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Title: Predicting ecological roles in the rhizosphere using metabolome and transportome modeling

Abstract

The ability to obtain complete genome sequences from bacteria in environmental samples, such as soil samples from the rhizosphere, has highlighted the microbial diversity and complexity of environmental communities. New algorithms to analyze genome sequence information in the context of community structure are needed to enhance our understanding of the specific ecological roles of these organisms in soil environments. We present a machine learning approach using sequenced Pseudomonad genomes coupled with outputs of metabolic and transportomic computational models for identifying the most predictive molecular mechanisms indicative of a Pseudomonad’s ecological role in the rhizosphere: a biofilm, biocontrol agent, promoter of plant growth, or plant pathogen. Computational predictions of ecological niche were highly accurate overall with models trained on transportomic model output being the most accurate (Leave One Out Validation F-scores between 0.82 and 0.89). The strongest predictive molecular mechanism features for rhizosphere ecological niche overlap with many previously reported analyses of Pseudomonad interactions in the rhizosphere, suggesting that this approach successfully informs a system-scale level understanding of how Pseudomonads sense and interact with their environments. The observation that an organism’s transportome is highly predictive of its ecological niche is a novel discovery and may have implications in our understanding microbialmore » ecology. The framework developed here can be generalized to the analysis of any bacteria across a wide range of environments and ecological niches making this approach a powerful tool for providing insights into functional predictions from bacterial genomic data.« less

Authors:
 [1];  [2];  [3];  [4]
  1. Argonne National Lab., Argonne, IL (United States). Biosciences Div.; Univ. of Chicago, Chicago, IL (United States). Dept. of Bioengineering.
  2. Argonne National Lab., Argonne, IL (United States). Biosciences Div.
  3. Univ. of Chicago, Chicago, IL (United States). Dept. of Bioengineering
  4. Univ. of Massachusetts, Worcester, MA (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1221792
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 10; Journal Issue: 9; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; ecological niches; enzyme metabolism; plant genomics; metabolomics; enzymes; rhizosphere; secondary metabolism; genome analysis

Citation Formats

Larsen, Peter E., Collart, Frank R., Dai, Yang, and Blanchard, Jeffrey L. Predicting ecological roles in the rhizosphere using metabolome and transportome modeling. United States: N. p., 2015. Web. doi:10.1371/journal.pone.0132837.
Larsen, Peter E., Collart, Frank R., Dai, Yang, & Blanchard, Jeffrey L. Predicting ecological roles in the rhizosphere using metabolome and transportome modeling. United States. doi:10.1371/journal.pone.0132837.
Larsen, Peter E., Collart, Frank R., Dai, Yang, and Blanchard, Jeffrey L. Wed . "Predicting ecological roles in the rhizosphere using metabolome and transportome modeling". United States. doi:10.1371/journal.pone.0132837. https://www.osti.gov/servlets/purl/1221792.
@article{osti_1221792,
title = {Predicting ecological roles in the rhizosphere using metabolome and transportome modeling},
author = {Larsen, Peter E. and Collart, Frank R. and Dai, Yang and Blanchard, Jeffrey L.},
abstractNote = {The ability to obtain complete genome sequences from bacteria in environmental samples, such as soil samples from the rhizosphere, has highlighted the microbial diversity and complexity of environmental communities. New algorithms to analyze genome sequence information in the context of community structure are needed to enhance our understanding of the specific ecological roles of these organisms in soil environments. We present a machine learning approach using sequenced Pseudomonad genomes coupled with outputs of metabolic and transportomic computational models for identifying the most predictive molecular mechanisms indicative of a Pseudomonad’s ecological role in the rhizosphere: a biofilm, biocontrol agent, promoter of plant growth, or plant pathogen. Computational predictions of ecological niche were highly accurate overall with models trained on transportomic model output being the most accurate (Leave One Out Validation F-scores between 0.82 and 0.89). The strongest predictive molecular mechanism features for rhizosphere ecological niche overlap with many previously reported analyses of Pseudomonad interactions in the rhizosphere, suggesting that this approach successfully informs a system-scale level understanding of how Pseudomonads sense and interact with their environments. The observation that an organism’s transportome is highly predictive of its ecological niche is a novel discovery and may have implications in our understanding microbial ecology. The framework developed here can be generalized to the analysis of any bacteria across a wide range of environments and ecological niches making this approach a powerful tool for providing insights into functional predictions from bacterial genomic data.},
doi = {10.1371/journal.pone.0132837},
journal = {PLoS ONE},
number = 9,
volume = 10,
place = {United States},
year = {2015},
month = {9}
}

