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we put our current knowledge of marine picocyanobacterial genomics into an environmental context and present previously unpublished genomic information arising from extensive genomic comparisons in order to provide insights into the adaptations of these marine microbes to their environment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.
Marine cyanobacteria of the genera Prochlorococcus and Synechococcus are important contributors to global primary production occupying a key position at the base of marine food webs. The genetically diverse nature of each genus is likely an important reason for their successful colonization of vast tracts of the world's oceans, a feature that has led to detailed analysis of the distribution of these genetic lineages at the local and ocean basin scale. Here, we extend these analyses to the global dimension, using new data from cruises in the Pacific, Indian and Arctic Oceans in combination with data from previous studies in the Atlantic Ocean, Arabian Sea, Red Sea and a circumnavigation of the southern hemisphere to form a data set which comprises most of the world's major ocean systems. We show that the distribution patterns of Prochlorococcus and Synechococcus lineages are remarkably similar in different ocean systems with comparable environmental conditions, but producing a strikingly different 'signature' in the four major ocean domains or biomes (the Polar Domain, Coastal Boundary Domain, Trade Winds Domain and Westerly Winds Domain). This clearly reiterates the idea of spatial partitioning of individual cyanobacterial lineages, but at the global scale.
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.
Phycobilisome diversity and evolution By comparing Synechococcus genomes, candidate genes required for the production of phycobiliproteins, which are part of the lightharvesting antenna complexes called phycobilisomes, were identified. Phylogenetic analyses suggest that the phycobilisome core evolved together with the core genome, whereas rods evolved independently.
Prochlorococcus marinus, the dominant photosynthetic organism in the ocean, is found in two main ecological forms: high-light-adapted genotypes in the upper part of the water column and low-lightadapted genotypes at the bottom of the illuminated layer. P. marinus SS120, the complete genome sequence reported here, is an extremely low-light-adapted form. The genome of P. marinus SS120 is composed of a single circular chromosome of 1,751,080 bp with an average G؉C content of 36.4%. It contains 1,884 predicted protein-coding genes with an average size of 825 bp, a single rRNA operon, and 40 tRNA genes. Together with the 1.66-Mbp genome of P. marinus MED4, the genome of P. marinus SS120 is one of the two smallest genomes of a photosynthetic organism known to date. It lacks many genes that are involved in photosynthesis, DNA repair, solute uptake, intermediary metabolism, motility, phototaxis, and other functions that are conserved among other cyanobacteria. Systems of signal transduction and environmental stress response show a particularly drastic reduction in the number of components, even taking into account the small size of the SS120 genome. In contrast, housekeeping genes, which encode enzymes of amino acid, nucleotide, cofactor, and cell wall biosynthesis, are all present. Because of its remarkable compactness, the genome of P. marinus SS120 might approximate the minimal gene complement of a photosynthetic organism.
