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PubMed2002

Conserved and variable domains within divergent rnase P RNA gene sequences of Prochlorococcus strains.

RNase P RNA gene (rnpB) sequences were PCR-amplified from different members of the Prochlorococcus group. Aligned nucleotide sequences revealed a variance of up to 27% for rnpB. Comparative secondary structure analysis showed that domains P12, P18 and P19 of these novel ribozyme sequences in particular are highly divergent. Thus, these regions in RNase P RNA might serve as potential targets for deoxyoligonucleotide primers for the identification of specific genotypes of Prochlorococcus and for probing field populations. Phylogenetic trees constructed from RNase P RNA sequences were similar to, but not fully congruent with, those derived previously using sequences of the 16S rRNA gene. However, the application of rnpB sequences allowed a better resolution within clades of very closely related genotypes. As is known from 16S rRNA-based phylogenetic trees, sequences from individual strains clustered according to their physiology and the conditions at the original site of isolation, rather than their geographical origin. All sequences obtained from high-light-adapted strains formed a single coherent clade, as did the four sequences from low-light-adapted strains that were previously isolated from the North Atlantic and the subtropical North Pacific. This suggests a remarkable genetic stability of Prochlorococcus genotypes that thrive under identical ecological conditions.

Base Sequence↗
PubMed2004

Effects of high light on transcripts of stress-associated genes for the cyanobacteria Synechocystis sp. PCC 6803 and Prochlorococcus MED4 and MIT9313.

Cyanobacteria constitute an ancient, diverse and ecologically important bacterial group. The responses of these organisms to light and nutrient conditions are finely controlled, enabling the cells to survive a range of environmental conditions. In particular, it is important to understand how cyanobacteria acclimate to the absorption of excess excitation energy and how stress-associated transcripts accumulate following transfer of cells from low- to high-intensity light. In this study, quantitative RT-PCR was used to monitor changes in levels of transcripts encoding chaperones and stress-associated proteases in three cyanobacterial strains that inhabit different ecological niches: the freshwater strain Synechocystis sp. PCC 6803, the marine high-light-adapted strain Prochlorococcus MED4 and the marine low-light-adapted strain Prochlorococcus MIT9313. Levels of transcripts encoding stress-associated proteins were very sensitive to changes in light intensity in all of these organisms, although there were significant differences in the degree and kinetics of transcript accumulation. A specific set of genes that seemed to be associated with high-light adaptation (groEL/groES, dnaK2, dnaJ3, clpB1 and clpP1) could be targeted for more detailed studies in the future. Furthermore, the strongest responses were observed in Prochlorococcus MED4, a strain characteristic of the open ocean surface layer, where hsp genes could play a critical role in cell survival.

Bacterial Proteins↗
PubMed2000

In situ hybridization of Prochlorococcus and Synechococcus (marine cyanobacteria) spp. with RRNA-targeted peptide nucleic acid probes.

A simple method for whole-cell hybridization using fluorescently labeled rRNA-targeted peptide nucleic acid (PNA) probes was developed for use in marine cyanobacterial picoplankton. In contrast to established protocols, this method is capable of detecting rRNA in Prochlorococcus, the most abundant unicellular marine cyanobacterium. Because the method avoids the use of alcohol fixation, the chlorophyll content of Prochlorococcus cells is preserved, facilitating the identification of these cells in natural samples. PNA probe-conferred fluorescence was measured flow cytometrically and was always significantly higher than that of the negative control probe, with positive/negative ratio varying between 4 and 10, depending on strain and culture growth conditions. Prochlorococcus cells from open ocean samples were detectable with this method. RNase treatment reduced probe-conferred fluorescence to background levels, demonstrating that this signal was in fact related to the presence of rRNA. In another marine cyanobacterium, Synechococcus, in which both PNA and oligonucleotide probes can be used in whole-cell hybridizations, the magnitude of fluorescence from the former was fivefold higher than that from the latter, although the positive/negative ratio was comparable for both probes. In Synechococcus cells growing at a range of growth rates (and thus having different rRNA concentrations per cell), the PNA- and oligonucleotide-derived signals were highly correlated (r = 0.99). The chemical nature of PNA, the sensitivity of PNA-RNA binding to single-base-pair mismatches, and the preservation of cellular integrity by this method suggest that it may be useful for phylogenetic probing of whole cells in the natural environment.