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Works referenced in this record:

The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms
journal, September 2013

  • Mendes, Rodrigo; Garbeva, Paolina; Raaijmakers, Jos M.
  • FEMS Microbiology Reviews, Vol. 37, Issue 5
  • DOI: 10.1111/1574-6976.12028

Pathogenesis, parasitism and mutualism in the trophic space of microbe–plant interactions
journal, August 2010

  • Newton, Adrian C.; Fitt, Bruce D. L.; Atkins, Simon D.
  • Trends in Microbiology, Vol. 18, Issue 8
  • DOI: 10.1016/j.tim.2010.06.002

Mycorrhizas improve nitrogen nutrition of Trifolium repens after 8 yr of selection under elevated atmospheric CO2 partial pressure
journal, April 2005


Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2
journal, June 2010

  • Drigo, B.; Pijl, A. S.; Duyts, H.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 24
  • DOI: 10.1073/pnas.0912421107

Going back to the roots: the microbial ecology of the rhizosphere
journal, September 2013

  • Philippot, Laurent; Raaijmakers, Jos M.; Lemanceau, Philippe
  • Nature Reviews Microbiology, Vol. 11, Issue 11
  • DOI: 10.1038/nrmicro3109

Mapping the niche space of soil microorganisms using taxonomy and traits
journal, August 2012

  • Lennon, Jay T.; Aanderud, Zachary T.; Lehmkuhl, B. K.
  • Ecology, Vol. 93, Issue 8
  • DOI: 10.1890/11-1745.1

Comparative genomics and functional analysis of niche-specific adaptation in Pseudomonas putida
journal, March 2011


Predicting Prokaryotic Ecological Niches Using Genome Sequence Analysis
journal, August 2007


16S rRNA Gene Sequencing for Bacterial Identification in the Diagnostic Laboratory: Pluses, Perils, and Pitfalls
journal, July 2007

  • Janda, J. M.; Abbott, S. L.
  • Journal of Clinical Microbiology, Vol. 45, Issue 9
  • DOI: 10.1128/JCM.01228-07

Microbial phylogeny and diversity: Small subunit ribosomal RNA sequence analysis and beyond
journal, February 2011


Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates
journal, January 2010


Ammonia-oxidizing archaea involved in nitrogen removal
journal, April 2009


Deadly syringes: type VI secretion system activities in pathogenicity and interbacterial competition
journal, February 2013


The type VI secretion toolkit
journal, July 2008


Type VI Secretion: Not Just for Pathogenesis Anymore
journal, July 2010


Plant pathogenesis-related (PR) proteins: A focus on PR peptides
journal, November 2008

  • Sels, Jan; Mathys, Janick; De Coninck, Barbara M. A.
  • Plant Physiology and Biochemistry, Vol. 46, Issue 11
  • DOI: 10.1016/j.plaphy.2008.06.011

Fluxomics - connecting ‘omics analysis and phenotypes: Fluxomics - a systems biology tool
journal, January 2013


Genomics of secondary metabolite production by Pseudomonas spp.
journal, January 2009

  • Gross, Harald; Loper, Joyce E.
  • Natural Product Reports, Vol. 26, Issue 11
  • DOI: 10.1039/b817075b

