Anion transport as a target of adaption to perchlorate in sulfate-reducing communities
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. Finally, this highlights the value of probing evolutionary questions in an ecological framework,more »
- Authors:
-
- Univ. of California, Berkeley, CA (United States); Energy Biosciences Inst., Berkeley, CA (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Univ. of California, Berkeley, CA (United States); Univ. of Otago, Dunedin (New Zealand)
- Univ. of California, Berkeley, CA (United States); Energy Biosciences Inst., Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1634072
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- The ISME Journal
- Additional Journal Information:
- Journal Volume: 14; Journal Issue: 2; Journal ID: ISSN 1751-7362
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; comparative genomics; microbial ecology
Citation Formats
Stoeva, Magdalena K., Kuehl, Jennifer, Kazakov, Alexey E., Wang, Ouwei, Rushton-Green, Rowena, and Coates, John D. Anion transport as a target of adaption to perchlorate in sulfate-reducing communities. United States: N. p., 2019.
Web. doi:10.1038/s41396-019-0540-7.
Stoeva, Magdalena K., Kuehl, Jennifer, Kazakov, Alexey E., Wang, Ouwei, Rushton-Green, Rowena, & Coates, John D. Anion transport as a target of adaption to perchlorate in sulfate-reducing communities. United States. https://doi.org/10.1038/s41396-019-0540-7
Stoeva, Magdalena K., Kuehl, Jennifer, Kazakov, Alexey E., Wang, Ouwei, Rushton-Green, Rowena, and Coates, John D. Mon .
"Anion transport as a target of adaption to perchlorate in sulfate-reducing communities". United States. https://doi.org/10.1038/s41396-019-0540-7. https://www.osti.gov/servlets/purl/1634072.
@article{osti_1634072,
title = {Anion transport as a target of adaption to perchlorate in sulfate-reducing communities},
author = {Stoeva, Magdalena K. and Kuehl, Jennifer and Kazakov, Alexey E. and Wang, Ouwei and Rushton-Green, Rowena and Coates, John D.},
abstractNote = {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. Finally, this highlights the value of probing evolutionary questions in an ecological framework, bridging the gap between ecology, evolution, genomics, and physiology.},
doi = {10.1038/s41396-019-0540-7},
journal = {The ISME Journal},
number = 2,
volume = 14,
place = {United States},
year = {Mon Oct 28 00:00:00 EDT 2019},
month = {Mon Oct 28 00:00:00 EDT 2019}
}
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