Cyanobacteria↗
PubMed2001

In vivo regulation of glutamine synthetase activity in the marine chlorophyll b-containing cyanobacterium Prochlorococcus sp. strain PCC 9511 (oxyphotobacteria).

The physiological regulation of glutamine synthetase (GS; EC 6.3.1.2) in the axenic Prochlorococcus sp. strain PCC 9511 was studied. GS activity and antigen concentration were measured using the transferase and biosynthetic assays and the electroimmunoassay, respectively. GS activity decreased when cells were subjected to nitrogen starvation or cultured with oxidized nitrogen sources, which proved to be nonusable for Prochlorococcus growth. The GS activity in cultures subjected to long-term phosphorus starvation was lower than that in equivalent nitrogen-starved cultures. Azaserine, an inhibitor of glutamate synthase, provoked an increase in enzymatic activity, suggesting that glutamine is not involved in GS regulation. Darkness did not affect GS activity significantly, while the addition of diuron provoked GS inactivation. GS protein determination showed that azaserine induces an increase in the concentration of the enzyme. The unusual responses to darkness and nitrogen starvation could reflect adaptation mechanisms of Prochlorococcus for coping with a light- and nutrient-limited environment.

Adaptation, Physiological↗
PubMed2001

Diel expression of cell cycle-related genes in synchronized cultures of Prochlorococcus sp. strain PCC 9511.

The cell cycle of the chlorophyll b-possessing marine cyanobacterium Prochlorococcus is highly synchronized under natural conditions. To understand the underlying molecular mechanisms we cloned and sequenced dnaA and ftsZ, two key cell cycle-associated genes, and studied their expression. An axenic culture of Prochlorococcus sp. strain PCC 9511 was grown in a turbidostat with a 12 h-12 h light-dark cycle for 2 weeks. During the light periods, a dynamic light regimen was used in order to simulate the natural conditions found in the upper layers of the world's oceans. This treatment resulted in strong cell cycle synchronization that was monitored by flow cytometry. The steady-state mRNA levels of dnaA and ftsZ were monitored at 4-h intervals during four consecutive division cycles. Both genes exhibited clear diel expression patterns with mRNA maxima during the replication (S) phase. Western blot experiments indicated that the peak of FtsZ concentration occurred at night, i.e., at the time of cell division. Thus, the transcript accumulation of genes involved in replication and division is coordinated in Prochlorococcus sp. strain PCC 9511 and might be crucial for determining the timing of DNA replication and cell division.

Bacterial Proteins↗
PubMed1995

Sequencing of RAPD fragments amplified from the genome of the prokaryote Prochlorococcus marinus (prochlorophyta).

DNA fingerprint patterns from the chlorophyll a and b containing prokaryote Prochlorococcus marinus were generated with the RAPD technique using two primers derived from repetitive sequence motifs, [(GATA)4 and M13] and a random primer (OPB-10]. Five RAPD fragments were reamplified, cloned and sequenced. The clones M13/1300 and OPB-10/1100 contained open reading frames, whereas the (GATA)4 fragments were interrupted by stop codons in all frames indicating their noncoding function and possessed a high AT score of 63% and 71%, respectively. With the two (GATA)4 clones and the M13/300 clone strain-specific signals were obtained in a Southern blot analysis of various Prochlorococcus strains. Clones M13/1300 and OPB-10/1100, containing the ORFs, produced RFLPs between the strains analyzed. All RAPD fragments are represented as single copy in the genome of Prochlorococcus.

Bacteria↗
PubMed2004

Adaptive mechanisms of nitrogen and carbon assimilatory pathways in the marine cyanobacteria Prochlorococcus.

Prochlorococcus is an abundant marine cyanobacterium responsible for a significant part of global primary production. There exist various ecotypes adapted to conditions found along the water column, showing that largely modified photosynthetic apparatus efficiently harvest the light energy penetrating into their habitats. In view of the recent availability of three Prochlorococcus genomes, we review here additional adaptive changes observed in nitrogen and carbon metabolism.

Carbon↗
PubMed2005

Identification of a vinyl reductase gene for chlorophyll synthesis in Arabidopsis thaliana and implications for the evolution of Prochlorococcus species.

