The marine unicellular cyanobacterium Prochlorococcus is the smallest-known oxygen-evolving autotroph. It numerically dominates the phytoplankton in the tropical and subtropical oceans, and is responsible for a significant fraction of global photosynthesis. Here we compare the genomes of two Prochlorococcus strains that span the largest evolutionary distance within the Prochlorococcus lineage and that have different minimum, maximum and optimal light intensities for growth. The high-light-adapted ecotype has the smallest genome (1,657,990 base pairs, 1,716 genes) of any known oxygenic phototroph, whereas the genome of its low-light-adapted counterpart is significantly larger, at 2,410,873 base pairs (2,275 genes). The comparative architectures of these two strains reveal dynamic genomes that are constantly changing in response to myriad selection pressures. Although the two strains have 1,350 genes in common, a significant number are not shared, and these have been differentially retained from the common ancestor, or acquired through duplication or lateral transfer. Some of these genes have obvious roles in determining the relative fitness of the ecotypes in response to key environmental variables, and hence in regulating their distribution and abundance in the oceans.
SUMMARY Marine picocyanobacteria of the genera Prochlorococcus and Synechococcus numerically dominate the picophytoplankton of the world ocean, making a key contribution to global primary production. Prochlorococcus was isolated around 20 years ago and is probably the most abundant photosynthetic organism on Earth. The genus comprises specific ecotypes which are phylogenetically distinct and differ markedly in their photophysiology, allowing growth over a broad range of light and nutrient conditions within the 45°N to 40°S latitudinal belt that they occupy. Synechococcus and Prochlorococcus are closely related, together forming a discrete picophytoplankton clade, but are distinguishable by their possession of dissimilar light-harvesting apparatuses and differences in cell size and elemental composition. Synechococcus strains have a ubiquitous oceanic distribution compared to that of Prochlorococcus strains and are characterized by phylogenetically discrete lineages with a wide range of pigmentation. In this review, we put our current knowledge of marine picocyanobacterial genomics into an environmental context and present previously unpublished genomic information arising from extensive genomic comparisons in order to provide insights into the adaptations of these marine microbes to their environment and how they are reflected at the genomic level.
Phylogenetic relationships among members of the marine Synechococcus genus were determined following sequencing of the 16S ribosomal DNA (rDNA) from 31 novel cultured isolates from the Red Sea and several other oceanic environments. This revealed a large genetic diversity within the marine Synechococcus cluster consistent with earlier work but also identified three novel clades not previously recognized. Phylogenetic analyses showed one clade, containing halotolerant isolates lacking phycoerythrin (PE) and including strains capable, or not, of utilizing nitrate as the sole N source, which clustered within the MC-A (Synechococcus subcluster 5.1) lineage. Two copies of the 16S rRNA gene are present in marine Synechococcus genomes, and cloning and sequencing of these copies from Synechococcus sp. strain WH 7803 and genomic information from Synechococcus sp. strain WH 8102 reveal these to be identical. Based on the 16S rDNA sequence information, clade-specific oligonucleotides for the marine Synechococcus genus were designed and their specificity was optimized. Using dot blot hybridization technology, these probes were used to determine the in situ community structure of marine Synechococcus populations in the Red Sea at the time of a Synechococcus maximum during April 1999. A predominance of genotypes representative of a single clade was found, and these genotypes were common among strains isolated into culture. Conversely, strains lacking PE, which were also relatively easily isolated into culture, represented only a minor component of the Synechococcus population. Genotypes corresponding to well-studied laboratory strains also appeared to be poorly represented in this stratified water column in the Red Sea.
Prochlorococcus is the most abundant phytoplankter throughout the photic zone in stratified marine waters and experiences distinct gradients of light and nitrogen nutrition. Physiologically and genetically distinct Prochlorococcus ecotypes partition the water column: high-B/A (low-light adapted) ecotypes are generally restricted to the deep euphotic zone near or at the nitracline. Low-B/A (high-light adapted) ecotypes predominate in, but are not limited to, NO -depleted surface waters, where they outnumber coexisting Synechococcus populations. The niche parti-tioning by different Prochlorococcus ecotypes begs the question of whether they also differ in their nitrogen (N) utilization physiology, especially with respect to NO utilization. To explore this possibility, we studied the capa-Ϫ 3 bilities of different Prochlorococcus and Synechococcus strains to grow on a variety of N sources. We found that all the isolates grew well on NH and all were capable of urea utilization, occasionally at a lower growth rate. physiology and ecology. Thus, the utilization of different N sources in the marine environment is partitioned among closely related ecotypes, each with adaptations optimized for the environment where these sources are available.Since the first description of unicellular cyanobacteria as an abundant component of the marine phytoplankton community (Johnson and Sieburth 1979), the genus Synechococcus has been established as a major primary producer in the surface ocean. Synechococcus presence has been reported from waters in the (sub)tropics, temperate, and even polar regions and is often the dominant phytoplankter in both nutrient-deplete stratified, and nutrient-rich mixed waters (Par-
Background: The picocyanobacterial genus Synechococcus occurs over wide oceanic expanses, having colonized most available niches in the photic zone. Large scale distribution patterns of the different Synechococcus clades (based on 16S rRNA gene markers) suggest the occurrence of two major lifestyles ('opportunists'/'specialists'), corresponding to two distinct broad habitats ('coastal'/'open ocean'). Yet, the genetic basis of niche partitioning is still poorly understood in this ecologically important group.
