fermentation and single chamber microbial electrolysis cells with double anode arrangement journal, June 2014

Performance of a semi-pilot tubular microbial electrolysis cell (MEC) under several hydraulic retention times and applied voltages journal, October 2013

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Physiology and tactic response of the phototrophic consortium " Chlorochromatium aggregatum " journal, February 1998

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Microbial Fuel Cells and Microbial Electrolyzers journal, January 2015

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Syntrophic interactions among anode respiring bacteria (ARB) and Non-ARB in a biofilm anode: electron balances journal, June 2009

Combining microbial cultures for efficient production of electricity from butyrate in a microbial electrochemical cell journal, October 2014

Microbial degradation of furanic compounds: biochemistry, genetics, and impact journal, October 2011

Process Design and Economics for the Conversion of Lignocellulosic Biomass to Hydrocarbon Fuels: Fast Pyrolysis and Hydrotreating Bio-oil Pathway report, November 2013

Comparison of anode bacterial communities and performance in microbial fuel cells with different electron donors journal, September 2007

Cloning of a novel levoglucosan kinase gene from Lipomyces starkeyi and its expression in Escherichia coli journal, April 2009

Hydrogen production from switchgrass via an integrated pyrolysis–microbial electrolysis process journal, November 2015

Electron and Carbon Balances in Microbial Fuel Cells Reveal Temporary Bacterial Storage Behavior During Electricity Generation journal, April 2007

Upgrading of straw hydrolysate for production of hydrogen and phenols in a microbial electrolysis cell (MEC) journal, December 2010

Developing symbiotic consortia for lignocellulosic biofuel production journal, January 2012

Relieving the fermentation inhibition enables high electron recovery from landfill leachate in a microbial electrolysis cell journal, January 2016

Investigation of an Acetate-Fed Denitrifying Microbial Community by Stable Isotope Probing, Full-Cycle rRNA Analysis, and Fluorescent In Situ Hybridization-Microautoradiography journal, December 2005

Syntrophic Processes Drive the Conversion of Glucose in Microbial Fuel Cell Anodes journal, November 2008

Methods for Pretreatment of Lignocellulosic Biomass for Efficient Hydrolysis and Biofuel Production journal, April 2009

Overview biohydrogen technologies and application in fuel cell technology journal, December 2016

Hydrogen production using biocathode single-chamber microbial electrolysis cells fed by molasses wastewater at low temperature journal, November 2014

A co-fermentation strategy to consume sugar mixtures effectively journal, January 2008

Understanding the impact of flow rate and recycle on the conversion of a complex biorefinery stream using a flow-through microbial electrolysis cell journal, December 2016

Multiple paths of electron flow to current in microbial electrolysis cells fed with low and high concentrations of propionate journal, March 2016

Iron and Manganese in Anaerobic Respiration: Environmental Significance, Physiology, and Regulation journal, October 1994

Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms journal, March 2012

A review on dark fermentative biohydrogen production from organic biomass: Process parameters and use of by-products journal, April 2015

Engineering ethanologenic Escherichia coli for levoglucosan utilization journal, September 2011

Bioelectrochemical Systems, Energy Production and Electrosynthesis journal, January 2012

Methanogenesis versus Electrogenesis: Morphological and Phylogenetic Comparisons of Microbial Communities journal, February 2008

Improving power production in acetate-fed microbial fuel cells via enrichment of exoelectrogenic organisms in flow-through systems journal, December 2009

Microbial population and functional dynamics associated with surface potential and carbon metabolism journal, December 2013

Hydrogen production from cellulose in a two-stage process combining fermentation and electrohydrogenesis journal, August 2009

Engineering inhibitor tolerance for the production of biorenewable fuels and chemicals
journal, October 2011

Enhanced H2 production from corn stalk by integrating dark fermentation and single chamber microbial electrolysis cells with double anode arrangement
journal, June 2014

Performance of a semi-pilot tubular microbial electrolysis cell (MEC) under several hydraulic retention times and applied voltages
journal, October 2013

Performance of a pilot-scale continuous flow microbial electrolysis cell fed winery wastewater
journal, February 2011

Dissimilatory Metal Reduction
journal, October 1993

Improving energy efficiency and enabling water recycling in biorefineries using bioelectrochemical systems†
journal, January 2011

Physiology and tactic response of the phototrophic consortium " Chlorochromatium aggregatum "
journal, February 1998

Biotransformation of Furanic and Phenolic Compounds with Hydrogen Gas Production in a Microbial Electrolysis Cell
journal, November 2015

Microbial Fuel Cells and Microbial Electrolyzers
journal, January 2015

Biohydrogen Production from Lignocellulosic Biomass: Technology and Sustainability
journal, November 2015

Isolation of the exoelectrogenic denitrifying bacterium Comamonas denitrificans based on dilution to extinction
journal, September 2009

The electric picnic: synergistic requirements for exoelectrogenic microbial communities
journal, June 2011

The evolution of social behavior in microorganisms
journal, April 2001

Diversity and dynamics of microbial communities in engineered environments and their implications for process stability
journal, June 2003

