A Diatom Ferritin Optimized for Iron Oxidation but Not Iron Storage

Pfaffen, Stephanie; Bradley, Justin M.; Abdulqadir, Raz; Firme, Marlo; Moore, Geoffrey R.; Brun, Nick E. Le; Murphy, M.E.P.

doi:10.1074/jbc.m115.669713

Cited by 32 publications

(46 citation statements)

References 28 publications

(64 reference statements)

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“…NH16 both exhibit increased FTN expression under high iron conditions while T. rotula ( FTN 2) and A. coffeaeformis ( FTN 1) increased FTN expression under iron limiting conditions, yet all of these ferritins group within the FTN‐I clade. Furthermore, as noted previously, a single residue substitution could substantially change ferritin functionality, suggesting that ferritin sequence homology alone may be an inaccurate indicator of ferritin function (Pfaffen et al ).…”

Section: Discussionmentioning

confidence: 77%

“…The coastal marine diatom P. multiseries has an isoform of ferritin that seems to be optimized for rapid iron sequestration and release. This diatom contains a glutamic acid residue in a region of the ferroxidase center (Glu130) that complexes and stabilizes Fe(III) following oxidation of Fe(II) (Pfaffen et al ). This complexation reduces the rate of Fe(III) transfer to the protein core and subsequent storage as ferrihydrate.…”

Section: Discussionmentioning

confidence: 99%

“…This complexation reduces the rate of Fe(III) transfer to the protein core and subsequent storage as ferrihydrate. By contrast, substitution of Glu130 with a non‐Fe coordinating residue allows for quicker Fe(III) mineralization and storage (Pfaffen et al ). Interestingly, aside from P. granii , none of the other ferritin‐containing diatoms examined in our study contain a glutamic acid or other iron‐binding amino acid at site 130, but instead have an alanine, serine, or glycine (Supporting Information Fig.…”

Section: Discussionmentioning

confidence: 99%

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Iron storage capacities and associated ferritin gene expression among marine diatoms

Cohen

Mann

Stemple

et al. 2018

Limnology & Oceanography

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In large regions of the ocean, low iron availability regulates diatom growth and species composition. Diatom species often vary in their physiological response to iron enrichment, with natural and artificial iron additions in iron‐limited regions of the ocean resulting in large blooms of primarily pennate diatoms. The ability of pennate diatoms to proliferate following pulse iron additions has been partly attributed to their ability to acquire and store excess intracellular iron in the iron storage protein ferritin. Recent transcriptome sequencing of diatoms indicate that some centric diatoms also possess ferritin. Using a combination of physiological and molecular techniques, we examined the iron storage capacities and associated ferritin gene expression in phylogenetically diverse centric and pennate diatoms grown under high and low iron concentrations. There were no systematic differences among ferritin‐containing and non‐containing diatom lineages in their ability to store iron in excess of that needed to support maximum growth rates. An exception, however, was the ferritin‐containing pennate diatom Pseudo‐nitzschia granii, native to iron‐limited waters of the Northeast Pacific Ocean. This species exhibited an exceptionally large luxury iron storage capacity and increased ferritin gene expression at high iron concentrations, supporting a role in long‐term iron storage. By contrast, two other diatoms species that exhibited minimal iron storage capacities contained two distinct ferritin genes where one ferritin gene increased in expression under iron limitation while the second showed no variation with cellular iron status. We conclude that ferritin may serve multiple functional roles that are independent of diatom phylogeny.

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Section: Discussionmentioning

confidence: 77%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Iron storage capacities and associated ferritin gene expression among marine diatoms

Cohen

Mann

Stemple

et al. 2018

Limnology & Oceanography

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“…Ferritin is another important protein of iron metabolism that was relatively recently identified in diatoms (Marchetti et al, 2009) and in other phytoplankton functional groups (Botebol et al, 2015). Although it appears to be involved in long-term iron storage in Pseudo-nitzschia (Marchetti et al, 2009), other studies have suggested that its principal role could be in cellular iron buffering and temporal storage over shorter timescales such as during diurnal cycles (Botebol et al, 2015;Cohen et al, 2018;Pfaffen et al, 2015). Our analysis revealed no clear pattern in ferritin gene abundance or expression and estimated iron levels ( Figure S2), suggesting that iron storage may not be the main function of ferritin in most eukaryotic marine phytoplankton.…”

Section: Global Biogeochemical Cyclesmentioning

confidence: 99%

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

Caputi

Carradec

Eveillard

et al. 2019

Global Biogeochemical Cycles

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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“…Ferritin was highly expressed post-upwelling, possibly providing a method of storing the essential micronutrient iron (Marchetti et al, 2009). As iron availability in the California upwelling regime can be sporadic and potentially growth limiting, ferritin may provide an advantage to Pseudo-nitzschia by concentrating iron for longer-term storage (Bruland et al, 2001), although it may also be used for iron homeostasis (Pfaffen et al, 2015).…”

Section: Molecular Characterization Of the Nitrogen Assimilation Respmentioning

confidence: 99%

Divergent gene expression among phytoplankton taxa in response to upwelling

Lampe

Cohen

Ellis

et al. 2018

Environmental Microbiology

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Frequent blooms of phytoplankton occur in coastal upwelling zones creating hotspots of biological productivity in the ocean. As cold, nutrient-rich water is brought up to sunlit layers from depth, phytoplankton are also transported upwards to seed surface blooms that are often dominated by diatoms. The physiological response of phytoplankton to this process, commonly referred to as shift-up, is characterized by increases in nitrate assimilation and rapid growth rates. To examine the molecular underpinnings behind this phenomenon, metatranscriptomics was applied to a simulated upwelling experiment using natural phytoplankton communities from the California Upwelling Zone. An increase in diatom growth following 5 days of incubation was attributed to the genera Chaetoceros and Pseudo-nitzschia. Here, we show that certain bloom-forming diatoms exhibit a distinct transcriptional response that coordinates shift-up where diatoms exhibited the greatest transcriptional change following upwelling; however, comparison of co-expressed genes exposed overrepresentation of distinct sets within each of the dominant phytoplankton groups. The analysis revealed that diatoms frontload genes involved in nitrogen assimilation likely in order to outcompete other groups for available nitrogen during upwelling events. We speculate that the evolutionary success of diatoms may be due, in part, to this proactive response to frequently encountered changes in their environment.

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A Diatom Ferritin Optimized for Iron Oxidation but Not Iron Storage

Cited by 32 publications

References 28 publications

Iron storage capacities and associated ferritin gene expression among marine diatoms

Iron storage capacities and associated ferritin gene expression among marine diatoms

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

Divergent gene expression among phytoplankton taxa in response to upwelling

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