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

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. In this paper, 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 ofmore » 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. 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. Finally, 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.« less

Authors:
 [1];  [2];  [3]; ORCiD logo [4];  [1]
  1. Georgia Inst. of Technology, Atlanta, GA (United States)
  2. USDA Agricultural Research Service, Urbana, IL (United States)
  3. Univ. of Illinois, Urbana, IL (United States)
  4. Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States); Georgia Inst. of Technology, Atlanta, GA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); National Science Foundation (NSF)
OSTI Identifier:
1468132
Grant/Contract Number:  
AC05-00OR22725; SC0006662; 1356288
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 84; Journal Issue: 2; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; metagenomics; nitrifiers; soil microbiology; seasonal dynamics

Citation Formats

Orellana, Luis H., Chee-Sanford, Joanne C., Sanford, Robert A., Löffler, Frank E., and Konstantinidis, Konstantinos T. Year-Round Shotgun Metagenomes Reveal Stable Microbial Communities in Agricultural Soils and Novel Ammonia Oxidizers Responding to Fertilization. United States: N. p., 2017. Web. doi:10.1128/AEM.01646-17.
Orellana, Luis H., Chee-Sanford, Joanne C., Sanford, Robert A., Löffler, Frank E., & Konstantinidis, Konstantinos T. Year-Round Shotgun Metagenomes Reveal Stable Microbial Communities in Agricultural Soils and Novel Ammonia Oxidizers Responding to Fertilization. United States. doi:10.1128/AEM.01646-17.
Orellana, Luis H., Chee-Sanford, Joanne C., Sanford, Robert A., Löffler, Frank E., and Konstantinidis, Konstantinos T. Fri . "Year-Round Shotgun Metagenomes Reveal Stable Microbial Communities in Agricultural Soils and Novel Ammonia Oxidizers Responding to Fertilization". United States. doi:10.1128/AEM.01646-17. https://www.osti.gov/servlets/purl/1468132.
@article{osti_1468132,
title = {Year-Round Shotgun Metagenomes Reveal Stable Microbial Communities in Agricultural Soils and Novel Ammonia Oxidizers Responding to Fertilization},
author = {Orellana, Luis H. and Chee-Sanford, Joanne C. and Sanford, Robert A. and Löffler, Frank E. and Konstantinidis, Konstantinos T.},
abstractNote = {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. In this paper, 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. 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. Finally, 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.},
doi = {10.1128/AEM.01646-17},
journal = {Applied and Environmental Microbiology},
number = 2,
volume = 84,
place = {United States},
year = {2017},
month = {11}
}

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Works referenced in this record:

Prokaryotes: The unseen majority
journal, June 1998

  • Whitman, W. B.; Coleman, D. C.; Wiebe, W. J.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 12
  • DOI: 10.1073/pnas.95.12.6578

A review: long-term effects of agricultural systems on soil biochemical and microbial parameters
journal, May 1992


SolexaQA: At-a-glance quality assessment of Illumina second-generation sequencing data
journal, September 2010

  • Cox, Murray P.; Peterson, Daniel A.; Biggs, Patrick J.
  • BMC Bioinformatics, Vol. 11, Issue 1
  • DOI: 10.1186/1471-2105-11-485

The ecodist Package for Dissimilarity-based Analysis of Ecological Data
journal, January 2007

  • Goslee, Sarah C.; Urban, Dean L.
  • Journal of Statistical Software, Vol. 22, Issue 7
  • DOI: 10.18637/jss.v022.i07

Aerobic nitrous oxide production through N-nitrosating hybrid formation in ammonia-oxidizing archaea
journal, January 2014

  • Stieglmeier, Michaela; Mooshammer, Maria; Kitzler, Barbara
  • The ISME Journal, Vol. 8, Issue 5
  • DOI: 10.1038/ismej.2013.220

Nitrous Oxide (N2O): The Dominant Ozone-Depleting Substance Emitted in the 21st Century
journal, August 2009


Soil Microbial Community Responses to a Decade of Warming as Revealed by Comparative Metagenomics
journal, December 2013