The metabolic versatility of pseudomonads
journal, January 1982


Pseudomonas genomes: diverse and adaptable
journal, July 2011


Biological control of soil-borne pathogens by fluorescent pseudomonads
journal, March 2005

  • Haas, Dieter; Défago, Geneviève
  • Nature Reviews Microbiology, Vol. 3, Issue 4
  • DOI: 10.1038/nrmicro1129

Bacterial endophytes: recent developments and applications
journal, January 2008


Inter-specific Interactions Between Carbon-limited Soil Bacteria Affect Behavior and Gene Expression
journal, March 2009


Causes and consequences of plant-associated biofilms: Causes and consequences of plant-associated biofilms
journal, May 2008


Top 10 plant pathogenic bacteria in molecular plant pathology: Top 10 plant pathogenic bacteria
journal, June 2012


The mycorrhiza helper bacteria revisited
journal, October 2007


KEGG for integration and interpretation of large-scale molecular data sets
journal, November 2011

  • Kanehisa, M.; Goto, S.; Sato, Y.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr988

KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 1999

  • Ogata, H.; Goto, S.; Sato, K.
  • Nucleic Acids Research, Vol. 27, Issue 1
  • DOI: 10.1093/nar/27.1.29

The ENZYME database in 2000
journal, January 2000


Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary
journal, April 2005


The microbial nitrogen cycling potential is impacted by polyaromatic hydrocarbon pollution of marine sediments
journal, March 2014


Satellite remote sensing data can be used to model marine microbial metabolite turnover
journal, July 2014

  • Larsen, Peter E.; Scott, Nicole; Post, Anton F.
  • The ISME Journal, Vol. 9, Issue 1
  • DOI: 10.1038/ismej.2014.107

Osmotic adaptation by gram-negative bacteria: possible role for periplasmic oligosaccharides
journal, January 1986


Periplasmic glucans of Pseudomonas syringae pv. syringae.
journal, November 1994


Iron uptake and metabolism in pseudomonads
journal, March 2010


Multiple roles of siderophores in free-living nitrogen-fixing bacteria
journal, March 2009


Microbial degradation of lignin: how a bulky recalcitrant polymer is efficiently recycled in nature and how we can take advantage of this
journal, March 2009


Catecholamines are active compounds in plants
journal, March 2007


The Dual Function of Sugar Carriers: Transport and Sugar Sensing
journal, April 1999

  • Lalonde, Sylvie; Boles, Eckhard; Hellmann, Hanjo
  • The Plant Cell, Vol. 11, Issue 4
  • DOI: 10.1105/tpc.11.4.707

Pathways of Glucose Regulation of Monosaccharide Transport in Grape Cells
journal, June 2006

  • Conde, Carlos; Agasse, Alice; Glissant, David
  • Plant Physiology, Vol. 141, Issue 4
  • DOI: 10.1104/pp.106.080804

Molecular mechanisms of lytic enzymes involved in the biocontrol activity of Trichoderma harzianum
journal, September 1996


An Oxyferrous Heme/Protein-based Radical Intermediate Is Catalytically Competent in the Catalase Reaction of Mycobacterium tuberculosis Catalase-Peroxidase (KatG)
journal, January 2009

  • Suarez, Javier; Ranguelova, Kalina; Jarzecki, Andrzej A.
  • Journal of Biological Chemistry, Vol. 284, Issue 11
  • DOI: 10.1074/jbc.M808106200

Anti-biofilm Effects of Honey Against Wound Pathogens Proteus mirabilis and Enterobacter cloacae : HONEY KILLS WOUND BIOFILM
journal, March 2013

  • Majtan, Juraj; Bohova, Jana; Horniackova, Miroslava
  • Phytotherapy Research, Vol. 28, Issue 1
  • DOI: 10.1002/ptr.4957

Methylglyoxal: (active agent of manuka honey) in vitro activity against bacterial biofilms
journal, May 2011

