Abstract
Inhibitors can be used to control the functionality of microbial communities by targeting specific metabolisms. The targeted inhibition of dissimilatory sulfate reduction limits the generation of toxic and corrosive hydrogen sulfide across several industrial systems. Sulfate-reducing microorganisms (SRM) are specifically inhibited by sulfate analogs, such as perchlorate. Previously, we showed pure culture SRM adaptation to perchlorate stress through mutation of the sulfate adenylyltransferase, a central enzyme in the sulfate reduction pathway. Here, we explored adaptation to perchlorate across unconstrained SRM on a community scale. We followed natural and bio-augmented sulfidogenic communities through serial transfers in increasing concentrations of perchlorate. Our results demonstrated that perchlorate stress altered community structure by initially selecting for innately more resistant strains. Isolation, whole-genome sequencing, and molecular biology techniques allowed us to define subsequent genetic mechanisms of adaptation that arose across the dominant adapting SRM. Changes in the regulation of divalent anion:sodium symporter family transporters led to increased intracellular sulfate to perchlorate ratios, allowing SRM to escape the effects of competitive inhibition. Thus, in contrast to pure-culture results, SRM in communities cope with perchlorate stress via changes in anion transport and its regulation. This highlights the value of probing evolutionary questions in an ecological framework, bridging the gap between ecology, evolution, genomics, and physiology.
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Acknowledgements
We would like to thank Andrew Jackson (Texas Tech University) for intracellular sulfate and perchlorate analysis, Grant Zane and the Judy Wall lab (University of Missouri) for discussions regarding overexpression in SRM, Angeliki Marietou (Aarhus University, Denmark) for discussions regarding SRM transporters, Misha Mehta for the FREQseq experiment, Tyler P. Barnum for editing the manuscript and figures, and Anchal Mehra and Nicholas Garcia for general support. Funding support for research on microbial sulfate reduction was generously provided by the Energy Biosciences Institute through their BP research program to JDC. All sequencing data is publicly available under the NCBI BioProject ID PRJNA560652.
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Stoeva, M.K., Kuehl, J., Kazakov, A.E. et al. Anion transport as a target of adaption to perchlorate in sulfate-reducing communities. ISME J 14, 450–462 (2020). https://doi.org/10.1038/s41396-019-0540-7
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DOI: https://doi.org/10.1038/s41396-019-0540-7
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