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Title: Synthetic photosynthetic consortia define interactions leading to robustness and photoproduction

Abstract

In this study, microbial consortia composed of autotrophic and heterotrophic species abound in nature, yet examples of synthetic communities with mixed metabolism are limited in the laboratory. We previously engineered a model cyanobacterium, Synechococcus elongatus PCC 7942, to secrete the bulk of the carbon it fixes as sucrose, a carbohydrate that can be utilized by many other microbes. Here, we tested the capability of sucrose-secreting cyanobacteria to act as a flexible platform for the construction of synthetic, light-driven consortia by pairing them with three disparate heterotrophs: Bacillus subtilis, Escherichia coli, or Saccharomyces cerevisiae. The comparison of these different co-culture dyads reveals general design principles for the construction of robust autotroph/heterotroph consortia. As a result, we observed heterotrophic growth dependent upon cyanobacterial photosynthate in each co-culture pair. Furthermore, these synthetic consortia could be stabilized over the long-term (weeks to months) and both species could persist when challenged with specific perturbations. Stability and productivity of autotroph/heterotroph co-cultures was dependent on heterotroph sucrose utilization, as well as other species-independent interactions that we observed across all dyads. One destabilizing interaction we observed was that non-sucrose byproducts of oxygenic photosynthesis negatively impacted heterotroph growth. Conversely, inoculation of each heterotrophic species enhanced cyanobacterial growth in comparisonmore » to axenic cultures. Finally, these consortia can be flexibly programmed for photoproduction of target compounds and proteins; by changing the heterotroph in co-culture to specialized strains of B. subtilis or E. coli we demonstrate production of alpha-amylase and polyhydroxybutyrate, respectively. In conclusion, enabled by the unprecedented flexibility of this consortia design, we uncover species-independent design principles that influence cyanobacteria/heterotroph consortia robustness. The modular nature of these communities and their unusual robustness exhibits promise as a platform for highly-versatile photoproduction strategies that capitalize on multi-species interactions and could be utilized as a tool for the study of nascent symbioses. Further consortia improvements via engineered interventions beyond those we show here (i.e., increased efficiency growing on sucrose) could improve these communities as production platforms.« less

Authors:
; ; ;
Publication Date:
Research Org.:
Johns Hopkins Univ., Baltimore, MD (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Science Foundation (NSF)
OSTI Identifier:
1618912
Alternate Identifier(s):
OSTI ID: 1367177; OSTI ID: 1485582
Grant/Contract Number:  
SC0012658
Resource Type:
Published Article
Journal Name:
Journal of Biological Engineering
Additional Journal Information:
Journal Name: Journal of Biological Engineering Journal Volume: 11 Journal Issue: 1; Journal ID: ISSN 1754-1611
Publisher:
Springer Science + Business Media
Country of Publication:
United Kingdom
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; synthetic biology; photoproduction; synthetic consortia; microbial communities

