Environmental Conditions Modulate the Transcriptomic Response of Both Caulobacter crescentus Morphotypes to Cu Stress.

Laurens Maertens,Pauline Cherry,Françoise Tilquin,Rob Van Houdt,Jean-Yves Matroule

doi:10.3390/microorganisms9061116

Laurens Maertens, Pauline Cherry + Show 3 more

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https://doi.org/10.3390/microorganisms9061116

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Abstract

Bacteria encounter elevated copper (Cu) concentrations in multiple environments, varying from mining wastes to antimicrobial applications of copper. As the role of the environment in the bacterial response to Cu ion exposure remains elusive, we used a tagRNA-seq approach to elucidate the disparate responses of two morphotypes of Caulobacter crescentus NA1000 to moderate Cu stress in a complex rich (PYE) medium and a defined poor (M2G) medium. The transcriptome was more responsive in M2G, where we observed an extensive oxidative stress response and reconfiguration of the proteome, as well as the induction of metal resistance clusters. In PYE, little evidence was found for an oxidative stress response, but several transport systems were differentially expressed, and an increased need for histidine was apparent. These results show that the Cu stress response is strongly dependent on the cellular environment. In addition, induction of the extracytoplasmic function sigma factor SigF and its regulon was shared by the Cu stress responses in both media, and its central role was confirmed by the phenotypic screening of a sigF::Tn5 mutant. In both media, stalked cells were more responsive to Cu stress than swarmer cells, and a stronger basal expression of several cell protection systems was noted, indicating that the swarmer cell is inherently more Cu resistant. Our approach also allowed for detecting several new transcription start sites, putatively indicating small regulatory RNAs, and additional levels of Cu-responsive regulation.

Highlights

Published: 21 May 2021Copper (Cu) is an essential micronutrient for all living organisms, but elevated intracellular concentrations can quickly lead to toxic effects
The effect of Cu on the growth of C. crescentus in M2G and PYE medium was compared via biomass accumulation after 24 h (Figure 2)
Cross-study transcriptome results are difficult to compare due to variability in, e.g., experimental setup, measurement sensitivity, and statistical methods, we examined the correlation of our results with existing datasets

Summary

Introduction

Copper (Cu) is an essential micronutrient for all living organisms, but elevated intracellular concentrations can quickly lead to toxic effects. Elevated Cu ion concentrations in the environment can originate from both natural and anthropogenic sources, with the latter including sources such as mining, smelting, domestic waste emission, and pesticide runoff [1]. Cu contamination in the environment is a growing issue, it is necessary to gain a thorough understanding of the biological response to this stressor. Microorganisms can come into contact with toxic Cu ion concentrations in macrophages, which use the metal to combat invading microbes [2]. New Cu-based antimicrobial therapies are in development as alternatives for traditional organic antibiotics [3]. The influence of a variable environment on the microbial Cu stress response remains elusive

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