  • Luo, Chengwei; Rodriguez-R, Luis M.; Johnston, Eric R.
  • Applied and Environmental Microbiology, Vol. 80, Issue 5
  • DOI: 10.1128/AEM.03712-13

The ecological role of biodiversity in agroecosystems
journal, June 1999


Interannual dynamics and phenology of bacterial communities in a eutrophic lake
journal, March 2007

  • Shade, Ashley; Kent, Angela D.; Jones, Stuart E.
  • Limnology and Oceanography, Vol. 52, Issue 2
  • DOI: 10.4319/lo.2007.52.2.0487

Archaea predominate among ammonia-oxidizing prokaryotes in soils
journal, August 2006


Pyrosequencing-Based Assessment of Soil pH as a Predictor of Soil Bacterial Community Structure at the Continental Scale
journal, June 2009

  • Lauber, C. L.; Hamady, M.; Knight, R.
  • Applied and Environmental Microbiology, Vol. 75, Issue 15
  • DOI: 10.1128/AEM.00335-09

A Mesophilic, Autotrophic, Ammonia-Oxidizing Archaeon of Thaumarchaeal Group I.1a Cultivated from a Deep Oligotrophic Soil Horizon
journal, April 2014

  • Jung, Man-Young; Park, Soo-Je; Kim, So-Jeong
  • Applied and Environmental Microbiology, Vol. 80, Issue 12
  • DOI: 10.1128/AEM.03730-13

Ecological and Evolutionary Forces Shaping Microbial Diversity in the Human Intestine
journal, February 2006


Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences
journal, August 2014

  • Yarza, Pablo; Yilmaz, Pelin; Pruesse, Elmar
  • Nature Reviews Microbiology, Vol. 12, Issue 9
  • DOI: 10.1038/nrmicro3330

Comparative Genomic Structure of Prokaryotes
journal, December 2004


MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences
journal, March 2014

  • Luo, Chengwei; Rodriguez-R, Luis M.; Konstantinidis, Konstantinos T.
  • Nucleic Acids Research, Vol. 42, Issue 8
  • DOI: 10.1093/nar/gku169

Global distribution of N2O emissions from aquatic systems: natural emissions and anthropogenic effects
journal, July 2000

  • Seitzinger, Sybil P.; Kroeze, Carolien; Styles, Renée V.
  • Chemosphere - Global Change Science, Vol. 2, Issue 3-4
  • DOI: 10.1016/S1465-9972(00)00015-5

CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015

  • Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
  • Genome Research, Vol. 25, Issue 7
  • DOI: 10.1101/gr.186072.114

MaxBin: an automated binning method to recover individual genomes from metagenomes using an expectation-maximization algorithm
journal, August 2014


Velvet: Algorithms for de novo short read assembly using de Bruijn graphs
journal, February 2008


Mash: fast genome and metagenome distance estimation using MinHash
journal, June 2016


Soil microbial diversity and the sustainability of agricultural soils
journal, March 1995


Circumpolar synchrony in big river bacterioplankton
journal, November 2009

  • Crump, Byron C.; Peterson, Bruce J.; Raymond, Peter A.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 50
  • DOI: 10.1073/pnas.0906149106

Prokaryotic taxonomy and phylogeny in the genomic era: advancements and challenges ahead
journal, October 2007

  • Konstantinidis, Konstantinos T.; Tiedje, James M.
  • Current Opinion in Microbiology, Vol. 10, Issue 5
  • DOI: 10.1016/j.mib.2007.08.006

IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth
journal, April 2012


Nonpareil: a redundancy-based approach to assess the level of coverage in metagenomic datasets
journal, October 2013


Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils
journal, November 2012

  • Sanford, R. A.; Wagner, D. D.; Wu, Q.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 48
  • DOI: 10.1073/pnas.1211238109

The Subsystems Approach to Genome Annotation and its Use in the Project to Annotate 1000 Genomes
journal, September 2005


FragGeneScan: predicting genes in short and error-prone reads
journal, August 2010

