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Title: Harnessing a methane‐fueled, sediment‐free mixed microbial community for utilization of distributed sources of natural gas

Journal Article · · Biotechnology and Bioengineering
DOI:https://doi.org/10.1002/bit.26576· OSTI ID:1429516
 [1];  [2]; ORCiD logo [1];  [3];  [3];  [4];  [1]
  1. Department of Organismic and Evolutionary Biology Harvard University Cambridge Massachusetts
  2. Department of Organismic and Evolutionary Biology Harvard University Cambridge Massachusetts, Department of Chemical Engineering Massachusetts Institute of Technology Cambridge Massachusetts
  3. Department of Human Evolutionary Biology Harvard University Cambridge Massachusetts
  4. Department of Chemical Engineering Massachusetts Institute of Technology Cambridge Massachusetts

Abstract Harnessing the metabolic potential of uncultured microbial communities is a compelling opportunity for the biotechnology industry, an approach that would vastly expand the portfolio of usable feedstocks. Methane is particularly promising because it is abundant and energy‐rich, yet the most efficient methane‐activating metabolic pathways involve mixed communities of anaerobic methanotrophic archaea and sulfate reducing bacteria. These communities oxidize methane at high catabolic efficiency and produce chemically reduced by‐products at a comparable rate and in near‐stoichiometric proportion to methane consumption. These reduced compounds can be used for feedstock and downstream chemical production, and at the production rates observed in situ they are an appealing, cost‐effective prospect. Notably, the microbial constituents responsible for this bioconversion are most prominent in select deep‐sea sediments, and while they can be kept active at surface pressures, they have not yet been cultured in the lab. In an industrial capacity, deep‐sea sediments could be periodically recovered and replenished, but the associated technical challenges and substantial costs make this an untenable approach for full‐scale operations. In this study, we present a novel method for incorporating methanotrophic communities into bioindustrial processes through abstraction onto low mass, easily transportable carbon cloth artificial substrates. Using Gulf of Mexico methane seep sediment as inoculum, optimal physicochemical parameters were established for methane‐oxidizing, sulfide‐generating mesocosm incubations. Metabolic activity required >∼40% seawater salinity, peaking at 100% salinity and 35 °C. Microbial communities were successfully transferred to a carbon cloth substrate, and rates of methane‐dependent sulfide production increased more than threefold per unit volume. Phylogenetic analyses indicated that carbon cloth‐based communities were substantially streamlined and were dominated by Desulfotomaculum geothermicum . Fluorescence in situ hybridization microscopy with carbon cloth fibers revealed a novel spatial arrangement of anaerobic methanotrophs and sulfate reducing bacteria suggestive of an electronic coupling enabled by the artificial substrate. This system: 1) enables a more targeted manipulation of methane‐activating microbial communities using a low‐mass and sediment‐free substrate; 2) holds promise for the simultaneous consumption of a strong greenhouse gas and the generation of usable downstream products; and 3) furthers the broader adoption of uncultured, mixed microbial communities for biotechnological use.

Research Organization:
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Sponsoring Organization:
USDOE Advanced Research Projects Agency - Energy (ARPA-E)
Grant/Contract Number:
AR0000433
OSTI ID:
1429516
Alternate ID(s):
OSTI ID: 1434364; OSTI ID: 1557841
Journal Information:
Biotechnology and Bioengineering, Journal Name: Biotechnology and Bioengineering Vol. 115 Journal Issue: 6; ISSN 0006-3592
Publisher:
Wiley Blackwell (John Wiley & Sons)Copyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 3 works
Citation information provided by
Web of Science

References (99)

