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Thiocyanate and organic carbon inputs drive convergent selection for specific autotrophic Afipia and Thiobacillus strains within complex microbiomes

Robert J. Huddy, Rohan Sachdeva, Fadzai Kadzinga, Rose Kantor, Susan T.L. Harrison, Jillian F. Banfield
doi: https://doi.org/10.1101/2020.04.29.067207
Robert J. Huddy
1The Center for Bioprocess Engineering Research, University of Cape Town, South Africa
2The Future Water Institute, University of Cape Town, South Africa
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Rohan Sachdeva
3The Innovative Genomics Institute at the University of California, Berkeley, California, USA
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Fadzai Kadzinga
1The Center for Bioprocess Engineering Research, University of Cape Town, South Africa
2The Future Water Institute, University of Cape Town, South Africa
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Rose Kantor
4The Department of Earth and Planetary Science, University of California, Berkeley, California, USA
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Susan T.L. Harrison
1The Center for Bioprocess Engineering Research, University of Cape Town, South Africa
2The Future Water Institute, University of Cape Town, South Africa
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Jillian F. Banfield
3The Innovative Genomics Institute at the University of California, Berkeley, California, USA
4The Department of Earth and Planetary Science, University of California, Berkeley, California, USA
5The Department of Environmental Science, Policy and Management, University of California, Berkeley, California, USA
6The University of Melbourne, Victoria, Australia
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  • For correspondence: jbanfield@berkeley.edu
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Abstract

Thiocyanate (SCN-) contamination threatens aquatic ecosystems and pollutes vital fresh water supplies. SCN- degrading microbial consortia are commercially deployed for remediation, but the impact of organic amendments on selection within SCN- degrading microbial communities has not been investigated. Here, we tested whether specific strains capable of degrading SCN- could be reproducibly selected for based on SCN- loading and the presence or absence of added organic carbon. Complex microbial communities derived from those used to treat SCN- contaminated water were exposed to systematically increased input SCN concentrations in molasses-amended and -unamended reactors and in reactors switched to unamended conditions after establishing the active SCN- degrading consortium. Five experiments were conducted over 790 days and genome-resolved metagenomics was used to resolve community composition at the strain level. A single Thiobacillus strain proliferated in all reactors at high loadings. Despite the presence of many Rhizobiales strains, a single Afipia variant dominated the molasses-free reactor at moderately high loadings. This strain is predicted to breakdown SCN- using a novel thiocyanate dehydrogenase, oxidize resulting reduced sulfur, degrade product cyanate (OCN−) to ammonia and CO2 via cyanase, and fix CO2 via the Calvin-Benson-Bassham cycle. Removal of molasses from input feed solutions reproducibly led to dominance of this strain. Neither this Afipia strain nor the thiobacilli have the capacity to produce cobalamin, a function detected in low abundance community members. Although sustained by autotrophy, reactors without molasses did not stably degrade SCN- at high loading rates, perhaps due to loss of biofilm-associated niche diversity. Overall, convergence in environmental conditions led to convergence in the strain composition, although reactor history also impacted the trajectory of community compositional change.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted April 30, 2020.
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Thiocyanate and organic carbon inputs drive convergent selection for specific autotrophic Afipia and Thiobacillus strains within complex microbiomes
Robert J. Huddy, Rohan Sachdeva, Fadzai Kadzinga, Rose Kantor, Susan T.L. Harrison, Jillian F. Banfield
bioRxiv 2020.04.29.067207; doi: https://doi.org/10.1101/2020.04.29.067207
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Thiocyanate and organic carbon inputs drive convergent selection for specific autotrophic Afipia and Thiobacillus strains within complex microbiomes
Robert J. Huddy, Rohan Sachdeva, Fadzai Kadzinga, Rose Kantor, Susan T.L. Harrison, Jillian F. Banfield
bioRxiv 2020.04.29.067207; doi: https://doi.org/10.1101/2020.04.29.067207

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