Chlorophyll metabolism has been extensively studied with various organisms, and almost all of the chlorophyll biosynthetic genes have been identified in higher plants. However, only the gene for 3,8-divinyl protochlorophyllide a 8-vinyl reductase (DVR), which is indispensable for monovinyl chlorophyll synthesis, has not been identified yet. In this study, we isolated an Arabidopsis thaliana mutant that accumulated divinyl chlorophyll instead of monovinyl chlorophyll by ethyl methanesulfonate mutagenesis. Map-based cloning of this mutant resulted in the identification of a gene (AT5G18660) that shows sequence similarity with isoflavone reductase genes. The mutant phenotype was complemented by the transformation with the wild-type gene. A recombinant protein encoded by AT5G18660 was expressed in Escherichia coli and found to catalyze the conversion of divinyl chlorophyllide to monovinyl chlorophyllide, thereby demonstrating that the gene encodes a functional DVR. DVR is encoded by a single copy gene in the A. thaliana genome. With the identification of DVR, finally all genes required for chlorophyll biosynthesis have been identified in higher plants. Analysis of the complete genome of A. thaliana showed that it has 15 enzymes encoded by 27 genes for chlorophyll biosynthesis from glutamyl-tRNA(glu) to chlorophyll b. Furthermore, identification of the DVR gene helped understanding the evolution of Prochlorococcus marinus, a marine cyanobacterium that is dominant in the open ocean and is uncommon in using divinyl chlorophylls. A DVR homolog was not found in the genome of P. marinus but found in the Synechococcus sp WH8102 genome, which is consistent with the distribution of divinyl chlorophyll in marine cyanobacteria of the genera Prochlorococcus and Synechococcus.

Amino Acid Sequence↗
PubMed2006

Genomic islands and the ecology and evolution of Prochlorococcus.

Prochlorococcus ecotypes are a useful system for exploring the origin and function of diversity among closely related microbes. The genetic variability between phenotypically distinct strains that differ by less that 1% in 16S ribosomal RNA sequences occurs mostly in genomic islands. Island genes appear to have been acquired in part by phage-mediated lateral gene transfer, and some are differentially expressed under light and nutrient stress. Furthermore, genome fragments directly recovered from ocean ecosystems indicate that these islands are variable among cooccurring Prochlorococcus cells. Genomic islands in this free-living photoautotroph share features with pathogenicity islands of parasitic bacteria, suggesting a general mechanism for niche differentiation in microbial species.

Adaptation, Physiological↗
PubMed2006

Oceanographic basis of the global surface distribution of Prochlorococcus ecotypes.

By using data collected during a continuous circumnavigation of the Southern Hemisphere, we observed clear patterns in the population-genetic structure of Prochlorococcus, the most abundant photosynthetic organism on Earth, between and within the three Southern Subtropical Gyres. The same mechanisms that were previously invoked to account for the vertical distribution of ecotypes at local scales accounted for the global (horizontal) patterns we observed. Basin-scale and seasonal variations in the structure and strength of vertical stratification provide a basis for understanding large-scale horizontal distribution in genetic and physiological traits of Prochlorococcus, and perhaps of marine microbial communities in general.

Atlantic Ocean↗
PubMed2005

Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations.

The oceanic cyanobacteria Prochlorococcus are globally important, ecologically diverse primary producers. It is thought that their viruses (phages) mediate population sizes and affect the evolutionary trajectories of their hosts. Here we present an analysis of genomes from three Prochlorococcus phages: a podovirus and two myoviruses. The morphology, overall genome features, and gene content of these phages suggest that they are quite similar to T7-like (P-SSP7) and T4-like (P-SSM2 and P-SSM4) phages. Using the existing phage taxonomic framework as a guideline, we examined genome sequences to establish "core" genes for each phage group. We found the podovirus contained 15 of 26 core T7-like genes and the two myoviruses contained 43 and 42 of 75 core T4-like genes. In addition to these core genes, each genome contains a significant number of "cyanobacterial" genes, i.e., genes with significant best BLAST hits to genes found in cyanobacteria. Some of these, we speculate, represent "signature" cyanophage genes. For example, all three phage genomes contain photosynthetic genes (psbA, hliP) that are thought to help maintain host photosynthetic activity during infection, as well as an aldolase family gene (talC) that could facilitate alternative routes of carbon metabolism during infection. The podovirus genome also contains an integrase gene (int) and other features that suggest it is capable of integrating into its host. If indeed it is, this would be unprecedented among cultured T7-like phages or marine cyanophages and would have significant evolutionary and ecological implications for phage and host. Further, both myoviruses contain phosphate-inducible genes (phoH and pstS) that are likely to be important for phage and host responses to phosphate stress, a commonly limiting nutrient in marine systems. Thus, these marine cyanophages appear to be variations of two well-known phages-T7 and T4-but contain genes that, if functional, reflect adaptations for infection of photosynthetic hosts in low-nutrient oceanic environments.

