title: Physiology and evolution of nitrate acquisition in Prochlorococcus.
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.
authors.affiliation: Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA.
authors.forename: Paul M
authors.initials: PM
authors.lastname: Berube
authors.affiliation: Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA.
authors.forename: Steven J
authors.initials: SJ
authors.lastname: Biller
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Irvine, Irvine, CA, USA.
authors.forename: Alyssa G
authors.initials: AG
authors.lastname: Kent
authors.affiliation: 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.
authors.forename: Jessie W
authors.initials: JW
authors.lastname: Berta-Thompson
authors.affiliation: Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA.
authors.forename: Sara E
authors.initials: SE
authors.lastname: Roggensack
authors.affiliation: 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.
authors.forename: Kathryn H
authors.initials: KH
authors.lastname: Roache-Johnson
authors.affiliation: Department of Biological Sciences, University of Southern Maine, Portland, ME, USA.
authors.forename: Marcia
authors.initials: M
authors.lastname: Ackerman
authors.affiliation: Department of Biological Sciences, University of Southern Maine, Portland, ME, USA.
authors.forename: Lisa R
authors.initials: LR
authors.lastname: Moore
authors.affiliation: Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.
authors.forename: Joshua D
authors.initials: JD
authors.lastname: Meisel
authors.affiliation: Department of Marine Biology, University of Haifa, Haifa, Israel.
authors.forename: Daniel
authors.initials: D
authors.lastname: Sher
authors.affiliation: Department of Chemistry and Biochemistry, University of Colorado, Boulder, CO, USA.
authors.forename: Luke R
authors.initials: LR
authors.lastname: Thompson
authors.affiliation: Department of Oceanography, Texas A&M University, College Station, TX, USA.
authors.forename: Lisa
authors.initials: L
authors.lastname: Campbell
authors.affiliation: 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.
authors.forename: Adam C
authors.initials: AC
authors.lastname: Martiny
authors.affiliation: 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.
authors.forename: Sallie W
authors.initials: SW
authors.lastname: Chisholm
mesh_terms: D001435:Bacteriophages / Q000235:genetics; D005075:Biological Evolution; D004777:Environment; D016680:Genome, Bacterial; D016013:Likelihood Functions; D050901:Nitrate Reductase / Q000378:metabolism; D009566:Nitrates / Q000378:metabolism*; D009584:Nitrogen / Q000378:metabolism; D009792:Oceans and Seas; D010802:Phylogeny; D048929:Prochlorococcus / Q000235:genetics* / Q000378:metabolism*; D014871:Water Microbiology
chemical_list: D009566:Nitrates; D050901:Nitrate Reductase; D009584:Nitrogen