Single-Cell Genomics Reveals Hundreds of Coexisting Subpopulations in Wild<i>Prochlorococcus</i>

Kashtan, Nadav; Roggensack, Sara E.; Rodrigue, Sébastien; Thompson, Jessie W.; Biller, Steven J.; Coe, Allison; Ding, Huiming; Marttinen, Pekka; Malmstrom, Rex R.; Stocker, Roman; Follows, Michael J.; Stepanauskas, Ramunas; Chisholm, Sallie W.

doi:10.1126/science.1248575

Cited by 494 publications

(634 citation statements)

References 86 publications

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“…In support of a primarily vertically driven evolutionary history, the gene content of 12 Prochlorococcus strains is largely congruent with a molecular phylogeny based on the core genes, suggesting a strong role of phylogenetic descent (Kettler et al, 2007). In addition, core gene alleles share evolutionary history with distinct sets of flexible genes in specific field populations of Prochlorococcus (Kashtan et al, 2014). Populations with these core gene alleles can change in abundance depending on environmental conditions owing to differential fitness of the allele or the associated flexible genes.…”

Section: Discussionmentioning

confidence: 69%

“…In our analysis, phylogeny and gene content is not perfectly correlated. This may be because of sampling error but can also be due to fine-scale diversity existing within the defined clades or due to particular sets of genes that vary independent of taxonomy (Kashtan et al, 2014;Pittera et al, 2014;see below). Divergent genes can be associated with variables that are not measured, such as trace metals, vitamins or ocean mixing.…”

Section: Discussionmentioning

confidence: 99%

“…Vertical descent, specifically the transfer of genes through cellular division, and horizontal gene transfer, encompassing the several mechanisms of moving genes between organisms without division, are two ways that genes can arrive in an organism. Based on a 'genomic backbones' concept (Kashtan et al, 2014), where a stable niche partitioning of sub-populations of Prochlorococcus is proposed, it should follow that phylogeny will largely correspond to the biogeography of the overall gene content. However, the genomic presence of many genes is highly variable as gene gain or loss may be a driving force in the evolution of Prochlorococcus (Kettler et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

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Global biogeography of Prochlorococcus genome diversity in the surface ocean

et al. 2016

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Prochlorococcus, the smallest known photosynthetic bacterium, is abundant in the ocean's surface layer despite large variation in environmental conditions. There are several genetically divergent lineages within Prochlorococcus and superimposed on this phylogenetic diversity is extensive gene gain and loss. The environmental role in shaping the global ocean distribution of genome diversity in Prochlorococcus is largely unknown, particularly in a framework that considers the vertical and lateral mechanisms of evolution. Here we show that Prochlorococcus field populations from a global circumnavigation harbor extensive genome diversity across the surface ocean, but this diversity is not randomly distributed. We observed a significant correspondence between phylogenetic and gene content diversity, including regional differences in both phylogenetic composition and gene content that were related to environmental factors. Several gene families were strongly associated with specific regions and environmental factors, including the identification of a set of genes related to lower nutrient and temperature regions. Metagenomic assemblies of natural Prochlorococcus genomes reinforced this association by providing linkage of genes across genomic backbones. Overall, our results show that the phylogeography in Prochlorococcus taxonomy is echoed in its genome content. Thus environmental variation shapes the functional capabilities and associated ecosystem role of the globally abundant Prochlorococcus.

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Section: Discussionmentioning

confidence: 69%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Global biogeography of Prochlorococcus genome diversity in the surface ocean

et al. 2016

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“…This similarity manifested itself not only in the gene order and chromosomal location, but also the phylogeny of the nitrate assimilation genes (Figures 3-5), placing the nitrate assimilation gene cluster in a genomic region that is syntenic with other HLII genomes and adjacent to a known genomic island (ISL3) in this clade (Figure 4). Furthermore, a partial genome from a Prochlorococcus single cell belonging to the HLII clade (B241-528J8; Genbank JFLE01000089.1) (Kashtan et al, 2014) also possesses a nitrate assimilation gene cluster in the same location and in the same order. The striking similarity between the nitrate assimilation gene clusters of these individual Prochlorococcus and the GOS consensus indicates that the order and location of nitrate assimilation genes are stable within HLII genomes.…”

Section: Resultsmentioning

confidence: 99%

Physiology and evolution of nitrate acquisition in Prochlorococcus

et al. 2014

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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 B17% 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.

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“…The existence of hypervariable genomic regions (or islands) (Palenik et al ., 2003; Coleman et al ., 2006; Dufresne et al ., 2008) has been linked with the importance of these regions in environmental adaptation (both biotic and abiotic) in both genera (Avrani et al ., 2011; Stuart et al ., 2013). Furthermore, closely related coexisting Prochlorococcus subpopulations according to their intergenic transcribed spacer showed a much higher divergence in terms of their genomic‐encoded auxilliary functions as a matter of avoiding competition and niche partitioning (Kashtan et al ., 2014). Hence, the existing diversity of functions encoded by this group of photosynthetic organisms is somewhat far from being understood.…”

Section: Introductionmentioning

confidence: 99%

Functional distinctness in the exoproteomes of marine Synechococcus

Christie-Oleza

Armengaud

Guérin

et al. 2015

Environmental Microbiology

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SummaryThe exported protein fraction of an organism may reflect its life strategy and, ultimately, the way it is perceived by the outside world. Bioinformatic prediction of the exported pan‐proteome of P rochlorococcus and S ynechococcus lineages demonstrated that (i) this fraction of the encoded proteome had a much higher incidence of lineage‐specific proteins than the cytosolic fraction (57% and 73% homologue incidence respectively) and (ii) exported proteins are largely uncharacterized to date (54%) compared with proteins from the cytosolic fraction (35%). This suggests that the genomic and functional diversity of these organisms lies largely in the diverse pool of novel functions these organisms export to/through their membranes playing a key role in community diversification, e.g. for niche partitioning or evading predation. Experimental exoproteome analysis of marine S ynechococcus showed transport systems for inorganic nutrients, an interesting array of strain‐specific exoproteins involved in mutualistic or hostile interactions (i.e. hemolysins, pilins, adhesins), and exoenzymes with a potential mixotrophic goal (i.e. exoproteases and chitinases). We also show how these organisms can remodel their exoproteome, i.e. by increasing the repertoire of interaction proteins when grown in the presence of a heterotroph or decrease exposure to prey when grown in the dark. Finally, our data indicate that heterotrophic bacteria can feed on the exoproteome of S ynechococcus.

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Single-Cell Genomics Reveals Hundreds of Coexisting Subpopulations in WildProchlorococcus

Cited by 494 publications

References 86 publications

Global biogeography of Prochlorococcus genome diversity in the surface ocean

Global biogeography of Prochlorococcus genome diversity in the surface ocean

Physiology and evolution of nitrate acquisition in Prochlorococcus

Functional distinctness in the exoproteomes of marine Synechococcus

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