Phosphate acquisition genes in Prochlorococcus ecotypes

Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 09/2006; 103(33):12552-7. DOI: 10.1073/pnas.0601301103
Source: PubMed


The cyanobacterium Prochlorococcus is the numerically dominant phototroph in the oligotrophic oceans. This group consists of multiple ecotypes that are physiologically and phylogenetically distinct and occur in different abundances along environmental gradients. Here we examine adaptations to phosphate (P) limitation among ecotypes. First, we used DNA microarrays to identify genes involved in the P-starvation response in two strains belonging to different ecotypes, MED4 (high-light-adapted) and MIT9313 (low-light-adapted). Most of the up-regulated genes under P starvation were unique to one strain. In MIT9313, many ribosomal genes were down-regulated, suggesting a general stress response in this strain. We also observed major differences in regulation. The P-starvation-induced genes comprise two clusters on the chromosome, the first containing the P master regulator phoB and most known P-acquisition genes and the second, absent in MIT9313, containing genes of unknown function. We examined the organization of the phoB gene cluster in 11 Prochlorococcus strains belonging to diverse ecotypes and found high variability in gene content that was not congruent with rRNA phylogeny. We hypothesize that this genome variability is related to differences in P availability in the oceans from which the strains were isolated. Analysis of a metagenomic library from the Sargasso Sea supports this hypothesis; most Prochlorococcus cells in this low-P environment contain the P-acquisition genes seen in MED4, although a number of previously undescribed gene combinations were observed.

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    • "In the Sargasso Sea, most of the total dissolved phosphorus is found as DOP (Ammerman et al., 2003) and Pi concentrations in surface waters can be lower than 1 nM (Wu, 2000; Lomas et al., 2010). However, there are regional differences in the concentrations of DOP and SRP and with various sources available, different strategies for P assimilation and allocation can be employed by picophytoplankton (Moore et al., 2005; Martiny et al., 2006; Van Mooy and Devol, 2008; Casey et al., 2009). "
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    ABSTRACT: Phosphate (P) is an important nutrient potentially limiting for primary productivity, yet, we currently know little about the relationship between growth rate and physiological response to P limitation in abundant marine Cyanobacteria. Thus, the aim of this research was to determine how variation in growth rate affected the physiology of marine Synechococcus WH8102 and CC9311 when growing under high N:P conditions. Experiments were carried out in chemostats with a media input N:P of 441 and we estimated the half saturation concentration for growth under P limiting conditions (K s,p) and cellular C:N:P ratios. The K s,p values were the lowest measured for any phytoplankton and on par with ambient P concentrations in oligotrophic regions. We also observed that both strains were able draw down P below 3 nM. Both K s,p and drawdown concentration were lower for the open ocean vs. coastal Synechococcus strain, which may be linked to differences in P acquisition genes in these strains. Cellular C:P and N:P ratios were significantly higher in relation to the Redfield ratio for both Synechococcus strains but we saw no difference in these ratios among growth rates or strains. These results demonstrate that Synechococcus can proliferate under very low P conditions and also that genetically different strains have unique physiological responses to P limitation.
    Frontiers in Microbiology 03/2015; 6. DOI:10.3389/fmicb.2015.00085 · 3.99 Impact Factor
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    • "Gene content in Prochlorococcus has been shown, for several traits, to reflect the 369 selective pressures in the specific environments from which they (or their genes) were 370 ACCEPTED AUTHOR MANUSCRIPT captured (Martiny et al., 2006; Coleman & Chisholm, 2010; Feingersch et al., 2012; 371 Malmstrom et al., 2013; Rusch et al., 2007). Thus, we wondered if other nitrogen assimilation 372 traits might co-occur with nitrate assimilation in Prochlorococcus, and examined the potential 373 for PAC1, SB, and MIT0604 to access alternative sources of nitrogen based on their gene 374 content (Supplementary Table S1 and Supplementary Figure S5). "
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    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.
    The ISME Journal 10/2014; 9(5). DOI:10.1038/ismej.2014.211 · 9.30 Impact Factor
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    • "Results from the two studies show that SAR11 phosphate and phosphonate transporters are abundant in the ocean gyre ecosystem but nearly absent from the Oregon shelf upwelling system. Meanwhile , other studies show that the proteins involved in phosphorus transport are more abundant in terms of phosphatestarvation [30] [31], this further demonstrates that oceanic oligotrophic gyre surface water has more chance to be subjected to phosphorus-limitation than productive coastal surface water. In addition, the substrates of SAR11 transport proteins are mainly carbon-and nitrogen-containing compounds, but not phosphate, suggesting that carbon and nitrogen, rather than phosphorus, are the major factors for the niche differentiation and productivity limitation in this productive region. "
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    ABSTRACT: Metaproteomics is a new field within the 'omics' science which investigates protein expression from a complex biological system and provides direct evidence of physiological and metabolic activities. Characterization of the metaproteome will enhance our understanding of the microbial world and link microbial communities to ecological functions. Recently, the availability of extensive metagenomic sequences from various marine microbial communities has extended the postgenomic era to the field of oceanography. Although still in its infancy, metaproteomics has shown its powerful potential with regard to functional gene expression within microbial habitats and their interactions with the ambient environment as well as their biogeochemical functions. However, the application of metaproteomic approaches to complex marine samples still faces considerable challenges. This review summarizes the recent progress in marine metaproteomics and discusses the limitations of and perspectives for this approach in the study of the marine ecosystem.
    Journal of proteomics 01/2014; 97:27-35. DOI:10.1016/j.jprot.2013.08.024 · 3.89 Impact Factor
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