Bacteriophage T7↗
PubMed2003

A novel type of lycopene epsilon-cyclase in the marine cyanobacterium Prochlorococcus marinus MED4.

Chlorophyll- b-possessing cyanobacteria of the genus Prochlorococcus share the presence of high amounts of alpha- and beta-carotenoids with green algae and higher plants. The branch point in carotenoid biosynthesis is the cyclization of lycopene, for which in higher plants two distinct enzymes are required, epsilon- and beta-lycopene cyclase. All cyanobacteria studied so far possess a single beta-cyclase. Here, two different Prochlorococcus sp. MED4 genes were functionally identified by heterologous gene complementation in Escherichia coli to encode lycopene cyclases. Whereas one is both functionally and in sequence highly similar to the beta-cyclase of Synechococcus sp. strain PCC 7942 and other cyanobacteria, the other showed several intriguing features. It acts as a bifunctional enzyme catalyzing the formation of epsilon- as well as of beta-ionone end groups. Expression of this cyclase in E. coli resulted in the simultaneous accumulation of alpha- beta-, delta-, and epsilon-carotene. Such an activity is in contrast to all lycopene epsilon-cyclases known so far, including those of the higher plants. Thus, for the first time among prokaryotes, two individual enzymes were identified in one organism that are responsible for the formation of cyclic carotenoids with either beta- or epsilon-end groups. These two genes are suggested to be designated as crtL-b and crtL-e. The results indicate that both enzymes might have originated from duplication of a single gene. Consequently, we suggest that multiple gene duplications followed by functional diversification resulted several times, and in independent lineages, in the appearance of enzymes for the biosynthesis of cyclic carotenoids.

Amino Acid Sequence↗
PubMed2003

Two-component systems in Prochlorococcus MED4: genomic analysis and differential expression under stress.

Two-component signal transduction systems, composed of histidine sensory kinases and response regulators, constitute a key element of the mechanism by which bacteria sense and acclimatize to changes in their environment. The availability of whole genome sequences permits a detailed analysis of these genes in cyanobacteria. In the present paper, we focus mainly on Prochlorococcus MED4, a strain adapted to surface oceanic conditions, for which six putative response regulators (rer) and five putative histidine kinases (hik) were identified. These numbers are comparable to those found in the other marine picocyanobacteria but much lower than those found in freshwater cyanobacteria. Moreover, the diversity of these genes is low in Prochlorococcus since most histidine kinases are related to a single group (type I) and most response regulators to a single family (OmpR). Under standard conditions, quantitative reverse transcription polymerase chain reaction revealed that one hik (hik03) and two rer (rer04 and rer05) genes were expressed at relatively high levels compared to the other two-component system genes. In response to high light exposure, a moderate increase (>5-fold) was observed in the expression of some putative rer genes (rer01, rer04, rer05, and rer06), whereas a smaller increase (<3-fold) in hik03 and hik04 mRNA levels was detected. In contrast, both cold and heat shocks decreased rather than increased the expression of most hik and rer genes.

Amino Acid Sequence↗
PubMed2000

Rapid evolutionary divergence of Photosystem I core subunits PsaA and PsaB in the marine prokaryote Prochlorococcus.

The nucleotide sequences of the genes coding for the subunits of the Photosystem I (PS I) core, PsaA and PsaB were determined for the marine prokaryotic oxyphototrophs Prochlorococcus sp. MED4 (CCMP1378), P. marinus SS120 (CCMP1375) and Synechococcus sp. WH7803. Divergence of these sequences from those of both freshwater cyanobacteria and higher plants was remarkably high, given the conserved nature of PsaA and PsaB proteins. In particular, the PsaA of marine prokaryotes showed several specific insertions and deletions with regard to known PsaA sequences. Even in between the two Prochlorococcus strains, which correspond to two genetically different ecotypes with shifted growth irradiance optima, the sequence identity was only 80.2% for PsaA and 88.9% for PsaB. Possible causes and implications of the fast evolution rates of these two PS I core subunits are discussed.

