Harnessing a methane-fueled, sediment-free mixed microbial community for utilization of distributed sources of natural gas
Biotechnology and Bioengineering Published by Wiley Periodicals Inc. 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 pro...
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| Format: | Article |
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Wiley Blackwell
2019
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| Online Access: | http://hdl.handle.net/1721.1/120332 https://orcid.org/0000-0001-6909-4568 |
| _version_ | 1826189590642294784 |
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| author | Marlow, Jeffrey J. Kumar, Amit Enalls, Brandon C. Reynard, Linda M. Tuross, Noreen Stephanopoulos, Gregory Girguis, Peter |
| author2 | Massachusetts Institute of Technology. Department of Chemical Engineering |
| author_facet | Massachusetts Institute of Technology. Department of Chemical Engineering Marlow, Jeffrey J. Kumar, Amit Enalls, Brandon C. Reynard, Linda M. Tuross, Noreen Stephanopoulos, Gregory Girguis, Peter |
| author_sort | Marlow, Jeffrey J. |
| collection | MIT |
| description | Biotechnology and Bioengineering Published by Wiley Periodicals Inc. 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. |
| first_indexed | 2024-09-23T08:18:02Z |
| format | Article |
| id | mit-1721.1/120332 |
| institution | Massachusetts Institute of Technology |
| last_indexed | 2024-09-23T08:18:02Z |
| publishDate | 2019 |
| publisher | Wiley Blackwell |
| record_format | dspace |
| spelling | mit-1721.1/1203322022-10-25T05:33:53Z Harnessing a methane-fueled, sediment-free mixed microbial community for utilization of distributed sources of natural gas Marlow, Jeffrey J. Kumar, Amit Enalls, Brandon C. Reynard, Linda M. Tuross, Noreen Stephanopoulos, Gregory Girguis, Peter Massachusetts Institute of Technology. Department of Chemical Engineering Kumar, Amit Stephanopoulos, Gregory Biotechnology and Bioengineering Published by Wiley Periodicals Inc. 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. United States. Department of Energy (Award DE‐AR0000433) National Science Foundation (U.S.) (Grant DEB‐1542506) 2019-02-11T19:10:19Z 2019-02-11T19:10:19Z 2018-04 2018-01 2019-01-29T12:43:41Z Article http://purl.org/eprint/type/JournalArticle 0006-3592 http://hdl.handle.net/1721.1/120332 Marlow, Jeffrey J. et al. “Harnessing a Methane-Fueled, Sediment-Free Mixed Microbial Community for Utilization of Distributed Sources of Natural Gas.” Biotechnology and Bioengineering 115, 6 (March 2018): 1450–1464 © 2018 The Authors https://orcid.org/0000-0001-6909-4568 http://dx.doi.org/10.1002/BIT.26576 Biotechnology and Bioengineering Creative Commons Attribution-NonCommercial-NoDerivs License http://creativecommons.org/licenses/by-nc-nd/4.0/ application/pdf Wiley Blackwell IOP Publishing |
| spellingShingle | 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 |
| title | Harnessing a methane-fueled, sediment-free mixed microbial community for utilization of distributed sources of natural gas |
| title_full | Harnessing a methane-fueled, sediment-free mixed microbial community for utilization of distributed sources of natural gas |
| title_fullStr | Harnessing a methane-fueled, sediment-free mixed microbial community for utilization of distributed sources of natural gas |
| title_full_unstemmed | Harnessing a methane-fueled, sediment-free mixed microbial community for utilization of distributed sources of natural gas |
| title_short | Harnessing a methane-fueled, sediment-free mixed microbial community for utilization of distributed sources of natural gas |
| title_sort | harnessing a methane fueled sediment free mixed microbial community for utilization of distributed sources of natural gas |
| url | http://hdl.handle.net/1721.1/120332 https://orcid.org/0000-0001-6909-4568 |
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