In-silico-driven metabolic engineering of Pseudomonas putida for enhanced production of poly-hydroxyalkanoates journal January 2013
Spectrophotometric Determination Of Hydrogen Sulfide In Natural Waters journal May 1969
Bacterial Adhesion on Commercially Pure Titanium and Zirconium Oxide Disks: An In Vivo Human Study journal February 2004
The anaerobic oxidation of methane and sulfate reduction in sediments from Gulf of Mexico cold seeps journal May 2004
Industrial biomanufacturing: The future of chemical production journal January 2017
Evidence for Anaerobic CH 4 Oxidation in Freshwater Peatlands journal December 2007
Candidatus Desulfofervidus auxilii, a hydrogenotrophic sulfate-reducing bacterium involved in the thermophilic anaerobic oxidation of methane : The partner bacterium in thermophilic methanotrophy journal April 2016
16S ribosomal DNA amplification for phylogenetic study. journal January 1991
Microbial synthesis of n-butanol, isobutanol, and other higher alcohols from diverse resources journal May 2013
Harnessing the power of microbial autotrophy journal September 2016
Methane-driven microbial fuel cells recover energy and mitigate dissolved methane emissions from anaerobic effluents journal January 2018
Methane Leaks from North American Natural Gas Systems journal February 2014
Bioremediation of acid mine water using facultatively methylotrophic metal-tolerant sulfate-reducing bacteria journal February 1997
A bridge to nowhere: methane emissions and the greenhouse gas footprint of natural gas journal May 2014
Diversity and dynamics of microbial communities in engineered environments and their implications for process stability journal June 2003
Bioreactor performance and methanogenic population dynamics in a low-temperature (5–18°C) anaerobic fixed-bed reactor journal January 2012
Biogeochemical processes and microbial diversity of the Gullfaks and Tommeliten methane seeps (Northern North Sea) journal January 2008
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample journal June 2010
Effects of Solution Chemistry on Bacterial Adhesion with Phyllosilicates and Goethite Explained by the Extended DLVO Theory journal March 2014
Metabolic engineering in chemolithoautotrophic hosts for the production of fuels and chemicals journal July 2015
Natural gas origin, composition, and processing: A review journal August 2016
Single cell activity reveals direct electron transfer in methanotrophic consortia journal September 2015
Embracing the unknown: disentangling the complexities of the soil microbiome journal August 2017
Geological, geochemical, and microbiological heterogeneity of the seafloor around methane vents in the Eel River Basin, offshore California journal May 2004
Anaerobic oxidation of methane above gas hydrates at Hydrate Ridge, NE Pacific Ocean journal January 2003
Assessing methanotrophy and carbon fixation for biofuel production by Methanosarcina acetivorans journal January 2016
Metabolic Capabilities of Microorganisms Involved in and Associated with the Anaerobic Oxidation of Methane journal February 2016
Carbonate-hosted methanotrophy represents an unrecognized methane sink in the deep sea journal October 2014
A fast and simple turbidimetric method for the determination of sulfate in sulfate-reducing bacterial cultures journal August 2000
Temperature dependence of microbial degradation of organic matter in marine sediments:polysaccharide hydrolysis, oxygen consumption, and sulfate reduction journal January 1998
Prokaryotic Osmoregulation: Genetics and Physiology journal October 1991
Desulfotomaculum spp. and related gram-positive sulfate-reducing bacteria in deep subsurface environments journal January 2013
Bacterial community segmentation facilitates the prediction of ecosystem function along the coast of the western Antarctic Peninsula journal January 2017
Engineering the iron-oxidizing chemolithoautotroph Acidithiobacillus ferrooxidans for biochemical production : Metabolic Engineering of journal October 2015
Temperature dependence and rates of sulfate reduction in cold sediments of svalbard, arctic ocean journal April 1998
Growth and Population Dynamics of Anaerobic Methane-Oxidizing Archaea and Sulfate-Reducing Bacteria in a Continuous-Flow Bioreactor journal July 2005
Microbial eukaryotic distributions and diversity patterns in a deep-sea methane seep ecosystem: Microbial eukaryotic patterns in deep-sea methane seeps journal January 2016
Effect of process temperature on bacterial and archaeal communities in two methanogenic bioreactors treating organic household waste: Temperature effects on microbial communities in bioreactors journal March 2007
Microbial diversity in sediments associated with surface-breaching gas hydrate mounds in the Gulf of Mexico journal October 2003
Growth and Methane Oxidation Rates of Anaerobic Methanotrophic Archaea in a Continuous-Flow Bioreactor journal September 2003
Tracing the slow growth of anaerobic methane-oxidizing communities by 15N-labelling techniques: 15N-labelling of anaerobic methanotrophs journal March 2008
Evaluation and optimization of PCR primers for selective and quantitative detection of marine ANME subclusters involved in sulfate-dependent anaerobic methane oxidation journal June 2017
Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. journal January 1988
Carbon cloth stimulates direct interspecies electron transfer in syntrophic co-cultures journal December 2014
Analysis of methane and sulfate flux in methane-charged sediments from the Mississippi Canyon, Gulf of Mexico journal November 2008
Thermophilic anaerobic oxidation of methane by marine microbial consortia journal June 2011
Formation processes of framboidal pyrite journal January 1997
Autoendoliths: a distinct type of rock-hosted microbial life journal April 2015
