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.

Metrics

  • 2,414
    Page views
  • 276
    Downloads
  • 16
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Ecology
    Yongzhi Yan, Scott Jarvie, Qing Zhang
    Research Article

    Habitat loss and fragmentation per se have been shown to be a major threat to global biodiversity and ecosystem function. However, little is known about how habitat loss and fragmentation per se alters the relationship between biodiversity and ecosystem function (BEF relationship) in the natural landscape context. Based on 130 landscapes identified by a stratified random sampling in the agro-pastoral ecotone of northern China, we investigated the effects of landscape context (habitat loss and fragmentation per se) on plant richness, above-ground biomass, and the relationship between them in grassland communities using a structural equation model. We found that habitat loss directly decreased plant richness and hence decreased above-ground biomass, while fragmentation per se directly increased plant richness and hence increased above-ground biomass. Fragmentation per se also directly decreased soil water content and hence decreased above-ground biomass. Meanwhile, habitat loss decreased the magnitude of the positive relationship between plant richness and above-ground biomass by reducing the percentage of grassland specialists in the community, while fragmentation per se had no significant modulating effect on this relationship. These results demonstrate that habitat loss and fragmentation per se have inconsistent effects on BEF, with the BEF relationship being modulated by landscape context. Our findings emphasise that habitat loss rather than fragmentation per se can weaken the positive BEF relationship by decreasing the degree of habitat specialisation of the community.

    1. Ecology
    Anna L Erdei, Aneth B David ... Teun Dekker
    Research Article

    Over two decades ago, an intercropping strategy was developed that received critical acclaim for synergizing food security with ecosystem resilience in smallholder farming. The push-pull strategy reportedly suppresses lepidopteran pests in maize through a combination of a repellent intercrop (push), commonly Desmodium spp., and an attractive, border crop (pull). Key in the system is the intercrop's constitutive release of volatile terpenoids that repel herbivores. However, the earlier described volatiles were not detectable in the headspace of Desmodium, and only minimally upon herbivory. This was independent of soil type, microbiome composition, and whether collections were made in the laboratory or in the field. Further, in oviposition choice tests in a wind tunnel, maize with or without an odor background of Desmodium was equally attractive for the invasive pest Spodoptera frugiperda. In search of an alternative mechanism, we found that neonate larvae strongly preferred Desmodium over maize. However, their development stagnated and no larva survived. In addition, older larvae were frequently seen impaled and immobilized by the dense network of silica-fortified, non-glandular trichomes. Thus, our data suggest that Desmodium may act through intercepting and decimating dispersing larval offspring rather than adult deterrence. As a hallmark of sustainable pest control, maize-Desmodium push-pull intercropping has inspired countless efforts to emulate stimulo-deterrent diversion in other cropping systems. However, detailed knowledge of the actual mechanisms is required to rationally improve the strategy, and translate the concept to other cropping systems.