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 Feist, Bernhard Palsson*

*Corresponding author for this work

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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 languageEnglish
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number50
Pages (from-to)25287-25292
ISSN0027-8424
DOIs
Publication statusPublished - 2019

Cite this

Anand, Amitesh ; Chen, Ke ; Yang, Laurence ; Sastry, Anand V. ; Olson, Connor A. ; Poudel, Saugat ; Seif, Yara ; Hefner, Ying ; Phaneuf, Patrick V. ; Xu, Sibei ; Szubin, Richard ; Feist, Adam ; Palsson, Bernhard. / Adaptive evolution reveals a tradeoff between growth rate and oxidative stress during naphthoquinone-based aerobic respiration. In: Proceedings of the National Academy of Sciences of the United States of America. 2019 ; Vol. 116, No. 50. pp. 25287-25292.
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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.",
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 Adam Feist and Bernhard Palsson",
year = "2019",
doi = "10.1073/pnas.1909987116",
language = "English",
volume = "116",
pages = "25287--25292",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
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Adaptive evolution reveals a tradeoff between growth rate and oxidative stress during naphthoquinone-based aerobic respiration. / Anand, Amitesh; Chen, Ke; Yang, Laurence; Sastry, Anand V.; Olson, Connor A.; Poudel, Saugat; Seif, Yara; Hefner, Ying; Phaneuf, Patrick V.; Xu, Sibei; Szubin, Richard; Feist, Adam; Palsson, Bernhard.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, No. 50, 2019, p. 25287-25292.

Research output: Contribution to journalJournal articleResearchpeer-review

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T1 - Adaptive evolution reveals a tradeoff between growth rate and oxidative stress during naphthoquinone-based aerobic respiration

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

AU - Palsson, Bernhard

PY - 2019

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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.

AB - 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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DO - 10.1073/pnas.1909987116

M3 - Journal article

C2 - 31767748

VL - 116

SP - 25287

EP - 25292

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 50

ER -