Surveys, simulation and single-cell assays relate function and phylogeny in a lake ecosystem journal August 2016
Process design for microbial plastic factories: metabolic engineering of polyhydroxyalkanoates journal October 2003
Anaerobic Oxidation of Methane in Sediments of Lake Constance, an Oligotrophic Freshwater Lake journal May 2011
Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria journal October 2015
Reversing methanogenesis to capture methane for liquid biofuel precursors journal January 2016
Spatial Structure and Activity of Sedimentary Microbial Communities Underlying a Beggiatoa spp. Mat in a Gulf of Mexico Hydrocarbon Seep journal January 2010
Brief Overview of the Partial Oxidation of Methane to Synthesis Gas journal January 2003
Effective bioremediation of Cadmium (II), nickel (II), and chromium (VI) in a marine environment by using Desulfovibrio desulfuricans journal September 2015
Measurement of Diversity journal April 1949
Decoupling of DAMO archaea from DAMO bacteria in a methane-driven microbial fuel cell journal March 2017
In vitro cell growth of marine archaeal-bacterial consortia during anaerobic oxidation of methane with sulfate journal January 2007
Filamentous bacteria transport electrons over centimetre distances journal October 2012
Global dispersion and local diversification of the methane seep microbiome journal March 2015
Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction journal February 2016
Bioremediation of chromate: thermodynamic analysis of the effects of Cr(VI) on sulfate-reducing bacteria journal November 2002
Microbial abundance and diversity patterns associated with sediments and carbonates from the methane seep environments of Hydrate Ridge, OR journal October 2014
Effects of Temperature and Pressure on Sulfate Reduction and Anaerobic Oxidation of Methane in Hydrothermal Sediments of Guaymas Basin journal February 2004
Correlation of mRNA and protein in complex biological samples journal October 2009
Abundance and spatial organization of Gram-negative sulfate-reducing bacteria in activated sludge investigated by in situ probing with specific 16S rRNA targeted oligonucleotides journal January 1998
Theoretical analysis of natural gas recovery from marginal wells with a deep well reactor journal April 2017
Oxidation of hydrogen sulfide byThiobacillus denitrificans: Desulfurization of natural gas journal February 1987
Diverse sulfate-reducing bacteria of the Desulfosarcina/Desulfococcus clade are the key alkane degraders at marine seeps journal April 2014
Search and clustering orders of magnitude faster than BLAST journal August 2010
Unexplored Archaeal Diversity in the Great Ape Gut Microbiome journal February 2017
Polyhydroxyalkanoates, challenges and opportunities journal December 2014
UPARSE: highly accurate OTU sequences from microbial amplicon reads journal August 2013
Long-term performance of sediment microbial fuel cells with multiple anodes journal August 2017
Polyhydroxyalkanoate (PHA) Accumulation in Sulfate-Reducing Bacteria and Identification of a Class III PHA Synthase (PhaEC) in Desulfococcus multivorans journal August 2004
Bacterial synthesis of biodegradable polyhydroxyalkanoates journal June 2007
Methane Seep Carbonates Host Distinct, Diverse, and Dynamic Microbial Assemblages journal December 2015
High rates of anaerobic methanotrophy at low sulfate concentrations with implications for past and present methane levels: Methanotrophy at low sulfate levels journal January 2011
Desulfotomaculum geothermicum sp. nov., a thermophilic, fatty acid-degrading, sulfate-reducing bacterium isolated with H2 from geothermal ground water journal January 1988
Rethinking biological activation of methane and conversion to liquid fuels journal April 2014
Methane activation: the past and future journal January 2014
Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples: Primers for marine microbiome studies journal October 2015
Consumption of Methane and CO2 by Methanotrophic Microbial Mats from Gas Seeps of the Anoxic Black Sea journal February 2007
Thermophilic archaea activate butane via alkyl-coenzyme M formation journal October 2016
A marine microbial consortium apparently mediating anaerobic oxidation of methane journal October 2000
Characterization of endogenous promoters for control of recombinant gene expression in Acidithiobacillus ferrooxidans : Endogenous Promoters for Use in journal May 2017
Bacterial diversity promotes community stability and functional resilience after perturbation journal March 2005
Anaerobic oxidation of methane associated with sulfate reduction in a natural freshwater gas source journal December 2015
Growth of Syntrophic Propionate-Oxidizing Bacteria with Fumarate in the Absence of Methanogenic Bacteria journal January 1993
Bioremediation of an industrial acid mine water by metal-tolerant sulphate-reducing bacteria journal September 2001
Deep-Sea Archaea Fix and Share Nitrogen in Methane-Consuming Microbial Consortia journal October 2009
The ecology and biotechnology of sulphate-reducing bacteria journal May 2008
Organic loading rate shock impact on operation and microbial communities in different anaerobic fixed-bed reactors journal July 2013
Temperature dependence of metabolic rates for microbial growth, maintenance, and survival journal March 2004
Metabolic engineering of Methanosarcina acetivorans for lactate production from methane : Anaerobic Lactate Production From Methane journal November 2016
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms journal March 2012
Methane-derived carbonates and authigenic pyrite from the northwestern Black Sea journal June 2001
Aerobic and anaerobic metabolism of squalene by a denitrifying bacterium isolated from marine sediment journal October 2002