The genetics of aerotolerant growth in an alphaproteobacterium with a naturally reduced genome

Enright, Amy L.; Banta, Amy B.; Ward, Ryan D.; Vazquez, Julio Rivera; Felczak, Magdalena M.; Wolfe, Michael B.; TerAvest, Michaela A.; Amador-Noguez, Daniel; Peters, Jason M.

doi:10.1128/mbio.01487-23

Title: The genetics of aerotolerant growth in an alphaproteobacterium with a naturally reduced genome

Journal Article · 18 December 2023 · mBio (Online)

DOI: https://doi.org/10.1128/mbio.01487-23 · OSTI ID:2294070

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^[2]; Vazquez, Julio Rivera ^[2]; Felczak, Magdalena M. ^[3]; Wolfe, Michael B. ^[2];

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University of Wisconsin-Madison, WI (United States); University of Wisconsin-Madison School of Pharmacy Pharmaceutical Sciences Division
University of Wisconsin-Madison, WI (United States)
University of Wisconsin-Madison, WI (United States); Michigan State University, East Lansing, MI (United States)

Reduced genome bacteria are genetically simplified systems that facilitate biological study and industrial use. The free-living alphaproteobacterium Zymomonas mobilis has a naturally reduced genome containing fewer than 2,000 protein-coding genes. Despite its small genome, Z. mobilis thrives in diverse conditions including the presence or absence of atmospheric oxygen. However, insufficient characterization of essential and conditionally essential genes has limited broader adoption of Z. mobilis as a model alphaproteobacterium. Here, we use genome-scale CRISPRi-seq (clustered regularly interspaced short palindromic repeats interference sequencing) to systematically identify and characterize Z. mobilis genes that are conditionally essential for aerotolerant or anaerobic growth or are generally essential across both conditions. Comparative genomics revealed that the essentiality of most “generally essential” genes was shared between Z. mobilis and other Alphaproteobacteria, validating Z. mobilis as a reduced genome model. Among conditionally essential genes, we found that the DNA repair gene, recJ, was critical only for aerobic growth but reduced the mutation rate under both conditions. Further, we show that genes encoding the F1FO ATP synthase and Rhodobacter nitrogen fixation (Rnf) respiratory complex are required for the anaerobic growth of Z. mobilis. Combining CRISPRi partial knockdowns with metabolomics and membrane potential measurements, we determined that the ATP synthase generates membrane potential that is consumed by Rnf to power downstream processes. Rnf knockdown strains accumulated isoprenoid biosynthesis intermediates, suggesting a key role for Rnf in powering essential biosynthetic reactions. Our work establishes Z. mobilis as a streamlined model for alphaproteobacterial genetics, has broad implications in bacterial energy coupling, and informs Z. mobilis genome manipulation for optimized production of valuable isoprenoid-based bioproducts.

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

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0018409

OSTI ID:: 2294070

Journal Information:: mBio (Online), Journal Name: mBio (Online) Journal Issue: 6 Vol. 14; ISSN 2150-7511

Publisher:: American Society for Microbiology (ASM)Copyright Statement

Country of Publication:: United States

Language:: English

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Title: The genetics of aerotolerant growth in an alphaproteobacterium with a naturally reduced genome

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