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

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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

1. Berube PM
2. Chisholm SW
(2018) Prochlorococcus sp. MIT0912
IMG, 2681812899.

https://img.jgi.doe.gov/cgi-bin/m/main.cgi?section=TaxonDetail&page=taxonDetail&taxon_oid=2681812899
1. Berube PM
2. Chisholm SW
(2018) Prochlorococcus sp. MIT0913
IMG, 2681812900.

https://img.jgi.doe.gov/cgi-bin/m/main.cgi?section=TaxonDetail&page=taxonDetail&taxon_oid=2681812900
1. Berube PM
2. Chisholm SW
(2018) Prochlorococcus sp. MIT0915
IMG, 2681812901.

https://img.jgi.doe.gov/cgi-bin/m/main.cgi?section=TaxonDetail&page=taxonDetail&taxon_oid=2681812901
1. Berube PM
2. Chisholm SW
(2018) Prochlorococcus sp. MIT0917
IMG, 2681812859.

https://img.jgi.doe.gov/cgi-bin/m/main.cgi?section=TaxonDetail&page=taxonDetail&taxon_oid=2681812859

The following previously published data sets were used

1. Berube PM
2. Biller SJ
3. Hackl T
4. Hogle SL
5. Satinsky BM
6. Becker JW
7. Braakman R
8. Collins SB
9. Kelly L
10. Berta-Thompson J
11. Coe A
12. Bergauer K
13. Bouman HA
14. Browning TJ
15. De Corte D
16. Hassler C
17. Hulata Y
18. Jacquot JE
19. Maas EW
20. Reinthaler T
21. Sintes E
22. Yokokawa T
23. Lindell D
24. Stepanauskas R
25. Chisholm SW
(2018) Single cell genomes of Prochlorococcus, Synechococcus, and sympatric microbes from diverse marine environments
NCBI, BioProject PRJNA445865.

https://www.nature.com/articles/sdata2018154

Article and author information

Author details

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.

"This ORCID iD identifies the author of this article:" 0000-0001-5598-6602
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.

"This ORCID iD identifies the author of this article:" 0000-0002-0031-2835
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.
Ramunas Stepanauskas

Bigelow Laboratory for Ocean Sciences, East Boothbay, United States

Competing interests
The authors declare that no competing interests exist.
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

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.