  • Kilty, Shaun J.; Duval, Melanie; Chan, Francis T.
  • International Forum of Allergy & Rhinology, Vol. 1, Issue 5
  • DOI: 10.1002/alr.20073

Evidence for the involvement of the anthranilate degradation pathway in Pseudomonas aeruginosa biofilm formation
journal, September 2012

  • Costaglioli, Patricia; Barthe, Christophe; Claverol, Stephane
  • MicrobiologyOpen, Vol. 1, Issue 3
  • DOI: 10.1002/mbo3.33

The Cpx system of Escherichia coli, a strategic signaling pathway for confronting adverse conditions and for settling biofilm communities?
journal, May 2006


Isolation of Streptococcus pneumoniae Biofilm Mutants and Their Characterization during Nasopharyngeal Colonization
journal, September 2008

  • Munoz-Elias, E. J.; Marcano, J.; Camilli, A.
  • Infection and Immunity, Vol. 76, Issue 11
  • DOI: 10.1128/IAI.00425-08

Nutritional Influences on Biofilm Development
journal, April 1997


Pseudomonas aeruginosa PA1006, Which Plays a Role in Molybdenum Homeostasis, Is Required for Nitrate Utilization, Biofilm Formation, and Virulence
journal, February 2013


Regulatory and Metabolic Networks for the Adaptation of Pseudomonas aeruginosa Biofilms to Urinary Tract-Like Conditions
journal, August 2013


Very long chain fatty acid and lipid signaling in the response of plants to pathogens
journal, February 2009

  • Raffaele, Sylvain; Leger, Amandine; Roby, Dominique
  • Plant Signaling & Behavior, Vol. 4, Issue 2
  • DOI: 10.4161/psb.4.2.7580

Agrobacterium tumefaciens recognizes its host environment using ChvE to bind diverse plant sugars as virulence signals
journal, December 2012

  • Hu, X.; Zhao, J.; DeGrado, W. F.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 2
  • DOI: 10.1073/pnas.1215033110

The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000
journal, August 2003

  • Buell, C. R.; Joardar, V.; Lindeberg, M.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 18
  • DOI: 10.1073/pnas.1731982100

Polyamines: Natural and engineered abiotic and biotic stress tolerance in plants
journal, May 2011


From perception to attenuation: auxin signalling and responses
journal, October 2013


The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia and Frankia bacteria
journal, June 2012

  • Abdel-Lateif, Khalid; Bogusz, Didier; Hocher, Valérie
  • Plant Signaling & Behavior, Vol. 7, Issue 6
  • DOI: 10.4161/psb.20039

Flavonoids and Strigolactones in Root Exudates as Signals in Symbiotic and Pathogenic Plant-Fungus Interactions
journal, July 2007

  • Steinkellner, Siegrid; Lendzemo, Venasius; Langer, Ingrid
  • Molecules, Vol. 12, Issue 7
  • DOI: 10.3390/12071290

Flavonoids as plant signals to rhizosphere microbes
journal, March 1992


Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes
journal, July 2008

  • Kosuta, S.; Hazledine, S.; Sun, J.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 28
  • DOI: 10.1073/pnas.0803499105

Activation of calcium- and calmodulin-dependent protein kinase (CCaMK), the central regulator of plant root endosymbiosis
journal, August 2012


Metagenomics - a guide from sampling to data analysis
journal, February 2012

  • Thomas, Torsten; Gilbert, Jack; Meyer, Folker
  • Microbial Informatics and Experimentation, Vol. 2, Issue 1
  • DOI: 10.1186/2042-5783-2-3

Emerging science of the human microbiome
journal, July 2014

  • Jones, Mitchell L.; Ganopolsky, Jorge G.; Martoni, Christopher J.
  • Gut Microbes, Vol. 5, Issue 4
  • DOI: 10.4161/gmic.29810

    Works referencing / citing this record:

    Metabolome of human gut microbiome is predictive of host dysbiosis
    journal, September 2015