Contextualizing context for synthetic biology - identifying causes of failure of synthetic biological systems
journal, May 2012

Coupling dark fermentation and microbial electrolysis to enhance bio-hydrogen production from agro-industrial wastewaters and by-products in a bio-refinery framework
journal, January 2017

Bioelectrochemical Systems: An Outlook for Practical Applications
journal, June 2012

Electricity generation from cellulose by rumen microorganisms in microbial fuel cells
journal, January 2007

Hydrogen production and COD elimination rate in a continuous microbial electrolysis cell: The influence of hydraulic retention time and applied voltage
journal, February 2012

Metabolic and practical considerations on microbial electrosynthesis
journal, June 2011

Better together: engineering and application of microbial symbioses
journal, December 2015

Hydrogen production with effluent from an ethanol–H2-coproducing fermentation reactor using a single-chamber microbial electrolysis cell
journal, June 2009

A novel metatranscriptomic approach to identify gene expression dynamics during extracellular electron transfer
journal, March 2013

Isotope array analysis of Rhodocyclales uncovers functional redundancy and versatility in an activated sludge
journal, July 2009

Identification, characterization of levoglucosan kinase, and cloning and expression of levoglucosan kinase cDNA from Aspergillus niger CBX-209 in Escherichia coli
journal, October 2002

Microbial electrolysis cell to treat hydrothermal liquefied wastewater from cornstalk and recover hydrogen: Degradation of organic compounds and characterization of microbial community
journal, February 2016

Integrated hydrogen production process from cellulose by combining dark fermentation, microbial fuel cells, and a microbial electrolysis cell
journal, March 2011

Microbial Electrolysis Cells for High Yield Hydrogen Gas Production from Organic Matter
journal, December 2008

Metabolism of levoglucosan(1,6-anhydro-.BETA.-D-glucopyranose) in microorganisms.
journal, January 1991

Syntrophic interactions among anode respiring bacteria (ARB) and Non-ARB in a biofilm anode: electron balances
journal, June 2009

Combining microbial cultures for efficient production of electricity from butyrate in a microbial electrochemical cell
journal, October 2014

Microbial degradation of furanic compounds: biochemistry, genetics, and impact
journal, October 2011

Process Design and Economics for the Conversion of Lignocellulosic Biomass to Hydrocarbon Fuels: Fast Pyrolysis and Hydrotreating Bio-oil Pathway
report, November 2013

Comparison of anode bacterial communities and performance in microbial fuel cells with different electron donors
journal, September 2007

Cloning of a novel levoglucosan kinase gene from Lipomyces starkeyi and its expression in Escherichia coli
journal, April 2009

Hydrogen production from switchgrass via an integrated pyrolysis–microbial electrolysis process
journal, November 2015

Electron and Carbon Balances in Microbial Fuel Cells Reveal Temporary Bacterial Storage Behavior During Electricity Generation
journal, April 2007

Upgrading of straw hydrolysate for production of hydrogen and phenols in a microbial electrolysis cell (MEC)
journal, December 2010

Developing symbiotic consortia for lignocellulosic biofuel production
journal, January 2012

Relieving the fermentation inhibition enables high electron recovery from landfill leachate in a microbial electrolysis cell
journal, January 2016

Investigation of an Acetate-Fed Denitrifying Microbial Community by Stable Isotope Probing, Full-Cycle rRNA Analysis, and Fluorescent In Situ Hybridization-Microautoradiography
journal, December 2005

Syntrophic Processes Drive the Conversion of Glucose in Microbial Fuel Cell Anodes
journal, November 2008

Methods for Pretreatment of Lignocellulosic Biomass for Efficient Hydrolysis and Biofuel Production
journal, April 2009

Overview biohydrogen technologies and application in fuel cell technology
journal, December 2016

Hydrogen production using biocathode single-chamber microbial electrolysis cells fed by molasses wastewater at low temperature
journal, November 2014

A co-fermentation strategy to consume sugar mixtures effectively
journal, January 2008

Understanding the impact of flow rate and recycle on the conversion of a complex biorefinery stream using a flow-through microbial electrolysis cell
journal, December 2016

Multiple paths of electron flow to current in microbial electrolysis cells fed with low and high concentrations of propionate
journal, March 2016

Iron and Manganese in Anaerobic Respiration: Environmental Significance, Physiology, and Regulation
journal, October 1994

Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
journal, March 2012

A review on dark fermentative biohydrogen production from organic biomass: Process parameters and use of by-products
journal, April 2015

Engineering ethanologenic Escherichia coli for levoglucosan utilization
journal, September 2011

Bioelectrochemical Systems, Energy Production and Electrosynthesis
journal, January 2012

Methanogenesis versus Electrogenesis: Morphological and Phylogenetic Comparisons of Microbial Communities
journal, February 2008

Improving power production in acetate-fed microbial fuel cells via enrichment of exoelectrogenic organisms in flow-through systems
journal, December 2009

Microbial population and functional dynamics associated with surface potential and carbon metabolism
journal, December 2013

Hydrogen production from cellulose in a two-stage process combining fermentation and electrohydrogenesis
journal, August 2009