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Title: System-level analysis of metabolic trade-offs during anaerobic photoheterotrophic growth in Rhodopseudomonas palustris

Abstract

Living organisms need to allocate their limited resources in a manner that optimizes their overall fitness by simultaneously achieving several different biological objectives. Examination of these biological trade-offs can provide invaluable information regarding the biophysical and biochemical bases behind observed cellular phenotypes. A quantitative knowledge of a cell system’s critical objectives is also needed for engineering of cellular metabolism, where there is interest in mitigating the fitness costs that may result from human manipulation. To study metabolism in photoheterotrophs, we developed and validated a genome-scale model of metabolism in Rhodopseudomonas palustris, a metabolically versatile gram-negative purple non-sulfur bacterium capable of growing phototrophically on various carbon sources, including inorganic carbon and aromatic compounds. To quantitatively assess trade-offs among a set of important biological objectives during different metabolic growth modes, we used our new model to conduct an 8-dimensional multi-objective flux analysis of metabolism in R. palustris. Our results revealed that phototrophic metabolism in R. palustris is light-limited under anaerobic conditions, regardless of the available carbon source. Under photoheterotrophic conditions, R. palustris prioritizes the optimization of carbon efficiency, followed by ATP production and biomass production rate, in a Pareto-optimal manner. To achieve maximum carbon fixation, cells appear to divert limited energy resourcesmore » away from growth and toward CO2 fixation, even in the presence of excess reduced carbon. We also found that to achieve the theoretical maximum rate of biomass production, anaerobic metabolism requires import of additional compounds (such as protons) to serve as electron acceptors. Finally, we found that production of hydrogen gas, of potential interest as a candidate biofuel, lowers the cellular growth rates under all circumstances. Photoheterotrophic metabolism of R. palustris is primarily regulated by the amount of light it can absorb and not the availability of carbon. However, despite carbon’s secondary role as a regulating factor, R. palustris’ metabolism strives for maximum carbon efficiency, even when this increased efficiency leads to slightly lower growth rates.« less

Authors:
ORCiD logo; ; ;
Publication Date:
Research Org.:
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1618551
Alternate Identifier(s):
OSTI ID: 1513153
Report Number(s):
LLNL-JRNL-727615
Journal ID: ISSN 1471-2105; 233; PII: 2844
Grant/Contract Number:  
SCW1039; AC52-07NA27344
Resource Type:
Published Article
Journal Name:
BMC Bioinformatics
Additional Journal Information:
Journal Name: BMC Bioinformatics Journal Volume: 20 Journal Issue: 1; Journal ID: ISSN 1471-2105
Publisher:
Springer Science + Business Media
Country of Publication:
United Kingdom
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; multi-objective analysis; metabolic trade-offs; flux balance analysis; genome-scale model; Rhodopseudomonas palustris; phototrophic metabolism; autotrophy; light limitation; carbon efficiency; carbon storage