Citation Formats

Hays, Stephanie G., Yan, Leo L. W., Silver, Pamela A., and Ducat, Daniel C. Synthetic photosynthetic consortia define interactions leading to robustness and photoproduction. United Kingdom: N. p., 2017. Web. doi:10.1186/s13036-017-0048-5.
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Hays, Stephanie G., Yan, Leo L. W., Silver, Pamela A., & Ducat, Daniel C. Synthetic photosynthetic consortia define interactions leading to robustness and photoproduction. United Kingdom. https://doi.org/10.1186/s13036-017-0048-5
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Hays, Stephanie G., Yan, Leo L. W., Silver, Pamela A., and Ducat, Daniel C. Mon . "Synthetic photosynthetic consortia define interactions leading to robustness and photoproduction". United Kingdom. https://doi.org/10.1186/s13036-017-0048-5.
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@article{osti_1618912,
title = {Synthetic photosynthetic consortia define interactions leading to robustness and photoproduction},
author = {Hays, Stephanie G. and Yan, Leo L. W. and Silver, Pamela A. and Ducat, Daniel C.},
abstractNote = {In this study, microbial consortia composed of autotrophic and heterotrophic species abound in nature, yet examples of synthetic communities with mixed metabolism are limited in the laboratory. We previously engineered a model cyanobacterium, Synechococcus elongatus PCC 7942, to secrete the bulk of the carbon it fixes as sucrose, a carbohydrate that can be utilized by many other microbes. Here, we tested the capability of sucrose-secreting cyanobacteria to act as a flexible platform for the construction of synthetic, light-driven consortia by pairing them with three disparate heterotrophs: Bacillus subtilis, Escherichia coli, or Saccharomyces cerevisiae. The comparison of these different co-culture dyads reveals general design principles for the construction of robust autotroph/heterotroph consortia. As a result, we observed heterotrophic growth dependent upon cyanobacterial photosynthate in each co-culture pair. Furthermore, these synthetic consortia could be stabilized over the long-term (weeks to months) and both species could persist when challenged with specific perturbations. Stability and productivity of autotroph/heterotroph co-cultures was dependent on heterotroph sucrose utilization, as well as other species-independent interactions that we observed across all dyads. One destabilizing interaction we observed was that non-sucrose byproducts of oxygenic photosynthesis negatively impacted heterotroph growth. Conversely, inoculation of each heterotrophic species enhanced cyanobacterial growth in comparison to axenic cultures. Finally, these consortia can be flexibly programmed for photoproduction of target compounds and proteins; by changing the heterotroph in co-culture to specialized strains of B. subtilis or E. coli we demonstrate production of alpha-amylase and polyhydroxybutyrate, respectively. In conclusion, enabled by the unprecedented flexibility of this consortia design, we uncover species-independent design principles that influence cyanobacteria/heterotroph consortia robustness. The modular nature of these communities and their unusual robustness exhibits promise as a platform for highly-versatile photoproduction strategies that capitalize on multi-species interactions and could be utilized as a tool for the study of nascent symbioses. Further consortia improvements via engineered interventions beyond those we show here (i.e., increased efficiency growing on sucrose) could improve these communities as production platforms.},
doi = {10.1186/s13036-017-0048-5},
journal = {Journal of Biological Engineering},
number = 1,
volume = 11,
place = {United Kingdom},
year = {Mon Jan 23 00:00:00 EST 2017},
month = {Mon Jan 23 00:00:00 EST 2017}
}
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Journal Article:
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https://doi.org/10.1186/s13036-017-0048-5
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Cited by: 69 works
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Figures / Tables:

Fig. 1 Fig. 1: Axenic characterizations of candidate strains. a This schematic shows the engineered microbial community design. CscB+ S. elongatus (green) capture light and CO2 via photosynthesis. Fixed carbon is secreted as sucrose (black arrows) when induced with IPTG in the presence of osmotic pressure (NaCl). This secreted carbon then supportsmore » the growth of B. subtilis (blue), S. cerevisiae (purple), or E. coli (orange) with the final goal of production of target compounds from those heterotrophs. Axenic cscB+ S. elongatus was grown in CoBBG-11 with (solid line) and without IPTG (dashed line) to induce sucrose secretion. Cell density (b) and sucrose levels in culture supernatants (c) were measured. Error bars are standard deviation of 8 biological replicates. For characterization of cyanobacteria in CoYBG-11 see Additional file 1: Figure S1. d Heterotroph growth in isolation was characterized via growth rate in co-culture buffer supplemented with 2% sucrose. Error is standard deviation of ≥ 3 replicates« less
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    Works referencing / citing this record:

    Engineering microbial consortia by division of labor
    journal, February 2019

    Photoautotrophic production of polyhydroxyalkanoates in a synthetic mixed culture of Synechococcus elongatus cscB and Pseudomonas putida cscAB
    journal, July 2017

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