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ISME J. 2015 May;9(5):1195-207. doi: 10.1038/ismej.2014.211. Epub 2014 Oct 28.

Physiology and evolution of nitrate acquisition in Prochlorococcus.

Author information

1
Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA.
2
Department of Ecology and Evolutionary Biology, University of California, Irvine, Irvine, CA, USA.
3
1] Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA [2] Microbiology Graduate Program, Massachusetts Institute of Technology, Cambridge, MA, USA.
4
1] Department of Molecular and Biomedical Sciences, University of Maine, Orono, ME, USA [2] Department of Biological Sciences, University of Southern Maine, Portland, ME, USA.
5
Department of Biological Sciences, University of Southern Maine, Portland, ME, USA.
6
Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.
7
Department of Marine Biology, University of Haifa, Haifa, Israel.
8
Department of Chemistry and Biochemistry, University of Colorado, Boulder, CO, USA.
9
Department of Oceanography, Texas A&M University, College Station, TX, USA.
10
1] Department of Ecology and Evolutionary Biology, University of California, Irvine, Irvine, CA, USA [2] Department of Earth System Science, University of California, Irvine, Irvine, CA, USA.
11
1] Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA [2] Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.

Abstract

Prochlorococcus is the numerically dominant phototroph in the oligotrophic subtropical ocean and carries out a significant fraction of marine primary productivity. Although field studies have provided evidence for nitrate uptake by Prochlorococcus, little is known about this trait because axenic cultures capable of growth on nitrate have not been available. Additionally, all previously sequenced genomes lacked the genes necessary for nitrate assimilation. Here we introduce three Prochlorococcus strains capable of growth on nitrate and analyze their physiology and genome architecture. We show that the growth of high-light (HL) adapted strains on nitrate is ∼17% slower than their growth on ammonium. By analyzing 41 Prochlorococcus genomes, we find that genes for nitrate assimilation have been gained multiple times during the evolution of this group, and can be found in at least three lineages. In low-light adapted strains, nitrate assimilation genes are located in the same genomic context as in marine Synechococcus. These genes are located elsewhere in HL adapted strains and may often exist as a stable genetic acquisition as suggested by the striking degree of similarity in the order, phylogeny and location of these genes in one HL adapted strain and a consensus assembly of environmental Prochlorococcus metagenome sequences. In another HL adapted strain, nitrate utilization genes may have been independently acquired as indicated by adjacent phage mobility elements; these genes are also duplicated with each copy detected in separate genomic islands. These results provide direct evidence for nitrate utilization by Prochlorococcus and illuminate the complex evolutionary history of this trait.

PMID:
25350156
PMCID:
PMC4409163
DOI:
10.1038/ismej.2014.211
[Indexed for MEDLINE]
Free PMC Article

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