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

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ENVIRONMENTAL MICROBIOLOGY

Diverse Thaumarchaeota Dominate Subsurface Ammonia-oxidizing Communities in Semi-arid Floodplains in the Western United States Emily L. Cardarelli 1 & John R. Bargar 2 & Christopher A. Francis 1 Received: 13 February 2020 / Accepted: 29 May 2020 # Springer Science+Business Media, LLC, part of Springer Nature 2020

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. Keywords Terrestrial subsurface . amoA . Ammonia-oxidizing archaea . Ammonia-oxidizing bacteria . Nitrification . Thaumarchaeota

Introduction Ammonia-oxidizing microorganisms link reduced and oxidized pools of nitrogen (N) in the biosphere and thereby play a critical role in the global N cycle. Aerobic ammonia oxidation is the first and rate-limiting step of nitrification, a two-step process catalyzed by ammonia-oxidizing and nitrite-oxidizing microorganisms. Chemoautotrophic ammonia oxidizers were first discovered over 100 years ago [1] and long believed to Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00248-020-01534-5) contains supplementary material, which is available to authorized users. * Christopher A. Francis [email protected] 1

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

2

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

consist solely of Beta- and Gammaproteobacteria [2]. In the last 15 years, the capacity for ammonia oxidation has expanded to include Thaumarchaeota, previously classified as Marine Group I Crenarchaeota [3–5], which are globally u