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

Abstract

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 seepmore » 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.« less

Authors:
 [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
Publication Date:
Research Org.:
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Sponsoring Org.:
USDOE Advanced Research Projects Agency - Energy (ARPA-E)
OSTI Identifier:
1429516
Alternate Identifier(s):
OSTI ID: 1434364; OSTI ID: 1557841
Grant/Contract Number:  
AR0000433
Resource Type:
Published Article
Journal Name:
Biotechnology and Bioengineering
Additional Journal Information:
Journal Name: Biotechnology and Bioengineering Journal Volume: 115 Journal Issue: 6; Journal ID: ISSN 0006-3592
Publisher:
Wiley Blackwell (John Wiley & Sons)
Country of Publication:
United States
Language:
English
Subject:
03 NATURAL GAS

Citation Formats

Marlow, Jeffrey J., Kumar, Amit, Enalls, Brandon C., Reynard, Linda M., Tuross, Noreen, Stephanopoulos, Gregory, and Girguis, Peter. Harnessing a methane‐fueled, sediment‐free mixed microbial community for utilization of distributed sources of natural gas. United States: N. p., 2018. Web. doi:10.1002/bit.26576.
Marlow, Jeffrey J., Kumar, Amit, Enalls, Brandon C., Reynard, Linda M., Tuross, Noreen, Stephanopoulos, Gregory, & Girguis, Peter. Harnessing a methane‐fueled, sediment‐free mixed microbial community for utilization of distributed sources of natural gas. United States. https://doi.org/10.1002/bit.26576
Marlow, Jeffrey J., Kumar, Amit, Enalls, Brandon C., Reynard, Linda M., Tuross, Noreen, Stephanopoulos, Gregory, and Girguis, Peter. Sat . "Harnessing a methane‐fueled, sediment‐free mixed microbial community for utilization of distributed sources of natural gas". United States. https://doi.org/10.1002/bit.26576.
@article{osti_1429516,
title = {Harnessing a methane‐fueled, sediment‐free mixed microbial community for utilization of distributed sources of natural gas},
author = {Marlow, Jeffrey J. and Kumar, Amit and Enalls, Brandon C. and Reynard, Linda M. and Tuross, Noreen and Stephanopoulos, Gregory and Girguis, Peter},
abstractNote = {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.},
doi = {10.1002/bit.26576},
journal = {Biotechnology and Bioengineering},
number = 6,
volume = 115,
place = {United States},
year = {Sat Mar 24 00:00:00 EDT 2018},
month = {Sat Mar 24 00:00:00 EDT 2018}
}

Journal Article:
Free Publicly Available Full Text
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https://doi.org/10.1002/bit.26576

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