Genomic mosaicism underlies the adaptation of marine <i>Synechococcus</i> ecotypes to distinct oceanic iron niches

Ahlgren, Nathan A.; Belisle, B. Shafer; Lee, Michael D.

doi:10.1111/1462-2920.14893

Cited by 31 publications

(66 citation statements)

References 88 publications

(129 reference statements)

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“…We could advocate achieving this via comparative genomics, but this usually necessitates hundreds to thousands of closely related genomes (for review see Read and Massey, 2014;Chen and Shapiro, 2015), as well as a refined phenotypic characterization of the sequenced strains. Alternatively, one could search in situ data for genes or substitutions related to a particular niche or environmental parameter (see e.g., Kent et al, 2016;Grébert et al, 2018;Ahlgren et al, 2019;Garcia et al, 2020). Given the wealth of marine metagenomes that are becoming available for a large variety of environmental niches, such an approach should be particularly powerful to unveil niche adaptation processes in the forthcoming years.…”

Section: Resultsmentioning

confidence: 99%

Evolutionary Mechanisms of Long-Term Genome Diversification Associated With Niche Partitioning in Marine Picocyanobacteria

et al. 2020

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Doré et al. Genome Diversification in Marine Picocyanobacteria variants specific to cold thermotypes, notably involved in carotenoid biosynthesis and the oxidative stress response, revealing that long-term adaptation to thermal niches relies on amino acid substitutions rather than on gene content variation. Altogether, this study not only deciphers the respective roles of gene gains/losses and sequence variation but also uncovers numerous gene candidates likely involved in niche partitioning of two key members of the marine phytoplankton.

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Section: Resultsmentioning

confidence: 99%

Evolutionary Mechanisms of Long-Term Genome Diversification Associated With Niche Partitioning in Marine Picocyanobacteria

et al. 2020

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“…Heme, which can be used as an iron source by numerous heterotrophic bacteria (Hopkinson et al, 2008;Hogle et al, 2017), is also transported in this way. TBDTs are widely distributed in heterotrophic bacteria, but are not present in all cyanobacteria, although they are present in various ecotypes of the ecologically important Prochlorococcus (Malmstrom et al, 2013) and Synechococcus strains (Ahlgren et al, 2020). Despite their abundance in heterotrophic bacteria, siderophores do not appear to be widely produced by marine cyanobacteria (Hopkinson and Morel, 2009).…”

Section: Siderophore-mediated Iron Uptakementioning

confidence: 99%

Iron Uptake Mechanisms in Marine Phytoplankton

2020

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Oceanic phytoplankton species have highly efficient mechanisms of iron acquisition, as they can take up iron from environments in which it is present at subnanomolar concentrations. In eukaryotes, three main models were proposed for iron transport into the cells by first studying the kinetics of iron uptake in different algal species and then, more recently, by using modern biological techniques on the model diatom Phaeodactylum tricornutum. In the first model, the rate of uptake is dependent on the concentration of unchelated Fe species, and is thus limited thermodynamically. Iron is transported by endocytosis after carbonate-dependent binding of Fe(III)' (inorganic soluble ferric species) to phytotransferrin at the cell surface. In this strategy the cells are able to take up iron from very low iron concentration. In an alternative model, kinetically limited for iron acquisition, the extracellular reduction of all iron species (including Fe') is a prerequisite for iron acquisition. This strategy allows the cells to take up iron from a great variety of ferric species. In a third model, hydroxamate siderophores can be transported by endocytosis (dependent on ISIP1) after binding to the FBP1 protein, and iron is released from the siderophores by FRE2-dependent reduction. In prokaryotes, one mechanism of iron uptake is based on the use of siderophores excreted by the cells. Iron-loaded siderophores are transported across the cell outer membrane via a TonB-dependent transporter (TBDT), and are then transported into the cells by an ABC transporter. Open ocean cyanobacteria do not excrete siderophores but can probably use siderophores produced by other organisms. In an alternative model, inorganic ferric species are transported through the outer membrane by TBDT or by porins, and are taken up by the ABC transporter system FutABC. Alternatively, ferric iron of the periplasmic space can be reduced by the alternative respiratory terminal oxidase (ARTO) and the ferrous ions can be transported by divalent metal transporters (FeoB or ZIP). After reoxidation, iron can be taken up by the high-affinity permease Ftr1.

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“…2B) and English Channel (library A) were exclusively composed of the cold-adapted clade I, mostly sub-clade Ib. Samples from the northeastern Atlantic Ocean were co-dominated by CRD1 and either clade I (libraries G1 and G2) or the environmental clades EnvA and EnvB (library E; EnvB is sometimes called CRD2; (Ahlgren et al 2019). Synechococcus populations from the western Mediterranean Sea were largely dominated by clade III (exclusively of sub-clade IIIa) at the coastal 'Point B' station located at the entrance of the Bay of Villefranche-sur-Mer (https://www.somlit.fr/villefranche/; library F), while they essentially consisted of clade I (mostly sub-clade Ib) at station A of the BOUM cruise (library I2; Moutin et al 2012) and at the long-term monitoring station BOUSSOLE located in the Gulf of Lions (library I1; Antoine et al 2008).…”

Section: Targeted Metagenomics Unveils Pbs Rod Regions From Field Populationsmentioning

confidence: 99%

Diversity and evolution of pigment types and the phycobilisome rod gene region of marine Synechococcus cyanobacteria

Grébert

Garczarek

Daubin³

et al. 2021

Preprint

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Synechococcus picocyanobacteria are ubiquitous and abundant photosynthetic organisms in the marine environment and contribute for an estimated 16% of the ocean net primary productivity. Their light-harvesting complexes, called phycobilisomes (PBS), are composed of a conserved allophycocyanin core from which radiates six to eight rods with variable phycobiliprotein and chromophore content. This variability allows Synechococcus to optimally exploit the wide variety of spectral niches existing in marine ecosystems. Seven distinct pigment types or subtypes have been identified so far in this taxon, based on the phycobiliprotein composition and/or the proportion of the different chromophores in PBS rods. Most genes involved in their biosynthesis and regulation are located in a dedicated genomic region called the PBS rod region. Here, we examined the variability of gene sequences and organization of this genomic region in a large set of sequenced isolates and natural populations of Synechococcus representative of all known pigment types. All regions start with a tRNA-PheGAA and some possess mobile elements including tyrosine recombinases, suggesting that their genomic plasticity relies on a tycheposon-like mechanism. Comparison of the phylogenies obtained for PBS and core genes revealed that the evolutionary history of PBS rod genes differs from the rest of the genome and is characterized by the co-existence of different alleles and frequent allelic exchange. We propose a scenario for the evolution of the different pigment types and highlight the importance of population-scale mechanisms in maintaining a wide diversity of pigment types in different Synechococcus lineages despite multiple speciation events.

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Genomic mosaicism underlies the adaptation of marine Synechococcus ecotypes to distinct oceanic iron niches

Cited by 31 publications

References 88 publications

Evolutionary Mechanisms of Long-Term Genome Diversification Associated With Niche Partitioning in Marine Picocyanobacteria

Evolutionary Mechanisms of Long-Term Genome Diversification Associated With Niche Partitioning in Marine Picocyanobacteria

Iron Uptake Mechanisms in Marine Phytoplankton

Diversity and evolution of pigment types and the phycobilisome rod gene region of marine Synechococcus cyanobacteria

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