Emergence of trait variability through the lens of nitrogen assimilation in Prochlorococcus

  1. Paul M Berube  Is a corresponding author
  2. Anna Rasmussen
  3. Rogier Braakman
  4. Ramunas Stepanauskas
  5. Sallie W Chisholm
  1. Massachusetts Institute of Technology, United States
  2. Bigelow Laboratory for Ocean Sciences, United States

Abstract

Intraspecific trait variability has important consequences for the function and stability of marine ecosystems. Here we examine variation in the ability to use nitrate across hundreds of Prochlorococcus genomes to better understand the modes of evolution influencing intraspecific allocation of ecologically important functions. Nitrate assimilation genes are absent in basal lineages but occur at an intermediate frequency that is randomly distributed within recently emerged clades. The distribution of nitrate assimilation genes within clades appears largely governed by vertical inheritance, gene loss, and homologous recombination. By mapping this process onto a model of Prochlorococcus' macroevolution, we propose that niche-constructing adaptive radiations and subsequent niche partitioning set the stage for loss of nitrate assimilation genes from basal lineages as they specialized to lower light levels. Retention of these genes in recently emerged lineages has likely been facilitated by selection as they sequentially partitioned into niches where nitrate assimilation conferred a fitness benefit.

Data availability

Sequencing data have been deposited in Integrated Microbial Genomes under the accession numbers (IMG Genome ID) 2681812899, 2681812900, 2681812901, and 2681812859.All data generated or analyzed during this study are included in the manuscript and supporting files. Source data files have been provided for Figure 1, Figure 2, Figure 3, Figure 6, Figure 7, Table 1, Table 2, Table 3, Table 4, and Table 5.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Paul M Berube

    Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, United States
    For correspondence
    pmberube@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5598-6602
  2. Anna Rasmussen

    Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0031-2835
  3. Rogier Braakman

    Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Ramunas Stepanauskas

    Bigelow Laboratory for Ocean Sciences, East Boothbay, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Sallie W Chisholm

    Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Science Foundation (OCE-1153588)

  • Sallie W Chisholm

National Science Foundation (DBI-0424599)

  • Sallie W Chisholm

National Science Foundation (OCE-1335810)

  • Ramunas Stepanauskas

Simons Foundation (337262)

  • Sallie W Chisholm

Simons Foundation (329108)

  • Sallie W Chisholm

Gordon and Betty Moore Foundation (GBMF495)

  • Sallie W Chisholm

Gordon and Betty Moore Foundation (GBMF4511)

  • Sallie W Chisholm

Simons Foundation (509034SCFY17)

  • Sallie W Chisholm

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

Reviewing Editor

  1. Paul G Falkowski, Rutgers University, United States

Publication history

  1. Received: August 13, 2018
  2. Accepted: January 31, 2019
  3. Accepted Manuscript published: February 1, 2019 (version 1)
  4. Version of Record published: February 11, 2019 (version 2)

Copyright

© 2019, Berube 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. Paul M Berube
  2. Anna Rasmussen
  3. Rogier Braakman
  4. Ramunas Stepanauskas
  5. Sallie W Chisholm
(2019)
Emergence of trait variability through the lens of nitrogen assimilation in Prochlorococcus
eLife 8:e41043.
https://doi.org/10.7554/eLife.41043

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