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

Abstract

Abstract 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 amoCABmore » 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.« less

Authors:
; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ORCiD logo
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23), Climate and Environmental Sciences Division (SC-23.1)
OSTI Identifier:
1784409
Alternate Identifier(s):
OSTI ID: 1797752
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Published Article
Journal Name:
Microbiome
Additional Journal Information:
Journal Name: Microbiome Journal Volume: 9 Journal Issue: 1; Journal ID: ISSN 2049-2618
Publisher:
Springer Science + Business Media
Country of Publication:
United Kingdom
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; Microbiome; Floodplain; Soil; Watershed; Genome-resolved metagenomics; Metatranscriptomics

Citation Formats

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, and Banfield, Jillian F. Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale. United Kingdom: N. p., 2021. Web. doi:10.1186/s40168-020-00957-z.
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. United Kingdom. https://doi.org/10.1186/s40168-020-00957-z
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, and Banfield, Jillian F. Sat . "Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale". United Kingdom. https://doi.org/10.1186/s40168-020-00957-z.
@article{osti_1784409,
title = {Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale},
author = {Matheus Carnevali, Paula B. and Lavy, Adi and Thomas, Alex D. and Crits-Christoph, Alexander and Diamond, Spencer and Méheust, Raphaël and Olm, Matthew R. and Sharrar, Allison and Lei, Shufei and Dong, Wenming and Falco, Nicola and Bouskill, Nicholas and Newcomer, Michelle E. and Nico, Peter and Wainwright, Haruko and Dwivedi, Dipankar and Williams, Kenneth H. and Hubbard, Susan and Banfield, Jillian F.},
abstractNote = {Abstract 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.},
doi = {10.1186/s40168-020-00957-z},
journal = {Microbiome},
number = 1,
volume = 9,
place = {United Kingdom},
year = {Sat May 22 00:00:00 EDT 2021},
month = {Sat May 22 00:00:00 EDT 2021}
}

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