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Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale

BACKGROUND: Biogeochemical exports from watersheds are modulated by the activity of microorganisms that function over micron scales. Here, we tested the hypothesis that meander-bound regions share a core microbiome and exhibit patterns of metabolic potential that broadly predict biogeochemical proce...

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Autores principales: Matheus Carnevali, Paula B., Lavy, Adi, Thomas, Alex D., Crits-Christoph, Alexander, Diamond, Spencer, Méheust, Raphaël, Olm, Matthew R., Sharrar, Allison, Lei, Shufei, Dong, Wenming, Falco, Nicola, Bouskill, Nicholas, Newcomer, Michelle E., Nico, Peter, Wainwright, Haruko, Dwivedi, Dipankar, Williams, Kenneth H., Hubbard, Susan, Banfield, Jillian F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8141241/
https://www.ncbi.nlm.nih.gov/pubmed/34022966
http://dx.doi.org/10.1186/s40168-020-00957-z
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author Matheus Carnevali, Paula B.
Lavy, Adi
Thomas, Alex D.
Crits-Christoph, Alexander
Diamond, Spencer
Méheust, Raphaël
Olm, Matthew R.
Sharrar, Allison
Lei, Shufei
Dong, Wenming
Falco, Nicola
Bouskill, Nicholas
Newcomer, Michelle E.
Nico, Peter
Wainwright, Haruko
Dwivedi, Dipankar
Williams, Kenneth H.
Hubbard, Susan
Banfield, Jillian F.
author_facet Matheus Carnevali, Paula B.
Lavy, Adi
Thomas, Alex D.
Crits-Christoph, Alexander
Diamond, Spencer
Méheust, Raphaël
Olm, Matthew R.
Sharrar, Allison
Lei, Shufei
Dong, Wenming
Falco, Nicola
Bouskill, Nicholas
Newcomer, Michelle E.
Nico, Peter
Wainwright, Haruko
Dwivedi, Dipankar
Williams, Kenneth H.
Hubbard, Susan
Banfield, Jillian F.
author_sort Matheus Carnevali, Paula B.
collection PubMed
description BACKGROUND: Biogeochemical exports from watersheds are modulated by the activity of microorganisms that function over micron scales. Here, we tested the hypothesis that meander-bound regions share a core microbiome and exhibit patterns of metabolic potential that broadly predict biogeochemical processes in floodplain soils along a river corridor. RESULTS: We intensively sampled the microbiomes of floodplain soils located in the upper, middle, and lower reaches of the East River, Colorado. Despite the very high microbial diversity and complexity of the soils, we reconstructed 248 quality draft genomes representative of subspecies. Approximately one third of these bacterial subspecies was detected across all three locations at similar abundance levels, and ~ 15% of species were detected in two consecutive years. Within the meander-bound floodplains, we did not detect systematic patterns of gene abundance based on sampling position relative to the river. However, across meanders, we identified a core floodplain microbiome that is enriched in capacities for aerobic respiration, aerobic CO oxidation, and thiosulfate oxidation with the formation of elemental sulfur. Given this, we conducted a transcriptomic analysis of the middle floodplain. In contrast to predictions made based on the prominence of gene inventories, the most highly transcribed genes were relatively rare amoCAB and nxrAB (for nitrification) genes, followed by genes involved in methanol and formate oxidation, and nitrogen and CO(2) fixation. Within all three meanders, low soil organic carbon correlated with high activity of genes involved in methanol, formate, sulfide, hydrogen, and ammonia oxidation, nitrite oxidoreduction, and nitrate and nitrite reduction. Overall, the results emphasize the importance of sulfur, one-carbon and nitrogen compound metabolism in soils of the riparian corridor. CONCLUSIONS: The disparity between the scale of a microbial cell and the scale of a watershed currently limits the development of genomically informed predictive models describing watershed biogeochemical function. Meander-bound floodplains appear to serve as scaling motifs that predict aggregate capacities for biogeochemical transformations, providing a foundation for incorporating riparian soil microbiomes in watershed models. Widely represented genetic capacities did not predict in situ activity at one time point, but rather they define a reservoir of biogeochemical potential available as conditions change. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-020-00957-z.
