Lipid membrane remodeling and metabolic response during isobutanol and ethanol exposure in Zymomonas mobilis

Rivera Vazquez, Julio; Trujillo, Edna; Williams, Jonathan; She, Fukang; Getahun, Fitsum; Callaghan, Melanie M.; Coon, Joshua J.; Amador-Noguez, Daniel

doi:10.1186/s13068-023-02450-9

Lipid membrane remodeling and metabolic response during isobutanol and ethanol exposure in Zymomonas mobilis

Journal Article · Sat Jan 27 23:00:00 EST 2024 · Biotechnology for Biofuels and Bioproducts

DOI:https://doi.org/10.1186/s13068-023-02450-9· OSTI ID:2283103

Rivera Vazquez, Julio; Trujillo, Edna; Williams, Jonathan; She, Fukang; Getahun, Fitsum; Callaghan, Melanie M.; Coon, Joshua J.; Amador-Noguez, Daniel

Abstract Background

Recent engineering efforts have targeted the ethanologenic bacterium Zymomonas mobilis for isobutanol production. However, significant hurdles remain due this organism’s vulnerability to isobutanol toxicity, adversely affecting its growth and productivity. The limited understanding of the physiological impacts of isobutanol on Z. mobilis constrains our ability to overcome these production barriers.

Results

We utilized a systems-level approach comprising LC–MS/MS-based lipidomics, metabolomics, and shotgun proteomics, to investigate how exposure to ethanol and isobutanol impact the lipid membrane composition and overall physiology of Z. mobilis . Our analysis revealed significant and distinct alterations in membrane phospholipid and fatty acid composition resulting from ethanol and isobutanol exposure. Notably, ethanol exposure increased membrane cyclopropane fatty acid content and expression of cyclopropane fatty acid (CFA) synthase. Surprisingly, isobutanol decreased cyclopropane fatty acid content despite robust upregulation of CFA synthase. Overexpression of the native Z. mobilis’ CFA synthase increased cyclopropane fatty acid content in all phospholipid classes and was associated with a significant improvement in growth rates in the presence of added ethanol and isobutanol. Heterologous expression of CFA synthase from Clostridium acetobutylicum resulted in a near complete replacement of unsaturated fatty acids with cyclopropane fatty acids, affecting all lipid classes. However, this did not translate to improved growth rates under isobutanol exposure.

Correlating with its greater susceptibility to isobutanol, Z. mobilis exhibited more pronounced alterations in its proteome, metabolome, and overall cell morphology—including cell swelling and formation of intracellular protein aggregates —when exposed to isobutanol compared to ethanol. Isobutanol triggered a broad stress response marked by the upregulation of heat shock proteins, efflux transporters, DNA repair systems, and the downregulation of cell motility proteins. Isobutanol also elicited widespread dysregulation of Z. mobilis ’ primary metabolism evidenced by increased levels of nucleotide degradation intermediates and the depletion of biosynthetic and glycolytic intermediates.

Conclusions

This study provides a comprehensive, systems-level evaluation of the impact of ethanol and isobutanol exposure on the lipid membrane composition and overall physiology of Z. mobilis . These findings will guide engineering of Z. mobilis towards the creation of isobutanol-tolerant strains that can serve as robust platforms for the industrial production of isobutanol from lignocellulosic sugars.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0018409

OSTI ID:: 2283103

Alternate ID(s):: OSTI ID: 2470738

Journal Information:: Biotechnology for Biofuels and Bioproducts, Journal Name: Biotechnology for Biofuels and Bioproducts Journal Issue: 1 Vol. 17; ISSN 2731-3654

Publisher:: Springer Science + Business MediaCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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