Endocytosis-mediated siderophore uptake as a strategy for Fe acquisition in diatoms

Kazamia, Elena; Šuták, Robert; Paz‐Yepes, Javier; Dorrell, Richard G.; Vieira, Fabio Rocha Jimenez; Mach, Jan; Morrissey, Joe; Léon, Sébastien; Pelletier, Éric; Camadro, Jean‐Michel; Bowler, Chris; Lesuisse, Emmanuel

doi:10.1126/sciadv.aar4536

Cited by 103 publications

(177 citation statements)

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“…The abundance of proteorhodopsin and ferritin genes and mRNA in diatoms were generally also consistent with this hypothesis, with decreases in proteorhodopsin transcripts and increases in ferritin in Station TARA_123 with respect to Station TARA_122 (Figures c, d, and S7d). These patterns of known iron‐responsive genes provide strong support that iron bioavailability is an important driver of the phytoplankton blooms in the Marquesas Islands (supporting information S4, Groussman et al, ; Kazamia, et al, ; Lane & Morel, ; McQuaid et al, ; Whitney et al, ).…”

Section: Resultsmentioning

confidence: 69%

Community‐Level Responses to Iron Availability in Open Ocean Plankton Ecosystems

Caputi

Carradec

Eveillard

et al. 2019

Global Biogeochemical Cycles

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100

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Predicting responses of plankton to variations in essential nutrients is hampered by limited in situ measurements, a poor understanding of community composition, and the lack of reference gene catalogs for key taxa. Iron is a key driver of plankton dynamics and, therefore, of global biogeochemical cycles and climate. To assess the impact of iron availability on plankton communities, we explored the comprehensive bio‐oceanographic and bio‐omics data sets from Tara Oceans in the context of the iron products from two state‐of‐the‐art global scale biogeochemical models. We obtained novel information about adaptation and acclimation toward iron in a range of phytoplankton, including picocyanobacteria and diatoms, and identified whole subcommunities covarying with iron. Many of the observed global patterns were recapitulated in the Marquesas archipelago, where frequent plankton blooms are believed to be caused by natural iron fertilization, although they are not captured in large‐scale biogeochemical models. This work provides a proof of concept that integrative analyses, spanning from genes to ecosystems and viruses to zooplankton, can disentangle the complexity of plankton communities and can lead to more accurate formulations of resource bioavailability in biogeochemical models, thus improving our understanding of plankton resilience in a changing environment.

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Section: Resultsmentioning

confidence: 69%

Community‐Level Responses to Iron Availability in Open Ocean Plankton Ecosystems

Caputi

Carradec

Eveillard

et al. 2019

Global Biogeochemical Cycles

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100

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“…In some cases, both groups use homologous genes and mechanisms to achieve these adaptations: ferritin and altering the balance of ferredoxin and flavodoxin. At the same time, Synechococcus uses different genes and mechanisms: the prokaryotic transporter genes feoA/feoB , bacterioferritin and siderophore uptake genes that are generally absent in diatoms (Kazamia et al ., ). An abundance of Synechococcus genomes paired with detailed knowledge of ecotype biogeography has allowed for powerful comparisons across these closely‐related phytoplankton populations in ways not currently feasible for diatom species.…”

Section: Discussionmentioning

confidence: 97%

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

Ahlgren

Belisle

Lee

2019

Environmental Microbiology

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Summary Phytoplankton are limited by iron (Fe) in ~40% of the world's oceans including high‐nutrient low‐chlorophyll (HNLC) regions. While low‐Fe adaptation has been well‐studied in large eukaryotic diatoms, less is known for small, prokaryotic marine picocyanobacteria. This study reveals key physiological and genomic differences underlying Fe adaptation in marine picocyanobacteria. HNLC ecotype CRD1 strains have greater physiological tolerance to low Fe congruent with their expanded repertoire of Fe transporter, storage and regulatory genes compared to other ecotypes. From metagenomic analysis, genes encoding ferritin, flavodoxin, Fe transporters and siderophore uptake genes were more abundant in low‐Fe waters, mirroring paradigms of low‐Fe adaptation in diatoms. Distinct Fe‐related gene repertories of HNLC ecotypes CRD1 and CRD2 also highlight how coexisting ecotypes have evolved independent approaches to life in low‐Fe habitats. Synechococcus and Prochlorococcus HNLC ecotypes likewise exhibit independent, genome‐wide reductions of predicted Fe‐requiring genes. HNLC ecotype CRD1 interestingly was most similar to coastal ecotype I in Fe physiology and Fe‐related gene content, suggesting populations from these different biomes experience similar Fe‐selective conditions. This work supports an improved perspective that phytoplankton are shaped by more nuanced Fe niches in the oceans than previously implied from mostly binary comparisons of low‐ versus high‐Fe habitats and populations.

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“…Our observations suggest that heterotrophic prokaryotes favour the uptake of Fe bound to siderophores, which presents several advantages. First, once complexed by siderophores, Fe is hardly available for most phytoplankton (Lis et al, 2015), even though the idea that phytoplankton cannot directly use Fe-siderophore complexes has recently been challenged (Kazamia et al, 2018;McQuaid et al, 2018). Heterotrophic prokaryotes thereby avoid competition with phytoplankton for this scare resource.…”

Section: Discussionmentioning

confidence: 99%

Microbial iron metabolism as revealed by gene expression profiles in contrasted Southern Ocean regimes

Debeljak

Toulza

Beier

et al. 2019

Environmental Microbiology

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Summary Iron (Fe) is a limiting nutrient in large regions of the ocean, but the strategies of prokaryotes to cope with this micronutrient are poorly known. Using a gene‐specific approach from metatranscriptomics data, we investigated seven Fe‐related metabolic pathways in microbial communities from high nutrient low chlorophyll and naturally Fe‐fertilized waters in the Southern Ocean. We observed major differences in the contribution of prokaryotic groups at different taxonomic levels to transcripts encoding Fe‐uptake mechanisms, intracellular Fe storage and replacement and Fe‐related pathways in the tricarboxylic acid (TCA) cycle. The composition of the prokaryotic communities contributing to the transcripts of a given Fe‐related pathway was overall independent of the in situ Fe supply, indicating that microbial taxa utilize distinct Fe‐related metabolic processes. Only a few prokaryotic groups contributed to the transcripts of more than one Fe‐uptake mechanism, suggesting limited metabolic versatility. Taxa‐specific expression of individual genes varied among prokaryotic groups and was substantially higher for all inspected genes in Fe‐limited as compared to naturally fertilized waters, indicating the link between transcriptional state and Fe regime. Different metabolic strategies regarding low Fe concentrations in the Southern Ocean are discussed for two abundant prokaryotic groups, Pelagibacteraceae and Flavobacteriaceae .

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Endocytosis-mediated siderophore uptake as a strategy for Fe acquisition in diatoms

Abstract: We report a new strategy uncovered for iron acquisition in globally important unicellular photosynthetic organisms.

Cited by 103 publications

References 63 publications

Community‐Level Responses to Iron Availability in Open Ocean Plankton Ecosystems

Community‐Level Responses to Iron Availability in Open Ocean Plankton Ecosystems

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

Microbial iron metabolism as revealed by gene expression profiles in contrasted Southern Ocean regimes

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