Abstract

The ability to perceive and respond to environmental change is essential to all organisms. In response to nutrient depletion, cells of the soil-dwelling δ-proteobacterium Myxococcus xanthus undergo collective morphogenesis into multicellular fruiting bodies and transform into stress-resistant spores. This process is strictly regulated by gene networks that incorporate both inter- and intracellular signals. While commonly studied M. xanthus reference strains and some natural isolates undergo development only in nutrient-poor conditions, some lab mutants and other natural isolates commit to development at much higher nutrient levels, but mechanisms enabling such rich medium development remain elusive. Here we investigate the genetic basis of rich medium development in one mutant and find that a single amino acid change (S534L) in RpoB, the β-subunit of RNA polymerase, is responsible for the phenotype. Ectopic expression of the mutant rpoB allele was sufficient to induce nutrient-rich development. These results suggest that the universal bacterial transcription machinery bearing the altered β-subunit can relax regulation of developmental genes that are normally strictly controlled by the bacterial stringent response. Moreover, the mutation also pleiotropically mediates a tradeoff in fitness during vegetative growth between high vs. low nutrient conditions and generates resistance to exploitation by a developmental cheater. Our findings reveal a previously unknown connection between the universal transcription machinery and one of the most behaviorally complex responses to environmental stress found among bacteria.

Highlights

  • Sensing and responding to varying nutrient availability are crucial to all forms of life

  • Proficiency at rich medium (RM) development is evident in sporulation assays (Figure 1B)

  • The three remaining mutations resulting in a R253L (CGT → CTT) substitution in Mxan_0795, S534L (TCG → TTG) in rpoB (β-subunit of DNA-directed RNA polymerase, RNAP), and V162I (GTC → ATC) in Mxan_6547 (TonB-dependent receptor) were considered as candidates for causing RM development

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Summary

Introduction

Sensing and responding to varying nutrient availability are crucial to all forms of life. A broadly conserved mechanism for responding to nutrient limitation is the stringent response, which was first discovered in Escherichia coli and has since been found throughout the bacterial domain (Chatterji and Kumar Ojha, 2001; Boutte and Crosson, 2013; Shimizu, 2014). Guanosine-5′-(tri)di-3′-diphosphate ((p)ppGpp) accumulates in response to amino rpoB Mutation Controls Developmental Initiation acid starvation and causes major transcriptional changes that promote survival under stress. These changes include inhibition of stable rRNA synthesis and increased transcription of amino acid biosynthetic operons and stress-adaptive genes (Chatterji and Kumar Ojha, 2001; Diodati et al, 2014; Sharma et al, 2021)

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