Citation Formats

Navid, Ali, Jiao, Yongqin, Wong, Sergio Ernesto, and Pett-Ridge, Jennifer. System-level analysis of metabolic trade-offs during anaerobic photoheterotrophic growth in Rhodopseudomonas palustris. United Kingdom: N. p., 2019. Web. doi:10.1186/s12859-019-2844-z.
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Navid, Ali, Jiao, Yongqin, Wong, Sergio Ernesto, & Pett-Ridge, Jennifer. System-level analysis of metabolic trade-offs during anaerobic photoheterotrophic growth in Rhodopseudomonas palustris. United Kingdom. https://doi.org/10.1186/s12859-019-2844-z
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Navid, Ali, Jiao, Yongqin, Wong, Sergio Ernesto, and Pett-Ridge, Jennifer. Thu . "System-level analysis of metabolic trade-offs during anaerobic photoheterotrophic growth in Rhodopseudomonas palustris". United Kingdom. https://doi.org/10.1186/s12859-019-2844-z.
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@article{osti_1618551,
title = {System-level analysis of metabolic trade-offs during anaerobic photoheterotrophic growth in Rhodopseudomonas palustris},
author = {Navid, Ali and Jiao, Yongqin and Wong, Sergio Ernesto and Pett-Ridge, Jennifer},
abstractNote = {Living organisms need to allocate their limited resources in a manner that optimizes their overall fitness by simultaneously achieving several different biological objectives. Examination of these biological trade-offs can provide invaluable information regarding the biophysical and biochemical bases behind observed cellular phenotypes. A quantitative knowledge of a cell system’s critical objectives is also needed for engineering of cellular metabolism, where there is interest in mitigating the fitness costs that may result from human manipulation. To study metabolism in photoheterotrophs, we developed and validated a genome-scale model of metabolism in Rhodopseudomonas palustris, a metabolically versatile gram-negative purple non-sulfur bacterium capable of growing phototrophically on various carbon sources, including inorganic carbon and aromatic compounds. To quantitatively assess trade-offs among a set of important biological objectives during different metabolic growth modes, we used our new model to conduct an 8-dimensional multi-objective flux analysis of metabolism in R. palustris. Our results revealed that phototrophic metabolism in R. palustris is light-limited under anaerobic conditions, regardless of the available carbon source. Under photoheterotrophic conditions, R. palustris prioritizes the optimization of carbon efficiency, followed by ATP production and biomass production rate, in a Pareto-optimal manner. To achieve maximum carbon fixation, cells appear to divert limited energy resources away from growth and toward CO2 fixation, even in the presence of excess reduced carbon. We also found that to achieve the theoretical maximum rate of biomass production, anaerobic metabolism requires import of additional compounds (such as protons) to serve as electron acceptors. Finally, we found that production of hydrogen gas, of potential interest as a candidate biofuel, lowers the cellular growth rates under all circumstances. Photoheterotrophic metabolism of R. palustris is primarily regulated by the amount of light it can absorb and not the availability of carbon. However, despite carbon’s secondary role as a regulating factor, R. palustris’ metabolism strives for maximum carbon efficiency, even when this increased efficiency leads to slightly lower growth rates.},
doi = {10.1186/s12859-019-2844-z},
journal = {BMC Bioinformatics},
number = 1,
volume = 20,
place = {United Kingdom},
year = {Thu May 09 00:00:00 EDT 2019},
month = {Thu May 09 00:00:00 EDT 2019}
}
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Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1186/s12859-019-2844-z
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Cited by: 14 works
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Figures / Tables:

Figure 1 Figure 1: Heat map of the 8-dimensional Pareto front from MOFA analysis (objectives: growth, carbon fixation/carbon efficiency, nutrient allocation, ATP production, production of some small organic byproduct (pyruvate, succinate and $α$-ketoglutarate), and H2 production) of anaerobic mixotrophic metabolism of acetate in R. palustris. a. 1719 unique Pareto-optimal solutions identified duringmore » our analysis. b. Select Pareto-optimal solutions from same MOFA study are highlighted for discussion. Each biological objective was examined at intervals equaling 1/10 maximum normalized value. The analyses showed that the observed growth rate (E) is smaller than the maximum theoretical growth rate (A) in a carbon-limited system with unlimited light absorbing capability. When CO2 export was constrained with experimental measurements (without limiting light) the predicted growth rate was still larger than the measured value (B). Eliminating CBB (with unlimited light) resulted in increased production of CO2, but the predicted growth rate was still greater than the measured value (C). Limiting light and carbon import brought the predicted growth rate closer to measured value (D), however the rate of CO2 export was greater than measured value. When light, acetate import, and CO2 export were limited the model predicted that succinate will be exported. Blocking export of succinate slightly lowered the growth rate and resulted in production of other small organic acids (F). Finally, the simulations showed that H2 production competes with growth pathways for resources and that maximum theoretical H2 production (G) would result in cessation of growth. This result is supported by experimental observations.« less
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