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Environmental Microbiology | Spotlight

Year-Round Shotgun Metagenomes Reveal Stable Microbial Communities in Agricultural Soils and Novel Ammonia Oxidizers Responding to Fertilization

Luis H. Orellana, Joanne C. Chee-Sanford, Robert A. Sanford, Frank E. Löffler, Konstantinos T. Konstantinidis
Marie A. Elliot, Editor
Luis H. Orellana
aGeorgia Institute of Technology, Atlanta, Georgia, USA
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Joanne C. Chee-Sanford
bU.S. Department of Agriculture, Agricultural Research Service, Urbana, Illinois, USA
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Robert A. Sanford
cUniversity of Illinois at Urbana-Champaign, Urbana, Illinois, USA
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Frank E. Löffler
dUniversity of Tennessee, Knoxville, Tennessee, USA
eBiosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA
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  • ORCID record for Frank E. Löffler
Konstantinos T. Konstantinidis
aGeorgia Institute of Technology, Atlanta, Georgia, USA
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Marie A. Elliot
McMaster University
Roles: Editor
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DOI: 10.1128/AEM.01646-17
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ABSTRACT

The dynamics of individual microbial populations and their gene functions in agricultural soils, especially after major activities such as nitrogen (N) fertilization, remain elusive but are important for a better understanding of nutrient cycling. Here, we analyzed 20 short-read metagenomes collected at four time points during 1 year from two depths (0 to 5 and 20 to 30 cm) in two Midwestern agricultural sites representing contrasting soil textures (sandy versus silty loam) with similar cropping histories. Although the microbial community taxonomic and functional compositions differed between the two locations and depths, they were more stable within a depth/site throughout the year than communities in natural aquatic ecosystems. For example, among the 69 population genomes assembled from the metagenomes, 75% showed a less than 2-fold change in abundance between any two sampling points. Interestingly, six deep-branching Thaumarchaeota and three complete ammonia oxidizer (comammox) Nitrospira populations increased up to 5-fold in abundance upon the addition of N fertilizer. These results indicated that indigenous archaeal ammonia oxidizers may respond faster (are more copiotrophic) to N fertilization than previously thought. None of 29 recovered putative denitrifier genomes encoded the complete denitrification pathway, suggesting that denitrification is carried out by a collection of different populations. Altogether, our study identified novel microbial populations and genes responding to seasonal and human-induced perturbations in agricultural soils that should facilitate future monitoring efforts and N-related studies.

IMPORTANCE Even though the impact of agricultural management on the microbial community structure has been recognized, an understanding of the dynamics of individual microbial populations and what functions each population carries are limited. Yet, this information is important for a better understanding of nutrient cycling, with potentially important implications for preserving nitrogen in soils and sustainability. Here, we show that reconstructed metagenome-assembled genomes (MAGs) are relatively stable in their abundance and functional gene content year round, and seasonal nitrogen fertilization has selected for novel Thaumarchaeota and comammox Nitrospira nitrifiers that are potentially less oligotrophic than their marine counterparts previously studied.

FOOTNOTES

    • Received 9 August 2017.
    • Accepted 29 October 2017.
    • Accepted manuscript posted online 3 November 2017.
  • Supplemental material for this article may be found at https://doi.org/10.1128/AEM.01646-17.

  • Copyright © 2018 American Society for Microbiology.

All Rights Reserved.

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Year-Round Shotgun Metagenomes Reveal Stable Microbial Communities in Agricultural Soils and Novel Ammonia Oxidizers Responding to Fertilization
Luis H. Orellana, Joanne C. Chee-Sanford, Robert A. Sanford, Frank E. Löffler, Konstantinos T. Konstantinidis
Applied and Environmental Microbiology Jan 2018, 84 (2) e01646-17; DOI: 10.1128/AEM.01646-17

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Year-Round Shotgun Metagenomes Reveal Stable Microbial Communities in Agricultural Soils and Novel Ammonia Oxidizers Responding to Fertilization
Luis H. Orellana, Joanne C. Chee-Sanford, Robert A. Sanford, Frank E. Löffler, Konstantinos T. Konstantinidis
Applied and Environmental Microbiology Jan 2018, 84 (2) e01646-17; DOI: 10.1128/AEM.01646-17
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KEYWORDS

metagenomics
nitrifiers
soil microbiology
seasonal dynamics

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