Adaptive evolution reveals a tradeoff between growth rate and oxidative stress during naphthoquinone-based aerobic respiration

Amitesh Anand; Ke Chen; Laurence Yang; Anand V. Sastry; Connor A. Olson; Saugat Poudel; Yara Seif; Ying Hefner; Patrick V. Phaneuf; Sibei Xu; Richard Szubin; Adam M. Feist; Bernhard O. Palsson

doi:10.1073/pnas.1909987116

Adaptive evolution reveals a tradeoff between growth rate and oxidative stress during naphthoquinone-based aerobic respiration

Amitesh Anand, Ke Chen, Laurence Yang, Anand V. Sastry, Connor A. Olson, Saugat Poudel, Yara Seif, Ying Hefner, Patrick V. Phaneuf, Sibei Xu, Richard Szubin, Adam M. Feist, Bernhard O. Palsson^*

^*Corresponding author for this work

University of Iceland

Research output: Contribution to journal › Article › peer-review

17 Citations (Scopus)

Abstract

Evolution fine-tunes biological pathways to achieve a robust cellular physiology. Two and a half billion years ago, rapidly rising levels of oxygen as a byproduct of blooming cyanobacterial photosynthesis resulted in a redox upshift in microbial energetics. The appearance of higher-redox-potential respiratory quinone, ubiquinone (UQ), is believed to be an adaptive response to this environmental transition. However, the majority of bacterial species are still dependent on the ancient respiratory quinone, naphthoquinone (NQ). Gammaproteobacteria can biosynthesize both of these respiratory quinones, where UQ has been associated with aerobic lifestyle and NQ with anaerobic lifestyle. We engineered an obligate NQ-dependent γ-proteobacterium, Escherichia coli ΔubiC, and performed adaptive laboratory evolution to understand the selection against the use of NQ in an oxic environment and also the adaptation required to support the NQ-driven aerobic electron transport chain. A comparative systems-level analysis of pre- and postevolved NQ-dependent strains revealed a clear shift from fermentative to oxidative metabolism enabled by higher periplasmic superoxide defense. This metabolic shift was driven by the concerted activity of 3 transcriptional regulators (PdhR, RpoS, and Fur). Analysis of these findings using a genome-scale model suggested that resource allocation to reactive oxygen species (ROS)mitigation results in lower growth rates. These results provide a direct elucidation of a resource allocation tradeoff between growth rate and ROS mitigation costs associated with NQ usage under oxygen-replete condition.

Original language	English
Pages (from-to)	25287-25292
Number of pages	6
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	116
Issue number	50
DOIs	https://doi.org/10.1073/pnas.1909987116
Publication status	Published - 10 Dec 2019

Bibliographical note

Funding Information:
This work was funded by Novo Nordisk Foundation Grant NNF10CC1016517 and NIH Grants R01GM057089 and U01AI124316. We thank Marc Abrams (Systems Biology Research Group, University of California San Diego) for assistance with manuscript editing. The support of University of California San Diego, Chemistry and Biochemistry Molecular Mass Spectrometry Facility is duly acknowledged.*%blankline%*

Funding Information:
ACKNOWLEDGMENTS. This work was funded by Novo Nordisk Foundation Grant NNF10CC1016517 and NIH Grants R01GM057089 and U01AI124316. We thank Marc Abrams (Systems Biology Research Group, University of

Publisher Copyright:
© 2019 National Academy of Sciences. All rights reserved.

Other keywords

Genome-scale model
Naphthoquinone
Oxidative stress
Respiration

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10.1073/pnas.1909987116

Cite this

Anand, A., Chen, K., Yang, L., Sastry, A. V., Olson, C. A., Poudel, S., Seif, Y., Hefner, Y., Phaneuf, P. V., Xu, S., Szubin, R., Feist, A. M., & Palsson, B. O. (2019). Adaptive evolution reveals a tradeoff between growth rate and oxidative stress during naphthoquinone-based aerobic respiration. Proceedings of the National Academy of Sciences of the United States of America, 116(50), 25287-25292. https://doi.org/10.1073/pnas.1909987116

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title = "Adaptive evolution reveals a tradeoff between growth rate and oxidative stress during naphthoquinone-based aerobic respiration",

abstract = "Evolution fine-tunes biological pathways to achieve a robust cellular physiology. Two and a half billion years ago, rapidly rising levels of oxygen as a byproduct of blooming cyanobacterial photosynthesis resulted in a redox upshift in microbial energetics. The appearance of higher-redox-potential respiratory quinone, ubiquinone (UQ), is believed to be an adaptive response to this environmental transition. However, the majority of bacterial species are still dependent on the ancient respiratory quinone, naphthoquinone (NQ). Gammaproteobacteria can biosynthesize both of these respiratory quinones, where UQ has been associated with aerobic lifestyle and NQ with anaerobic lifestyle. We engineered an obligate NQ-dependent γ-proteobacterium, Escherichia coli ΔubiC, and performed adaptive laboratory evolution to understand the selection against the use of NQ in an oxic environment and also the adaptation required to support the NQ-driven aerobic electron transport chain. A comparative systems-level analysis of pre- and postevolved NQ-dependent strains revealed a clear shift from fermentative to oxidative metabolism enabled by higher periplasmic superoxide defense. This metabolic shift was driven by the concerted activity of 3 transcriptional regulators (PdhR, RpoS, and Fur). Analysis of these findings using a genome-scale model suggested that resource allocation to reactive oxygen species (ROS)mitigation results in lower growth rates. These results provide a direct elucidation of a resource allocation tradeoff between growth rate and ROS mitigation costs associated with NQ usage under oxygen-replete condition.",

