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Diverse Thaumarchaeota Dominate Subsurface Ammonia-oxidizing Communities in Semi-arid Floodplains in the Western United States

  • Environmental Microbiology
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Abstract

Subsurface microbial communities mediate biogeochemical transformations that drive both local and ecosystem-level cycling of essential elements, including nitrogen. However, their study has been largely limited to the deep ocean, terrestrial mines, caves, and topsoils (< 30 cm). Here, we present regional insights into the microbial ecology of aerobic ammonia oxidation within the terrestrial subsurface of five semi-arid riparian sites spanning a 900-km N-S transect. We sampled sediments, profiled communities to depths of ≤ 10 m, and compared them to reveal trends regionally within and surrounding the Upper Colorado River Basin (CRB). The diversity and abundance of ammonia-oxidizing microbial communities were evaluated in the context of subsurface geochemistry by applying a combination of amoA (encoding ammonia monooxygenase subunit A) gene sequencing, quantitative PCR, and geochemical techniques. Analysis of 898 amoA sequences from ammonia-oxidizing archaea (AOA) and bacteria (AOB) revealed extensive ecosystem-scale diversity, including archaeal amoA sequences from four of the five major AOA lineages currently found worldwide as well as distinct AOA ecotypes associated with naturally reduced zones (NRZs) and hydrogeochemical zones (unsaturated, capillary fringe, and saturated). Overall, AOA outnumber AOB by 2- to 5000-fold over this regional scale, suggesting that AOA may play a prominent biogeochemical role in nitrification within terrestrial subsurface sediments.

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Acknowledgments

We thank Vincent Noël, Kristin Boye, Juan de la Paz, Kenneth Williams, and William Dam for their assistance accessing and collecting the samples described. The authors would also like to acknowledge Kolyne DeJesus for her assistance preparing and analyzing geochemical properties of samples and Bradley Tolar for providing useful feedback on an earlier version of this manuscript.

Funding

Funding was provided by the DOE Office of Biological and Environmental Research, Subsurface Biogeochemistry Research (SBR) activity to the SLAC SFA program under contract DE-AC02-76SF00515 to SLAC and to the LBL Watershed Function SFA under Award Number DE-AC02-05CH11231, as well as contract DE-SC0019119 to C.A.F. SSRL and SLAC are supported by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences under Contract No. DE-AC02-76SF00515, the DOE Office of Biological and Environmental Research, and by the National Institutes of Health, National Institute of General Medical Sciences (including P41GM103393). We gratefully acknowledge substantial logistical support from the US Department of Energy, Office of Legacy Management, which provided access to the Riverton, Shiprock, Naturita, and Grand Junction field sites, obtained permits for operations, provided ES&H support, and conducted drilling operations. Access to the Rifle field site, logistical support, and drilling operations were provided by the LBNL Watershed Function SFA.

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Authors and Affiliations

  1. Department of Earth System Science, Stanford University, Stanford, CA, 94305-4216, USA

    Emily L. Cardarelli & Christopher A. Francis

  2. Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, Menlo Park, CA, 94025, USA

    John R. Bargar

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  1. Emily L. Cardarelli
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  2. John R. Bargar
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  3. Christopher A. Francis
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Correspondence to Christopher A. Francis.

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Cardarelli, E.L., Bargar, J.R. & Francis, C.A. Diverse Thaumarchaeota Dominate Subsurface Ammonia-oxidizing Communities in Semi-arid Floodplains in the Western United States. Microb Ecol 80, 778–792 (2020). https://doi.org/10.1007/s00248-020-01534-5

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