Prochlorococcus and Synechococcus are the two most abundant and widespread phytoplankton in the global ocean. To better understand the factors controlling their biogeography, a reference database of the high-resolution taxonomic marker petB, encoding cytochrome b 6 , was used to recruit reads out of 109 metagenomes from the Tara Oceans expedition. An unsuspected novel genetic diversity was unveiled within both genera, even for the most abundant and well-characterized clades, and 136 divergent petB sequences were successfully assembled from metagenomic reads, significantly enriching the reference database. We then defined Ecologically Significant Taxonomic Units (ESTUs)-that is, organisms belonging to the same clade and occupying a common oceanic niche. Three major ESTU assemblages were identified along the cruise transect for Prochlorococcus and eight for Synechococcus. Although Prochlorococcus HLIIIA and HLIVA ESTUs codominated in irondepleted areas of the Pacific Ocean, CRD1 and the yet-to-be cultured EnvB were the prevalent Synechococcus clades in this area, with three different CRD1 and EnvB ESTUs occupying distinct ecological niches with regard to iron availability and temperature. Sharp community shifts were also observed over short geographic distances-for example, around the Marquesas Islands or between southern Indian and Atlantic Oceans-pointing to a tight correlation between ESTU assemblages and specific physico-chemical parameters. Together, this study demonstrates that there is a previously overlooked, ecologically meaningful, fine-scale diversity within some currently defined picocyanobacterial ecotypes, bringing novel insights into the ecology, diversity, and biology of the two most abundant phototrophs on Earth. molecular ecology | metagenomics | Tara Oceans | Synechococcus | Prochlorococcus
Conserved markers such as the 16S rRNA gene do not provide sufficient molecular resolution to identify spatially structured populations of marine Synechococcus, or 'ecotypes' adapted to distinct ecological niches. Multi-locus sequence analysis targeting seven 'core' genes was employed to taxonomically resolve Synechococcus isolates and correlate previous phylogenetic analyses encompassing a range of markers. Despite the recognized importance of lateral gene transfer in shaping the genomes of marine cyanobacteria, multi-locus sequence analysis of more than 120 isolates reflects a clonal population structure of major lineages and subgroups. A single core genome locus, petB, encoding the cytochrome b(6) subunit of the cytochrome b(6) f complex, was selected to expand our understanding of the diversity and ecology of marine Synechococcus populations. Environmental petB sequences cloned from contrasting sites highlight numerous genetically and ecologically distinct clusters, some of which represent novel, environmentally abundant clades without cultured representatives. With a view to scaling ecological analyses, the short sequence, taxonomic resolution and accurate automated alignment of petB is ideally suited to high-throughput and high-resolution sequencing projects to explore links between the ecology, evolution and biology of marine Synechococcus.
Prochlorococcus and Synechococcus are major prokaryotic primary producers in the oligotrophic oceans that may be affected by the climate-related increases in nitrogen fixation and subsequent phosphorus (P) limitation in some parts of the oceans. Evidence that Prochlorococcus populations in the North Pacific subtropical gyre (NPSG) have increased over the past decades, possibly due to having a competitive advantage under conditions of P limitation, suggests aspects of their P physiology that are important for dictating their in situ success. Here, we compared the physiology of P acquisition and response to P stress (indicated by alkaline phosphatase activity, APA) among isolates of Prochlorococcus and Synechococcus representing different genotypic clades within the marine picophytoplankton lineage (sensu Urbach et al. 1998: J Mol Evol 46:188-201). The 2 Synechococcus isolates examined (WH 8102 and WH 7803) can utilize a wide variety of organic P sources. Of the 3 Prochlorococcus isolates examined, only the HLI genotype, MED4, is capable of growth on a variety of organic P sources. Under conditions of P starvation the 2 Synechococcus strains and Prochlorococcus MED4 exhibit significant increases in APA, above their measurable constitutive activities. The genomes of the Synechococcus strains and Prochlorococcus MED4 indicate the presence of many P-uptake and -regulatory genes required under conditions of P stress, including the phoA gene that encodes for an alkaline phosphatase enzyme. The other isolates of Prochlorococcus, HLII MIT 9312 and LLIV MIT 9313, have distinctly different P-stress responses. MIT 9312, which contains the same P-uptake and -regulatory genes as MED4, except for psip1 and ptrA, has no constitutive APA, but does exhibit measurable, albeit very low, activity when P starved. MIT 9313, which lacks phoA and a functional phosphate-sensing histidine kinase gene, phoR, exhibits low constitutive activity that decreases when the cells become P-starved. These results show variability in P utilization and in P-stress response between the 2 genera of marine unicellular cyanobacteria, and marked differences among Prochlorococcus genotypes, implying that only certain eco/genotypes of these marine cyanobacteria will have an ecological advantage under conditions of P limitation in the oceans. This further points to the critical need to continue developing genotypic-or cell-specific tools to assess the response of the picophytoplankton community to large-scale changes in nutrient conditions in the oceans.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
10624 S. Eastern Ave., Ste. A-614
Henderson, NV 89052, USA
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.