Genomic adaptations in information processing underpin trophic strategy in a whole-ecosystem nutrient enrichment experiment

  1. Jordan G Okie  Is a corresponding author
  2. Amisha T Poret-Peterson
  3. Zarraz MP Lee
  4. Alexander Richter
  5. Luis D Alcaraz
  6. Luis E Eguiarte
  7. Janet L Siefert
  8. Valeria Souza
  9. Chris L Dupont
  10. James J Elser
  1. Arizona State University, United States
  2. USDA, United States
  3. J Craig Venter Institute, United States
  4. Universidad Nacional Autónoma de México, Mexico
  5. Rice University, United States
  6. University of Montana, United States

Abstract

Several universal genomic traits affect trade-offs in the capacity, cost, and efficiency of biochemical information processing underpinning metabolism and reproduction. We analyzed their role in mediating planktonic microbial community responses to nutrient enrichment in an oligotrophic, phosphorus-deficient pond in Cuatro Ciénegas, Mexico—one of the first whole-ecosystem experiments involving replicated metagenomic assessment. Mean bacterial genome size, GC content, total number of tRNA genes, total number of rRNA genes, and codon usage bias in ribosomal protein sequences were higher in the fertilized treatment, as predicted assuming oligotrophy favors lower information-processing costs while copiotrophy favors higher processing rates. Contrasting changes in trait variances also suggested differences between traits in mediating assembly under copiotrophic versus oligotrophic conditions. Trade-offs in information-processing traits are apparently sufficiently pronounced to play a role in community assembly as the major components of metabolism—information, energy, and nutrient requirements—are fine-tuned to an organism's growth and trophic strategy.

Data availability

Raw sequence data and metadata have been submitted to NCBI Sequence Read Archives, accessible through BioProject PRJEB22811.

The following data sets were generated

Article and author information

Author details

  1. Jordan G Okie

    School of Earth and Space Exploration, Arizona State University, Tempe, United States
    For correspondence
    jordan.okie@asu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7884-7688
  2. Amisha T Poret-Peterson

    ARS Crops Pathology and Genetic Research Unit, USDA, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Zarraz MP Lee

    School of Life Sciences, Arizona State University, Tempe, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Alexander Richter

    J Craig Venter Institute, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Luis D Alcaraz

    Departamento de Biología Celular, Universidad Nacional Autónoma de México, Mexico City, Mexico
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3284-0605
  6. Luis E Eguiarte

    Departamento de Ecología Evolutiva, Universidad Nacional Autónoma de México, Mexico City, Mexico
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5906-9737
  7. Janet L Siefert

    Department of Statistics, Rice University, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Valeria Souza

    Departamento de Ecología Evolutiva, Universidad Nacional Autónoma de México, Mexico City, Mexico
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2992-4229
  9. Chris L Dupont

    J Craig Venter Institute, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. James J Elser

    Flathead Lake Biological Station, University of Montana, Missoula, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Science Foundation (DEB-0950175)

  • James J Elser

National Aeronautics and Space Administration (NAI5-0018)

  • James J Elser

National Aeronautics and Space Administration (NNH05ZDA001C)

  • Janet L Siefert

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. David Donoso, Escuela Politécnica Nacional, Ecuador

Version history

  1. Received: July 1, 2019
  2. Accepted: January 27, 2020
  3. Accepted Manuscript published: January 28, 2020 (version 1)
  4. Version of Record published: February 18, 2020 (version 2)

Copyright

© 2020, Okie et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Jordan G Okie
  2. Amisha T Poret-Peterson
  3. Zarraz MP Lee
  4. Alexander Richter
  5. Luis D Alcaraz
  6. Luis E Eguiarte
  7. Janet L Siefert
  8. Valeria Souza
  9. Chris L Dupont
  10. James J Elser
(2020)
Genomic adaptations in information processing underpin trophic strategy in a whole-ecosystem nutrient enrichment experiment
eLife 9:e49816.
https://doi.org/10.7554/eLife.49816

Share this article

https://doi.org/10.7554/eLife.49816

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