1. Ecology
  2. Evolutionary Biology

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
https://doi.org/10.7554/eLife.41043
Share this article
Cite this article
  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
  2. Download BibTeX
  3. Download .RIS

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.

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.

Metrics

  • 2,531
    views
  • 365
    downloads
  • 56
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. 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

Share this article

https://doi.org/10.7554/eLife.41043

Categories and tags

Further reading

    1. Ecology
    2. Microbiology and Infectious Disease

    Novel class IIb microcins show activity against Gram-negative ESKAPE and plant pathogens

    Benedikt M Mortzfeld, Shakti K Bhattarai, Vanni Bucci
    Short Report

    Interspecies interactions involving direct competition via bacteriocin production play a vital role in shaping ecological dynamics within microbial ecosystems. For instance, the ribosomally produced siderophore bacteriocins, known as class IIb microcins, affect the colonization of host-associated pathogenic Enterobacteriaceae species. Notably, to date, only five of these antimicrobials have been identified, all derived from specific Escherichia coli and Klebsiella pneumoniae strains. We hypothesized that class IIb microcin production extends beyond these specific compounds and organisms. With a customized informatics-driven approach, screening bacterial genomes in public databases with BLAST and manual curation, we have discovered 12 previously unknown class IIb microcins in seven additional Enterobacteriaceae species, encompassing phytopathogens and environmental isolates. We introduce three novel clades of microcins (MccW, MccX, and MccZ), while also identifying eight new variants of the five known class IIb microcins. To validate their antimicrobial potential, we heterologously expressed these microcins in E. coli and demonstrated efficacy against a variety of bacterial isolates, including plant pathogens from the genera Brenneria, Gibbsiella, and Rahnella. Two newly discovered microcins exhibit activity against Gram-negative ESKAPE pathogens, i.e., Acinetobacter baumannii or Pseudomonas aeruginosa, providing the first evidence that class IIb microcins can target bacteria outside of the Enterobacteriaceae family. This study underscores that class IIb microcin genes are more prevalent in the microbial world than previously recognized and that synthetic hybrid microcins can be a viable tool to target clinically relevant drug-resistant pathogens. Our findings hold significant promise for the development of innovative engineered live biotherapeutic products tailored to combat these resilient bacteria.

    1. Ecology

    Polarised moonlight guides nocturnal bull ants home

    Cody A Freas, Ajay Narenda ... Ken Cheng
    Research Article

    For the first time in any animal, we show that nocturnal bull ants use the exceedingly dim polarisation pattern produced by the moon for overnight navigation. The sun or moon can provide directional information via their position; however, they can often be obstructed by clouds, canopy, or the horizon. Despite being hidden, these bodies can still provide compass information through the polarised light pattern they produce/reflect. Sunlight produces polarised light patterns across the overhead sky as it enters the atmosphere, and solar polarised light is a well-known compass cue for navigating animals. Moonlight produces an analogous pattern, albeit a million times dimmer than sunlight. Here, we show evidence that polarised moonlight forms part of the celestial compass of navigating nocturnal ants. Nocturnal bull ants leave their nest at twilight and rely heavily on the overhead solar polarisation pattern to navigate. Yet many foragers return home overnight when the sun cannot guide them. We demonstrate that these bull ants use polarised moonlight to navigate home during the night, by rotating the overhead polarisation pattern above homing ants, who alter their headings in response. Furthermore, these ants can detect this cue throughout the lunar month, even under crescent moons, when polarised light levels are at their lowest. Finally, we show the long-term incorporation of this moonlight pattern into the ants’ path integration system throughout the night for homing, as polarised sunlight is incorporated throughout the day.

    1. Ecology

    Habitat fragmentation mediates the mechanisms underlying long-term climate-driven thermophilization in birds

    Juan Liu, Morgan W Tingley ... Xingfeng Si
    Research Article

    Climatic warming can shift community composition driven by the colonization-extinction dynamics of species with different thermal preferences; but simultaneously, habitat fragmentation can mediate species’ responses to warming. As this potential interactive effect has proven difficult to test empirically, we collected data on birds over 10 years of climate warming in a reservoir subtropical island system that was formed 65 years ago. We investigated how the mechanisms underlying climate-driven directional change in community composition were mediated by habitat fragmentation. We found thermophilization driven by increasing warm-adapted species and decreasing cold-adapted species in terms of trends in colonization rate, extinction rate, occupancy rate and population size. Critically, colonization rates of warm-adapted species increased faster temporally on smaller or less isolated islands; cold-adapted species generally were lost more quickly temporally on closer islands. This provides support for dispersal limitation and microclimate buffering as primary proxies by which habitat fragmentation mediates species range shift. Overall, this study advances our understanding of biodiversity responses to interacting global change drivers.