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spelling pubmed-81412412021-05-25 Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale Matheus Carnevali, Paula B. Lavy, Adi Thomas, Alex D. Crits-Christoph, Alexander Diamond, Spencer Méheust, Raphaël Olm, Matthew R. Sharrar, Allison Lei, Shufei Dong, Wenming Falco, Nicola Bouskill, Nicholas Newcomer, Michelle E. Nico, Peter Wainwright, Haruko Dwivedi, Dipankar Williams, Kenneth H. Hubbard, Susan Banfield, Jillian F. Microbiome Research BACKGROUND: Biogeochemical exports from watersheds are modulated by the activity of microorganisms that function over micron scales. Here, we tested the hypothesis that meander-bound regions share a core microbiome and exhibit patterns of metabolic potential that broadly predict biogeochemical processes in floodplain soils along a river corridor. RESULTS: We intensively sampled the microbiomes of floodplain soils located in the upper, middle, and lower reaches of the East River, Colorado. Despite the very high microbial diversity and complexity of the soils, we reconstructed 248 quality draft genomes representative of subspecies. Approximately one third of these bacterial subspecies was detected across all three locations at similar abundance levels, and ~ 15% of species were detected in two consecutive years. Within the meander-bound floodplains, we did not detect systematic patterns of gene abundance based on sampling position relative to the river. However, across meanders, we identified a core floodplain microbiome that is enriched in capacities for aerobic respiration, aerobic CO oxidation, and thiosulfate oxidation with the formation of elemental sulfur. Given this, we conducted a transcriptomic analysis of the middle floodplain. In contrast to predictions made based on the prominence of gene inventories, the most highly transcribed genes were relatively rare amoCAB and nxrAB (for nitrification) genes, followed by genes involved in methanol and formate oxidation, and nitrogen and CO(2) fixation. Within all three meanders, low soil organic carbon correlated with high activity of genes involved in methanol, formate, sulfide, hydrogen, and ammonia oxidation, nitrite oxidoreduction, and nitrate and nitrite reduction. Overall, the results emphasize the importance of sulfur, one-carbon and nitrogen compound metabolism in soils of the riparian corridor. CONCLUSIONS: The disparity between the scale of a microbial cell and the scale of a watershed currently limits the development of genomically informed predictive models describing watershed biogeochemical function. Meander-bound floodplains appear to serve as scaling motifs that predict aggregate capacities for biogeochemical transformations, providing a foundation for incorporating riparian soil microbiomes in watershed models. Widely represented genetic capacities did not predict in situ activity at one time point, but rather they define a reservoir of biogeochemical potential available as conditions change. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-020-00957-z. BioMed Central 2021-05-22 /pmc/articles/PMC8141241/ /pubmed/34022966 http://dx.doi.org/10.1186/s40168-020-00957-z Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Matheus Carnevali, Paula B.
Lavy, Adi
Thomas, Alex D.
Crits-Christoph, Alexander
Diamond, Spencer
Méheust, Raphaël
Olm, Matthew R.
Sharrar, Allison
Lei, Shufei
Dong, Wenming
Falco, Nicola
Bouskill, Nicholas
Newcomer, Michelle E.
Nico, Peter
Wainwright, Haruko
Dwivedi, Dipankar
Williams, Kenneth H.
Hubbard, Susan
Banfield, Jillian F.
Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale
title Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale
title_full Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale
title_fullStr Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale
title_full_unstemmed Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale
title_short Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale
title_sort meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8141241/
https://www.ncbi.nlm.nih.gov/pubmed/34022966
http://dx.doi.org/10.1186/s40168-020-00957-z
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