Widespread metabolic potential for nitrite and nitrate assimilation among Prochlorococcus ecotypes

Abstract

The marine cyanobacterium Prochlorococcus is the most abundant photosynthetic organism in oligotrophic regions of the oceans. The inability to assimilate nitrate is considered an important factor underlying the distribution of Prochlorococcus, and thought to explain, in part, low abundance of Prochlorococcus in coastal, temperate, and upwelling zones. Here, we describe the widespread occurrence of a genomic island containing nitrite and nitrate assimilation genes in uncultured Prochlorococcus cells from marine surface waters. These genes are characterized by low GC content, form a separate phylogenetic clade most closely related to marine Synechococcus, and are located in a different genomic region compared with an orthologous cluster found in marine Synechococcus strains. This sequence distinction suggests that these genes were not transferred recently from Synechococcus. We demonstrate that the nitrogen assimilation genes encode functional proteins and are expressed in the ocean. Also, we find that their relative occurrence is higher in the Caribbean Sea and Indian Ocean compared with the Sargasso Sea and Eastern Pacific Ocean, which may be related to the nitrogen availability in each region. Our data suggest that the ability to assimilate nitrite and nitrate is associated with microdiverse lineages within high-and low-light (LL) adapted Prochlorococcus ecotypes. It challenges 2 long-held assumptions that (i) Prochlorococcus cannot assimilate nitrate, and (ii) only LL adapted ecotypes can use nitrite. The potential for previously unrecognized productivity by Prochlorococcus in the presence of oxidized nitrogen species has implications for understanding the biogeography of Prochlorococcus and its role in the oceanic carbon and nitrogen cycles.metagenomics ͉ cyanobacteria ͉ nitrogen cycle ͉ narB ͉ nirA

Genomic island genes in a coastal marine Synechococcus strain confer enhanced tolerance to copper and oxidative stress

“…In Prochlorococcus, macronutrient levels in the ocean are predicted to drive genomic content and ecotype formation, potentially through lateral gene transfer Martiny et al, 2006Martiny et al, , 2009aMartiny et al, , 2009b. Although copper and oxidative stress response genes may be less recognizable than nutrient acquisition genes, our data predicts that this stress response differentiation can also influence genomic content and may be an additional mechanism driving population structure in picocyanobacteria.…”

Global biogeography of Prochlorococcus genome diversity in the surface ocean

“…Additionally, the greater variability in the genomic context of environmental assemblies versus sequenced strains suggests that the assemblies are capturing new genomic backbones to some extent. Thus strains in culture may not fully represent Prochlorococcus diversity as it relates to temperature adaptation-as was recently observed for nitrogen assimilation (Martiny et al, 2009b;Berube et al, 2015). In Synechococcus, variation has been observed in the thermal niches of strains consistent with the thermal range of their isolation location.…”

“…Nitrogen assimilation genes significant in the indicator analysis were almost always associated with the Equatorial Pacific Ocean (Supplementary Table S4; Martiny et al, 2009b). Most were negatively associated specifically with the Equatorial Pacific Ocean and South Atlantic Ocean (napA-a nitrate/ nitrite transporter and moaA-a molybdenum cofactor biosynthesis protein necessary for nitrate reductase) or with these two regions and a third (North Atlantic Ocean: narB-an assimilatory nitrate reductase; South Pacific Ocean: moeA-molydobpterin biosynthesis protein, a cofactor necessary for nitrate reductase; North Indian Ocean: an agmatinase; Supplementary Table S4).…”

“…For example, many genes differentially distributed along the nitrogen gradient. This includes previously identified genes responsible for nitrate uptake present in lower nitrogen waters (Martiny et al, 2009b) as well as a higher frequency of genes related to reduced nitrogen uptake in Equatorial Pacific and South Atlantic Oceans. In an environmental context, average annual nitrate concentrations of these two regions were higher than other regions (Garcia et al, 2010), and our data suggest that there appears to be a shift in nitrogen assimilation between oxidized and reduced forms of nitrogen, in contrast to phosphate, which simply drives the acquisition or loss of specialized transport.…”

Analogous nutrient limitations in unicellular diazotrophs and Prochlorococcus in the South Pacific Ocean

“…This genotype is part of a Prochlorococcus clade termed high light ecotype (Moore et al, 1998) and several other Prochlorococcus strains with unique characteristics share closely similar ribosomal RNA genes with this type strain (Rocap et al, 2002;Zinser et al, 2006). While some uncultivated Prochlorococcus are thought to acquire nitrate (Martiny et al, 2009), none of the cultivated strains have this capability. In the Sargasso Sea, Prochlorococcus pigment content responded positively to NH 4 NO 3 additions, although nitrate alone or iron had no effect (Davey et al, 2008;Moore et al, 2008).…”