Orthogonal chemical genomics approaches reveal genomic targets for increasing anaerobic chemical tolerance in Zymomonas mobilis

Eckmann, Jacob B.; Enright Steinberger, Amy L.; Davies, Morgan; Whelan, Elizabeth; Myers, Kevin S.; Robinson, Margaret L.; Banta, Amy B.; Lal, Piyush B.; Coon, Joshua J.; Sato, Trey K.; Kiley, Patricia J.; Peters, Jason M.

doi:10.1128/msystems.01001-25

Orthogonal chemical genomics approaches reveal genomic targets for increasing anaerobic chemical tolerance in Zymomonas mobilis

Journal Article · Thu Dec 04 00:00:00 EST 2025 · mSystems

DOI:https://doi.org/10.1128/msystems.01001-25· OSTI ID:3006149

^[1]; ^[1]; Davies, Morgan ^[1]; Whelan, Elizabeth ^[1]; ^[1]; Robinson, Margaret L. ^[1]; ^[1]; ^[1]; ^[1]; ^[1]; ^[1]; ^[1]

Univ. of Wisconsin, Madison, WI (United States)

Genetically engineered microbes have the potential to increase efficiency in the bioeconomy by overcoming growth-limiting production stress. Screens of gene perturbation libraries against production stressors can identify high-value engineering targets, but follow-up experiments needed to guard against false positives are slow and resource-intensive. In principle, the use of orthogonal gene perturbation approaches could increase recovery of true positives over false positives because the strengths of one technique compensate for the weaknesses of the other, but, in practice, two parallel screens are rarely performed at the genome scale. Here, we screen genome-scale CRISPRi (CRISPR interference) knockdown and transposon insertion libraries of the bioenergy-relevant Alphaproteobacterium, Zymomonas mobilis, against growth inhibitors commonly found in deconstructed plant material. Integrating data from the two gene perturbation techniques, we established an approach for defining engineering targets with high specificity. This allowed us to identify all known genes in the cytochrome bc1 and cytochrome c synthesis pathway as potential targets for engineering resistance to phenolic acids under anaerobic conditions, a subset of which we validated using precise gene deletions. Strikingly, this finding is specific to the cytochrome bc1 and cytochrome c pathway and does not extend to other branches of the electron transport chain. We further show that exposure of Z. mobilis to ferulic acid causes substantial remodeling of the cell envelope proteome, as well as the downregulation of TonB-dependent transporters. Our work provides a generalizable strategy for identifying high-value engineering targets from gene perturbation screens that is broadly applicable.

View Accepted Manuscript (DOE)

Research Organization:: Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)

Sponsoring Organization:: National Institutes of Health (NIH); National Science Foundation (NSF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0018409

OSTI ID:: 3006149

Journal Information:: mSystems, Journal Name: mSystems; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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High‐throughput CRISPRi phenotyping identifies new essential genes in Streptococcus pneumoniae Liu, Xue; Gallay, Clement; Kjos, Morten Molecular Systems Biology, Vol. 13, Issue 5 https://doi.org/10.15252/msb.20167449	journal	May 2017
The poolr Package for Combining Independent and Dependent p Values Cinar, Ozan; Viechtbauer, Wolfgang Journal of Statistical Software, Vol. 101, Issue 1 https://doi.org/10.18637/jss.v101.i01	journal	January 2022
Regulation and Function of Versatile Aerobic and Anaerobic Respiratory Metabolism in Pseudomonas aeruginosa Arai, Hiroyuki Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00103	journal	January 2011
Death by a thousand cuts: the challenges and diverse landscape of lignocellulosic hydrolysate inhibitors Piotrowski, Jeff S.; Zhang, Yaoping; Bates, Donna M. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00090	journal	March 2014
Aromatic inhibitors derived from ammonia-pretreated lignocellulose hinder bacterial ethanologenesis by activating regulatory circuits controlling inhibitor efflux and detoxification Keating, David H.; Zhang, Yaoping; Ong, Irene M. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00402	journal	August 2014
A Markerless Method for Genome Engineering in Zymomonas mobilis ZM4 Lal, Piyush Behari; Wells, Fritz M.; Lyu, Yucai Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02216	journal	October 2019
Gene Silencing Through CRISPR Interference in Bacteria: Current Advances and Future Prospects Zhang, Riyu; Xu, Wensheng; Shao, Shuai Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.635227	journal	March 2021
Genome Copy Number Quantification Revealed That the Ethanologenic Alpha-Proteobacterium Zymomonas mobilis Is Polyploid Fuchino, Katsuya; Wasser, Daniel; Soppa, Jörg Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.705895	journal	August 2021
The Chelating Ability of Plant Polyphenols Can Affect Iron Homeostasis and Gut Microbiota Scarano, Aurelia; Laddomada, Barbara; Blando, Federica Antioxidants, Vol. 12, Issue 3 https://doi.org/10.3390/antiox12030630	journal	March 2023
Phenolic Acid Profiles and Antioxidant Activity of Major Cereal Crops Horvat, Daniela; Šimić, Gordana; Drezner, Georg Antioxidants, Vol. 9, Issue 6 https://doi.org/10.3390/antiox9060527	journal	June 2020
Ferredoxins: Functions, Evolution, Potential Applications, and Challenges of Subtype Classification Syed, Khajamohiddin Current Issues in Molecular Biology, Vol. 46, Issue 9 https://doi.org/10.3390/cimb46090574	journal	September 2024

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