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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    • "Specifically, light and temperature drove ancient niche differentiation at higher taxonomic levels, nutrient acquisition drove mid-level differentiation and phage/grazer resistance drove more recent fine-scale genotype selection at the 'leaves' of the Prochlorococcus phylogenetic tree (Coleman and Chisholm, 2007). For example, phosphorus or nitrate acquisition genes have been shown to be polyphyletic in Prochlorococcus (Martiny et al., 2006;Berube et al., 2014), whereas photosynthesis and light harvesting genes show more basal patterns (Scanlan et al., 2009). However, genomic signatures for other important environmental variables such as temperature have yet to be identified (Kettler et al., 2007;Scanlan et al., 2009), even though there are clear physiological and biogeographic differences among ecotypes (Johnson et al., 2006). "
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    ABSTRACT: The distribution of major clades of Prochlorococcus tracks light, temperature and other environmental variables; yet, the drivers of genomic diversity within these ecotypes and the net effect on biodiversity of the larger community are poorly understood. We examined high light (HL) adapted Prochlorococcus communities across spatial and temporal environmental gradients in the Pacific Ocean to determine the ecological drivers of population structure and diversity across taxonomic ranks. We show that the Prochlorococcus community has the highest diversity at low latitudes, but seasonality driven by temperature, day length and nutrients adds complexity. At finer taxonomic resolution, some 'sub-ecotype' clades have unique, cohesive responses to environmental variables and distinct biogeographies, suggesting that presently defined ecotypes can be further partitioned into ecologically meaningful units. Intriguingly, biogeographies of the HL-I sub-ecotypes are driven by unique combinations of environmental traits, rather than through trait hierarchy, while the HL-II sub-ecotypes appear ecologically similar, thus demonstrating differences among these dominant HL ecotypes. Examining biodiversity across taxonomic ranks reveals high-resolution dynamics of Prochlorococcus evolution and ecology that are masked at phylogenetically coarse resolution. Spatial and seasonal trends of Prochlorococcus communities suggest that the future ocean may be comprised of different populations, with implications for ecosystem structure and function.The ISME Journal advance online publication, 22 January 2016; doi:10.1038/ismej.2015.244.
    No preview · Article · Jan 2016 · The ISME Journal
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    • "Thus, the variability in the rrn operon copy number could reflect broader life history strategies in which each taxa uses different sets of resources or inhabits distinct microhabitats in structured sediments, potentially decreasing competition. In agreement with this view, various bacterial communities have been shown to have similar functional heterogeneity regarding other important ecological traits (Martínez-Alonso et al., 2004;Giovannoni and Stingl, 2005;Martiny et al., 2006). Additional work is needed to understand the importance of conserving high rrn operon copy numbers in CCB Bacillus. "
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    ABSTRACT: The ribosomal RNA (rrn) operon is a key suite of genes related to the production of protein synthesis machinery and thus to bacterial growth physiology. Experimental evidence has suggested an intrinsic relationship between the number of copies of this operon and environmental resource availability, especially the availability of phosphorus (P), because bacteria that live in oligotrophic ecosystems usually have few rrn operons and a slow growth rate. The Cuatro Ciénegas Basin (CCB) is a complex aquatic ecosystem that contains an unusually high microbial diversity that is able to persist under highly oligotrophic conditions. These environmental conditions impose a variety of strong selective pressures that shape the genome dynamics of their inhabitants. The genus Bacillus is one of the most abundant cultivable bacterial groups in the CCB and usually possesses a relatively large number of rrn operon copies (6–15 copies). The main goal of this study was to analyze the variation in the number of rrn operon copies of Bacillus in the CCB and to assess their growth-related properties as well as their stoichiometric balance (N and P content). We defined 18 phylogenetic groups within the Bacilli clade and documented a range of from six to 14 copies of the rrn operon. The growth dynamic of these Bacilli was heterogeneous and did not show a direct relation to the number of operon copies. Physiologically, our results were not consistent with the Growth Rate Hypothesis, since the copies of the rrn operon were decoupled from growth rate. However, we speculate that the diversity of the growth properties of these Bacilli as well as the low P content of their cells in an ample range of rrn copy number is an adaptive response to oligotrophy of the CCB and could represent an ecological mechanism that allows these taxa to coexist. These findings increase the knowledge of the variability in the number of copies of the rrn operon in the genus Bacillus and give insights about the physiology of this bacterial group under extreme oligotrophic conditions.
    Full-text · Article · Jan 2016 · Frontiers in Microbiology
    • "Many of these genes are found on genomic islands (Coleman et al., 2006) and some have been acquired by horizontal transfer (Rocap et al., 2003). Thus, the occurrence of phosphate acquisition genes is not congruent with 16S rRNA phylogeny (Martiny et al., 2006), but can be correlated with phosphate concentrations in the regions these strains were isolated from. In the field, Prochlorococcus populations in phosphorus-scarce regions contain a greater number of phosphorus acquisition genes, indicating the selective force of nutrient availability on Prochlorococcus genetic capacity (Martiny et al., 2009). "
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    ABSTRACT: The globally significant picocyanobacterium Prochlorococcus is the main primary producer in oligotrophic subtropical gyres. When phosphate concentrations are very low in the marine environment, the mol:mol availability of phosphate relative to the chemically similar arsenate molecule is reduced, potentially resulting in increased cellular arsenic exposure. To mediate accidental arsenate uptake, some Prochlorococcus isolates contain genes encoding a full or partial efflux detoxification pathway, consisting of an arsenate reductase (arsC), an arsenite-specific efflux pump (acr3) and an arsenic-related repressive regulator (arsR). This efflux pathway was the only previously known arsenic detox pathway in Prochlorococcus. We have identified an additional putative arsenic mediation strategy in Prochlorococcus driven by the enzyme arsenite S-adenosylmethionine methyltransferase (ArsM) which can convert inorganic arsenic into more innocuous organic forms and appears to be a more widespread mode of detoxification. We used a phylogenetically informed approach to identify Prochlorococcus linked arsenic genes from both pathways in the Global Ocean Sampling survey. The putative arsenic methylation pathway is nearly ubiquitously present in global Prochlorococcus populations. In contrast, the complete efflux pathway is only maintained in populations which experience extremely low PO4:AsO4, such as regions in the tropical and subtropical Atlantic. Thus, environmental exposure to arsenic appears to select for maintenance of the efflux detoxification pathway in Prochlorococcus. The differential distribution of these two pathways has implications for global arsenic cycling, as their associated end products, arsenite or organoarsenicals, have differing biochemical activities and residence times.The ISME Journal advance online publication, 7 July 2015; doi:10.1038/ismej.2015.85.
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