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

Paula B. Matheus Carnevali, Adi Lavy, Alex D. Thomas, Alexander Crits-Christoph, Spencer Diamond, Raphaël Méheust, Matthew R. Olm, Allison Sharrar, Shufei Lei, Wenming Dong, Nicola Falco, Nicholas Bouskill, Michelle E. Newcomer, Peter Nico, Haruko Wainwright, Dipankar Dwivedi, Kenneth H. Williams, Susan Hubbard, Jillian F. Banfield

Research output: Contribution to journalArticlepeer-review

17 Scopus citations

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 CO2 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. [MediaObject not available: see fulltext.]

Original languageEnglish
Article number121
JournalMicrobiome
Volume9
Issue number1
DOIs
StatePublished - Dec 2021
Externally publishedYes

Funding

We are grateful to Chad Hobson, David McGrath, and Rosemary Carrol for their support in the field during sample collection; to Joel Rowland (Los Alamos National Lab) and Helen Malenda (USGS) for their useful insights, and to Kate Lane, Brian C. Thomas, and Rohan Sachdeva for their technical support. We thank the Rocky Mountain Biological Laboratory for the lab space at the field site. This work was supported as part of the Watershed Function Scientific Focus Area funded by the US Department of Energy, Office of Science, Office of Biological and Environmental Research under Award Number DE-AC02-05CH11231. Sequencing was conducted at the Joint Genome Institute (a DOE Office of Science User Facility) under a CSP award.

FundersFunder number
Rocky Mountain Biological Laboratory
U.S. Department of Energy
Office of Science
Biological and Environmental ResearchDE-AC02-05CH11231

    Keywords

    • Floodplain
    • Genome-resolved metagenomics
    • Metatranscriptomics
    • Microbiome
    • Soil
    • Watershed

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