keywords = "Genome-scale model, Naphthoquinone, Oxidative stress, Respiration",

author = "Amitesh Anand and Ke Chen and Laurence Yang and Sastry, {Anand V.} and Olson, {Connor A.} and Saugat Poudel and Yara Seif and Ying Hefner and Phaneuf, {Patrick V.} and Sibei Xu and Richard Szubin and Feist, {Adam M.} and Palsson, {Bernhard O.}",

note = "Funding Information: This work was funded by Novo Nordisk Foundation Grant NNF10CC1016517 and NIH Grants R01GM057089 and U01AI124316. We thank Marc Abrams (Systems Biology Research Group, University of California San Diego) for assistance with manuscript editing. The support of University of California San Diego, Chemistry and Biochemistry Molecular Mass Spectrometry Facility is duly acknowledged.*%blankline%* Funding Information: ACKNOWLEDGMENTS. This work was funded by Novo Nordisk Foundation Grant NNF10CC1016517 and NIH Grants R01GM057089 and U01AI124316. We thank Marc Abrams (Systems Biology Research Group, University of Publisher Copyright: {\textcopyright} 2019 National Academy of Sciences. All rights reserved.",

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day = "10",

doi = "10.1073/pnas.1909987116",

language = "English",

volume = "116",

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Anand, A, Chen, K, Yang, L, Sastry, AV, Olson, CA, Poudel, S, Seif, Y, Hefner, Y, Phaneuf, PV, Xu, S, Szubin, R, Feist, AM & Palsson, BO 2019, 'Adaptive evolution reveals a tradeoff between growth rate and oxidative stress during naphthoquinone-based aerobic respiration', Proceedings of the National Academy of Sciences of the United States of America, vol. 116, no. 50, pp. 25287-25292. https://doi.org/10.1073/pnas.1909987116

Adaptive evolution reveals a tradeoff between growth rate and oxidative stress during naphthoquinone-based aerobic respiration. / Anand, Amitesh; Chen, Ke; Yang, Laurence et al.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, No. 50, 10.12.2019, p. 25287-25292.

Research output: Contribution to journal › Article › peer-review

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AU - Anand, Amitesh

AU - Chen, Ke

AU - Yang, Laurence

AU - Sastry, Anand V.

AU - Olson, Connor A.

AU - Poudel, Saugat

AU - Seif, Yara

AU - Hefner, Ying

AU - Phaneuf, Patrick V.

AU - Xu, Sibei

AU - Szubin, Richard

AU - Feist, Adam M.

AU - Palsson, Bernhard O.

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PY - 2019/12/10

Y1 - 2019/12/10

N2 - Evolution fine-tunes biological pathways to achieve a robust cellular physiology. Two and a half billion years ago, rapidly rising levels of oxygen as a byproduct of blooming cyanobacterial photosynthesis resulted in a redox upshift in microbial energetics. The appearance of higher-redox-potential respiratory quinone, ubiquinone (UQ), is believed to be an adaptive response to this environmental transition. However, the majority of bacterial species are still dependent on the ancient respiratory quinone, naphthoquinone (NQ). Gammaproteobacteria can biosynthesize both of these respiratory quinones, where UQ has been associated with aerobic lifestyle and NQ with anaerobic lifestyle. We engineered an obligate NQ-dependent γ-proteobacterium, Escherichia coli ΔubiC, and performed adaptive laboratory evolution to understand the selection against the use of NQ in an oxic environment and also the adaptation required to support the NQ-driven aerobic electron transport chain. A comparative systems-level analysis of pre- and postevolved NQ-dependent strains revealed a clear shift from fermentative to oxidative metabolism enabled by higher periplasmic superoxide defense. This metabolic shift was driven by the concerted activity of 3 transcriptional regulators (PdhR, RpoS, and Fur). Analysis of these findings using a genome-scale model suggested that resource allocation to reactive oxygen species (ROS)mitigation results in lower growth rates. These results provide a direct elucidation of a resource allocation tradeoff between growth rate and ROS mitigation costs associated with NQ usage under oxygen-replete condition.

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KW - Genome-scale model

KW - Naphthoquinone

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Adaptive evolution reveals a tradeoff between growth rate and oxidative stress during naphthoquinone-based aerobic respiration

Abstract

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