contributed equally to this work Proteorhodopsins, ubiquitous retinylidene photoactive proton pumps, were recently discovered in the cosmopolitan uncultured SAR86 bacterial group in oceanic surface waters. Two related proteorhodopsin families were found that absorb light with different absorption maxima, 525 nm (green) and 490 nm (blue), and their distribution was shown to be strati®ed with depth. Using structural modeling comparisons and mutagenesis, we report here on a single amino acid residue at position 105 that functions as a spectral tuning switch and accounts for most of the spectral difference between the two pigment families. Furthermore, looking at natural environments, we found novel proteorhodopsin gene clusters spanning the range of 540±505 nm and containing changes in the same identi®ed key switch residue leading to changes in their absorption maxima. The results suggest a simultaneous diversi®cation of green proteorhodopsin and the new key switch variant pigments. Our observations demonstrate that this single-residue switch mechanism is the major determinant of proteorhodopsin wavelength regulation in natural marine environments.
Atmospheric aerosol deposition is an important source of nutrients and trace metals to the open ocean that can enhance ocean productivity and carbon sequestration and thus influence atmospheric carbon dioxide concentrations and climate. Using aerosol samples from different back trajectories in incubation experiments with natural communities, we demonstrate that the response of phytoplankton growth to aerosol additions depends on specific components in aerosols and differs across phytoplankton species. Aerosol additions enhanced growth by releasing nitrogen and phosphorus, but not all aerosols stimulated growth. Toxic effects were observed with some aerosols, where the toxicity affected picoeukaryotes and Synechococcus but not Prochlorococcus. We suggest that the toxicity could be due to high copper concentrations in these aerosols and support this by laboratory copper toxicity tests preformed with Synechococcus cultures. However, it is possible that other elements present in the aerosols or unknown synergistic effects between these elements could have also contributed to the toxic effect. Anthropogenic emissions are increasing atmospheric copper deposition sharply, and based on coupled atmosphere-ocean calculations, we show that this deposition can potentially alter patterns of marine primary production and community structure in high aerosol, low chlorophyll areas, particularly in the Bay of Bengal and downwind of South and East Asia.L aboratory experiments, field observations, and numerical simulations all link atmospheric deposition events to increases in ocean chlorophyll concentrations and phytoplankton biomass (1-3), suggesting that atmospheric deposition of nutrients and trace metals can stimulate phytoplankton growth. Indeed, enrichment experiments with iron (a required nutrient scarce in seawater and enriched in dust) show that in highnutrient low-chlorophyll areas (representing 20-40% of the ocean), iron addition can increase primary production, export production, and carbon sequestration (4-7). In areas where phosphorus and nitrogen concentrations are low, aerosol deposition can supply both iron and phosphate, nutrients that stimulate nitrogen fixation (8-9). It has been suggested that increases in dust deposition during glacial periods have been responsible for lowering atmospheric carbon dioxide concentrations thus impacting climate (10-12).Aerosol particles consist of many natural and anthropogenic components, including mineral dust, soot, organic molecules, sea salt crystals, spores, bacteria, and other microscopic particles (13), and can supply many elements and compounds to seawater (14-16). Little research has been done to elucidate what specific component(s) in aerosols affect phytoplankton at the level of community or individual species or how certain taxa within the community respond to distinct aerosol deposition events and to aerosols of different composition. Results and DiscussionTo assess the short-term response of phytoplankton communities to aerosol deposition, we performed bioassay e...
The seasonal dynamics of ultraphytoplankton for the northern Gulf of Aqaba (29"28'N, 34"55'E) were investigated in detail. Monthly analysis of pigments by HPLC and cell abundances by epifluorescence microscopy showed large fluctuations in ultraphytoplankton community structure concurrent with strong seasonal changes in water-column conditions. Following extensive winter mixing, ultraphytoplankton seasonal succession progressed rapidly as water-column stratification strengthened. Eucaryotic algae dominated in nutrient-replete winter mixing conditions, Synechococcus was the major component of the ultraphytoplankton during a spring bloom of massive proportions, and Prochlorococcus was dominant in nutrient-depleted summer-stratified waters. Over the fall-winter period, as water-column mixing progressed, succession was in the reverse order but at a much slower rate. Prochlorococcus was the major component of the community during summer stratification, yet was not detected at the height of the mixing event in late winter. The reestablishment of the population occurred only 3 months after the onset of stratification. This is the first report on seasonal succession involving all three ultraphytoplankton groups. We suggest that water-column stability is an important factor influencing seasonal variations in ultraphytoplankton community structure.For some time, water-column conditions have been known to affect phytoplankton community structure. In oceanic regions of low latitudes, conditions are fairly constant throughout the year, with stably stratified waters that are usually limiting in nutrients (with the exception of equatorial upwelling regions). As such, phytoplankton community structure in these environments is fairly stable (Campbell and Vaulot 1993; Cushing 1989). Subtropical and temperate latitude environments undergo noticeable changes in water-column conditions during the year. The seasonal thermocline existing in summer is progressively eroded by convective mixing that often reaches below the euphotic zone in winter. As a result, the euphotic zone alternates from a stratified water body with fairly constant levels of light and nutrients to a mixed water column in which the phytoplankton experience lower temperatures, continually changing light conditions, and higher concentrations of nutrients. Striking variations in phytoplankton community structure are
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