  • Rho, Mina; Tang, Haixu; Ye, Yuzhen
  • Nucleic Acids Research, Vol. 38, Issue 20
  • DOI: 10.1093/nar/gkq747

Complete nitrification by Nitrospira bacteria
journal, November 2015

  • Daims, Holger; Lebedeva, Elena V.; Pjevac, Petra
  • Nature, Vol. 528, Issue 7583
  • DOI: 10.1038/nature16461

Accelerated Profile HMM Searches
journal, October 2011


The do-it-all nitrifier
journal, January 2016


FunGene: the functional gene pipeline and repository
journal, January 2013


MICROBIAL DIVERSITY IN SOIL: Selection of Microbial Populations by Plant and Soil Type and Implications for Disease Suppressiveness
journal, September 2004


The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013

  • Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1178

Complete nitrification by a single microorganism
journal, November 2015

  • van Kessel, Maartje A. H. J.; Speth, Daan R.; Albertsen, Mads
  • Nature, Vol. 528, Issue 7583
  • DOI: 10.1038/nature16459

Temporal variability in soil microbial communities across land-use types
journal, April 2013

  • Lauber, Christian L.; Ramirez, Kelly S.; Aanderud, Zach
  • The ISME Journal, Vol. 7, Issue 8
  • DOI: 10.1038/ismej.2013.50

Isotopic signatures of N2O produced by ammonia-oxidizing archaea from soils
journal, November 2013


Stimulation of thaumarchaeal ammonia oxidation by ammonia derived from organic nitrogen but not added inorganic nitrogen
journal, January 2012


Detecting Nitrous Oxide Reductase (nosZ) Genes in Soil Metagenomes: Method Development and Implications for the Nitrogen Cycle
journal, June 2014


BLAST+: architecture and applications
journal, January 2009

  • Camacho, Christiam; Coulouris, George; Avagyan, Vahram
  • BMC Bioinformatics, Vol. 10, Issue 1
  • DOI: 10.1186/1471-2105-10-421

Contributions of ammonia-oxidizing archaea and bacteria to nitrification in Oregon forest soils
journal, June 2015


Trends between gene content and genome size in prokaryotic species with larger genomes
journal, February 2004

  • Konstantinidis, K. T.; Tiedje, J. M.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 9
  • DOI: 10.1073/pnas.0308653100

Microbial seed banks: the ecological and evolutionary implications of dormancy
journal, January 2011

  • Lennon, Jay T.; Jones, Stuart E.
  • Nature Reviews Microbiology, Vol. 9, Issue 2
  • DOI: 10.1038/nrmicro2504

Distinct soil microbial diversity under long-term organic and conventional farming
journal, October 2014


Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms
journal, January 2011

  • Verhamme, Daniel T.; Prosser, James I.; Nicol, Graeme W.
  • The ISME Journal, Vol. 5, Issue 6
  • DOI: 10.1038/ismej.2010.191

Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota
journal, February 2016

  • Kozlowski, Jessica A.; Stieglmeier, Michaela; Schleper, Christa
  • The ISME Journal, Vol. 10, Issue 8
  • DOI: 10.1038/ismej.2016.2

Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation
journal, November 2012


Diversity and dynamics of microbial communities in soils from agro-ecosystems
journal, June 2003


Microbial and biochemical soil quality indicators and their potential for differentiating areas under contrasting agricultural management regimes
journal, November 2004


Physiology and Diversity of Ammonia-Oxidizing Archaea
journal, October 2012


DNA–DNA hybridization values and their relationship to whole-genome sequence similarities
journal, January 2007

  • Klappenbach, Joel A.; Goris, Johan; Vandamme, Peter
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 57, Issue 1
  • DOI: 10.1099/ijs.0.64483-0

Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle
journal, August 2017

  • Kits, K. Dimitri; Sedlacek, Christopher J.; Lebedeva, Elena V.
  • Nature, Vol. 549, Issue 7671
  • DOI: 10.1038/nature23679

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


Bacterial species may exist, metagenomics reveal: Bacterial species may exist
journal, December 2011