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

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 investig...

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Autores principales: Huddy, Robert J., Sachdeva, Rohan, Kadzinga, Fadzai, Kantor, Rose S., Harrison, Susan T. L., Banfield, Jillian F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8061750/
https://www.ncbi.nlm.nih.gov/pubmed/33897653
http://dx.doi.org/10.3389/fmicb.2021.643368
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author Huddy, Robert J.
Sachdeva, Rohan
Kadzinga, Fadzai
Kantor, Rose S.
Harrison, Susan T. L.
Banfield, Jillian F.
author_facet Huddy, Robert J.
Sachdeva, Rohan
Kadzinga, Fadzai
Kantor, Rose S.
Harrison, Susan T. L.
Banfield, Jillian F.
author_sort Huddy, Robert J.
collection PubMed
description 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 CO(2) via cyanate hydratase, and fix CO(2) 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.
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spelling pubmed-80617502021-04-23 Thiocyanate and Organic Carbon Inputs Drive Convergent Selection for Specific Autotrophic Afipia and Thiobacillus Strains Within Complex Microbiomes Huddy, Robert J. Sachdeva, Rohan Kadzinga, Fadzai Kantor, Rose S. Harrison, Susan T. L. Banfield, Jillian F. Front Microbiol Microbiology 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 CO(2) via cyanate hydratase, and fix CO(2) 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. Frontiers Media S.A. 2021-04-08 /pmc/articles/PMC8061750/ /pubmed/33897653 http://dx.doi.org/10.3389/fmicb.2021.643368 Text en Copyright © 2021 Huddy, Sachdeva, Kadzinga, Kantor, Harrison and Banfield. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Huddy, Robert J.
Sachdeva, Rohan
Kadzinga, Fadzai
Kantor, Rose S.
Harrison, Susan T. L.
Banfield, Jillian F.
Thiocyanate and Organic Carbon Inputs Drive Convergent Selection for Specific Autotrophic Afipia and Thiobacillus Strains Within Complex Microbiomes
title Thiocyanate and Organic Carbon Inputs Drive Convergent Selection for Specific Autotrophic Afipia and Thiobacillus Strains Within Complex Microbiomes
title_full Thiocyanate and Organic Carbon Inputs Drive Convergent Selection for Specific Autotrophic Afipia and Thiobacillus Strains Within Complex Microbiomes
title_fullStr Thiocyanate and Organic Carbon Inputs Drive Convergent Selection for Specific Autotrophic Afipia and Thiobacillus Strains Within Complex Microbiomes
title_full_unstemmed Thiocyanate and Organic Carbon Inputs Drive Convergent Selection for Specific Autotrophic Afipia and Thiobacillus Strains Within Complex Microbiomes
title_short Thiocyanate and Organic Carbon Inputs Drive Convergent Selection for Specific Autotrophic Afipia and Thiobacillus Strains Within Complex Microbiomes
title_sort thiocyanate and organic carbon inputs drive convergent selection for specific autotrophic afipia and thiobacillus strains within complex microbiomes
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8061750/
https://www.ncbi.nlm.nih.gov/pubmed/33897653
http://dx.doi.org/10.3389/fmicb.2021.643368
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