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 S Kantor; Susan T L Harrison; Jillian F Banfield

doi:10.3389/fmicb.2021.643368

Thiocyanate and Organic Carbon Inputs Drive Convergent Selection for Specific Autotrophic Afipia and Thiobacillus Strains Within Complex Microbiomes

Front Microbiol. 2021 Apr 8:12:643368. doi: 10.3389/fmicb.2021.643368. eCollection 2021.

Authors

Robert J Huddy^{1

2}, Rohan Sachdeva³, Fadzai Kadzinga^{1

2}, Rose S Kantor⁴, Susan T L Harrison^{1

2}, Jillian F Banfield^{3

4

5

6}

Affiliations

¹ Centre for Bioprocess Engineering Research, University of Cape Town, Cape Town, South Africa.
² Future Water Institute, University of Cape Town, Cape Town, South Africa.
³ Innovative Genomics Institute, University of California, Berkeley, Berkeley, CA, United States.
⁴ Department of Earth and Planetary Science, University of California, Berkeley, Berkeley, CA, United States.
⁵ Department of Environmental Science, Policy, and Management, University of California, Berkeley, Berkeley, CA, United States.
⁶ School of Earth Sciences, University of Melbourne, Melbourne, VIC, Australia.

Abstract

Thiocyanate (SCN^-) contamination threatens aquatic ecosystems and pollutes vital freshwater supplies. SCN^--degrading microbial consortia are commercially adapted 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 break down SCN^- using a novel thiocyanate desulfurase, oxidize resulting reduced sulfur, degrade product cyanate to ammonia and CO₂ via cyanate hydratase, and fix CO₂ via the Calvin-Benson-Bassham cycle. Removal of molasses from input feed solutions reproducibly led to dominance of this strain. 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.

Keywords: bioremediation; metagenomics; microbiome; pollution; thiocyanate.