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Artificial consortium demonstrates emergent properties of enhanced cellulosic-sugar degradation and biofuel synthesis

Planktonic cultures, of a rationally designed consortium, demonstrated emergent properties that exceeded the sums of monoculture properties, including a >200% increase in cellobiose catabolism, a >100% increase in glycerol catabolism, a >800% increase in ethanol production, and a >120% i...

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Autores principales: Park, Heejoon, Patel, Ayushi, Hunt, Kristopher A., Henson, Michael A., Carlson, Ross P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7710750/
https://www.ncbi.nlm.nih.gov/pubmed/33268782
http://dx.doi.org/10.1038/s41522-020-00170-8
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author Park, Heejoon
Patel, Ayushi
Hunt, Kristopher A.
Henson, Michael A.
Carlson, Ross P.
author_facet Park, Heejoon
Patel, Ayushi
Hunt, Kristopher A.
Henson, Michael A.
Carlson, Ross P.
author_sort Park, Heejoon
collection PubMed
description Planktonic cultures, of a rationally designed consortium, demonstrated emergent properties that exceeded the sums of monoculture properties, including a >200% increase in cellobiose catabolism, a >100% increase in glycerol catabolism, a >800% increase in ethanol production, and a >120% increase in biomass productivity. The consortium was designed to have a primary and secondary-resource specialist that used crossfeeding with a positive feedback mechanism, division of labor, and nutrient and energy transfer via necromass catabolism. The primary resource specialist was Clostridium phytofermentans (a.k.a. Lachnoclostridium phytofermentans), a cellulolytic, obligate anaerobe. The secondary-resource specialist was Escherichia coli, a versatile, facultative anaerobe, which can ferment glycerol and byproducts of cellobiose catabolism. The consortium also demonstrated emergent properties of enhanced biomass accumulation when grown as biofilms, which created high cell density communities with gradients of species along the vertical axis. Consortium biofilms were robust to oxic perturbations with E. coli consuming O(2), creating an anoxic environment for C. phytofermentans. Anoxic/oxic cycling further enhanced biomass productivity of the biofilm consortium, increasing biomass accumulation ~250% over the sum of the monoculture biofilms. Consortium emergent properties were credited to several synergistic mechanisms. E. coli consumed inhibitory byproducts from cellobiose catabolism, driving higher C. phytofermentans growth and higher cellulolytic enzyme production, which in turn provided more substrate for E. coli. E. coli necromass enhanced C. phytofermentans growth while C. phytofermentans necromass aided E. coli growth via the release of peptides and amino acids, respectively. In aggregate, temporal cycling of necromass constituents increased flux of cellulose-derived resources through the consortium. The study establishes a consortia-based, bioprocessing strategy built on naturally occurring interactions for improved conversion of cellulose-derived sugars into bioproducts.
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spelling pubmed-77107502020-12-03 Artificial consortium demonstrates emergent properties of enhanced cellulosic-sugar degradation and biofuel synthesis Park, Heejoon Patel, Ayushi Hunt, Kristopher A. Henson, Michael A. Carlson, Ross P. NPJ Biofilms Microbiomes Article Planktonic cultures, of a rationally designed consortium, demonstrated emergent properties that exceeded the sums of monoculture properties, including a >200% increase in cellobiose catabolism, a >100% increase in glycerol catabolism, a >800% increase in ethanol production, and a >120% increase in biomass productivity. The consortium was designed to have a primary and secondary-resource specialist that used crossfeeding with a positive feedback mechanism, division of labor, and nutrient and energy transfer via necromass catabolism. The primary resource specialist was Clostridium phytofermentans (a.k.a. Lachnoclostridium phytofermentans), a cellulolytic, obligate anaerobe. The secondary-resource specialist was Escherichia coli, a versatile, facultative anaerobe, which can ferment glycerol and byproducts of cellobiose catabolism. The consortium also demonstrated emergent properties of enhanced biomass accumulation when grown as biofilms, which created high cell density communities with gradients of species along the vertical axis. Consortium biofilms were robust to oxic perturbations with E. coli consuming O(2), creating an anoxic environment for C. phytofermentans. Anoxic/oxic cycling further enhanced biomass productivity of the biofilm consortium, increasing biomass accumulation ~250% over the sum of the monoculture biofilms. Consortium emergent properties were credited to several synergistic mechanisms. E. coli consumed inhibitory byproducts from cellobiose catabolism, driving higher C. phytofermentans growth and higher cellulolytic enzyme production, which in turn provided more substrate for E. coli. E. coli necromass enhanced C. phytofermentans growth while C. phytofermentans necromass aided E. coli growth via the release of peptides and amino acids, respectively. In aggregate, temporal cycling of necromass constituents increased flux of cellulose-derived resources through the consortium. The study establishes a consortia-based, bioprocessing strategy built on naturally occurring interactions for improved conversion of cellulose-derived sugars into bioproducts. Nature Publishing Group UK 2020-12-02 /pmc/articles/PMC7710750/ /pubmed/33268782 http://dx.doi.org/10.1038/s41522-020-00170-8 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Park, Heejoon
Patel, Ayushi
Hunt, Kristopher A.
Henson, Michael A.
Carlson, Ross P.
Artificial consortium demonstrates emergent properties of enhanced cellulosic-sugar degradation and biofuel synthesis
title Artificial consortium demonstrates emergent properties of enhanced cellulosic-sugar degradation and biofuel synthesis
title_full Artificial consortium demonstrates emergent properties of enhanced cellulosic-sugar degradation and biofuel synthesis
title_fullStr Artificial consortium demonstrates emergent properties of enhanced cellulosic-sugar degradation and biofuel synthesis
title_full_unstemmed Artificial consortium demonstrates emergent properties of enhanced cellulosic-sugar degradation and biofuel synthesis
title_short Artificial consortium demonstrates emergent properties of enhanced cellulosic-sugar degradation and biofuel synthesis
title_sort artificial consortium demonstrates emergent properties of enhanced cellulosic-sugar degradation and biofuel synthesis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7710750/
https://www.ncbi.nlm.nih.gov/pubmed/33268782
http://dx.doi.org/10.1038/s41522-020-00170-8
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