Journal Article↗
PubMed1998

Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes.

The cyanobacterium Prochlorococcus is the dominant oxygenic phototroph in the tropical and subtropical regions of the world's oceans. It can grow at a range of depths over which light intensities can vary by up to 4 orders of magnitude. This broad depth distribution has been hypothesized to stem from the coexistence of genetically different populations adapted for growth at high- and low-light intensities. Here we report direct evidence supporting this hypothesis, which has been generated by isolating and analysing distinct co-occurring populations of Prochlorococcus at two locations in the North Atlantic. Co-isolates from the same water sample have very different light-dependent physiologies, one growing maximally at light intensities at which the other is completely photoinhibited. Despite this ecotypic differentiation, the co-isolates have 97% similarity in their 16S ribosomal RNA sequences, demonstrating that molecular microdiversity, commonly observed in microbial systems, can be due to the coexistence of closely related, physiologically distinct populations. The coexistence and distribution of multiple ecotypes permits the survival of the population as a whole over a broader range of environmental conditions than would be possible for a homogeneous population.

Cyanobacteria↗
PubMed2003

Experimental and computational analysis of transcriptional start sites in the cyanobacterium Prochlorococcus MED4.

In contrast to certain model eubacteria, little is known as to where transcription is initiated in the genomes of cyanobacteria, which are largely distinct from other prokaryotes. In this work, 25 transcription start sites (TSS) of 21 different genes of Prochlorococcus sp. MED4 were determined experimentally. The data suggest more than one TSS for the genes ftsZ, petH, psbD and ntcA. In contrast, the rbcL-rbcS operon encoding ribulose 1,5-bisphosphate carboxylase/oxygenase lacks a detectable promoter and is co-transcribed with the upstream located gene ccmK. The entire set of experimental data was used in a genome-wide scan for putative TSS in Prochlorococcus. A -10 element could be defined, whereas at the -35 position there was no element common to all investigated sequences. However, splitting the data set into sub-classes revealed different types of putative -35 boxes. Only one of them resembled the consensus sequence TTGACA recognized by the vegetative sigma factor (sigma70) of enterobacteria. Using a scoring matrix of the -10 element, more than 3000 TSS were predicted, about 40% of which were estimated to be functional. This is the first systematic study of transcription initiation sites in a cyanobacterium.

Base Sequence↗
PubMed1998

Ultradian Growth in Prochlorococcus spp.

Species of the widespread marine prokaryote Prochlorococcus exhibited ultradian growth (faster than 1 division per day) both in situ and in culture, even though cell division is strictly phased to the light-dark cycle. Under optimal conditions a second DNA replication and cell division closely followed, but did not overlap with, the first division. The timing of cell cycle events was not affected by light intensity or duration, suggesting control by a light-triggered timer or circadian clock rather than by completion of a light-dependent assimilation phase. This mode of ultradian growth has not been observed previously and poses new questions about the regulation of cellular rhythms in prokaryotes. In addition, it implies that conclusions regarding the lack of nutrient limitation of Prochlorococcus in the open ocean, which were based on the appearance that cells were growing at their maximal rate, need to be reconsidered.

Journal Article↗
PubMed2003

High rate of uptake of organic nitrogen compounds by Prochlorococcus cyanobacteria as a key to their dominance in oligotrophic oceanic waters.

Direct evidence that marine cyanobacteria take up organic nitrogen compounds in situ at high rates is reported. About 33% of the total bacterioplankton turnover of amino acids, determined with a representative [(35)S]methionine precursor and flow sorting, can be assigned to Prochlorococcus spp. and 3% can be assigned to Synechococcus spp. in the oligotrophic and mesotrophic parts of the Arabian Sea, respectively. This finding may provide a mechanism for Prochlorococcus' competitive dominance over both strictly autotrophic algae and other bacteria in oligotrophic regions sustained by nutrient remineralization via a microbial loop.

Amino Acids↗