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Title: Reduction-dependent siderophore assimilation in a model pennate diatom

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
ORCiD logo [1];  [1];  [2];  [2];  [3]; ORCiD logo [1]
  1. Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093,, Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA 92037,
  2. Biology Centre, Institute of Parasitology, Academy of Sciences of the Czech Republic, 370 05 České Budějovice, Czech Republic,, Faculty of Science, University of South Bohemia, 370 05 České Budějovice, Czech Republic
  3. Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093,

Iron uptake by diatoms is a biochemical process with global biogeochemical implications. In large regions of the surface ocean diatoms are both responsible for the majority of primary production and frequently experiencing iron limitation of growth. The strategies used by these phytoplankton to extract iron from seawater constrain carbon flux into higher trophic levels and sequestration into sediments. In this study we use reverse genetic techniques to target putative iron-acquisition genes in the model pennate diatom Phaeodactylum tricornutum. We describe components of a reduction-dependent siderophore acquisition pathway that relies on a bacterial-derived receptor protein and provides a viable alternative to inorganic iron uptake under certain conditions. This form of iron uptake entails a close association between diatoms and siderophore-producing organisms during low-iron conditions. Homologs of these proteins are found distributed across diatom lineages, suggesting the significance of siderophore utilization by diatoms in the marine environment. Evaluation of specific proteins enables us to confirm independent iron-acquisition pathways in diatoms and characterize their preferred substrates. These findings refine our mechanistic understanding of the multiple iron-uptake systems used by diatoms and help us better predict the influence of iron speciation on taxa-specific iron bioavailability.

Research Organization:
J. Craig Venter Institute, Inc., Rockville, MD (United States)
Sponsoring Organization:
USDOE Office of Science (SC); National Science Foundation (NSF); Gordon and Betty Moore Foundation; Czech Science Foundation; European Regional Development Fund/European Social Fund
Grant/Contract Number:
SC0018344; NSF-OCE-1756884; NSF-OCE-1756860; NSF-MCB-1818390; GBMF3828; GBMF5006; 18-13458S; CZ.02.1.01/0.0/0.0/16_019/0000759
OSTI ID:
1573107
Alternate ID(s):
OSTI ID: 1625043
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 116 Journal Issue: 47; ISSN 0027-8424
Publisher:
Proceedings of the National Academy of SciencesCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 34 works
Citation information provided by
Web of Science

References (83)

Iron-limited diatom growth and Si:N uptake ratios in a coastal upwelling regime journal June 1998
Coastal iron and nitrate distributions during the spring and summer upwelling season in the central California Current upwelling regime journal September 2013
Siderophores and the Dissolution of Iron-Bearing Minerals in Marine Systems journal January 2005
SEQUENCE ANALYSIS AND TRANSCRIPTIONAL REGULATION OF IRON ACQUISITION GENES IN TWO MARINE DIATOMS 1 journal August 2007
Expression of the retrotransposons Surcouf and Blackbeard in the marine diatom Phaeodactylum tricornutum under thermal stress journal November 2015
Lipoproteins of gram-positive bacteria. journal March 1995
Identification of a ferrireductase required for efficient transferrin-dependent iron uptake in erythroid cells journal October 2005
fhuC and fhuD genes for iron (III)-ferrichrome transport into Escherichia coli K-12. journal August 1987
Structural biology of bacterial iron uptake journal September 2008
Comparative metatranscriptomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability journal January 2012
Siderophore uptake and use by the yeast Saccharomyces cerevisiae journal February 2001
Iron in north-east Pacific waters journal October 1982
Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation journal January 2012
Continental-shelf sediment as a primary source of iron for coastal phytoplankton journal April 1999
The Role of the FRE Family of Plasma Membrane Reductases in the Uptake of Siderophore-Iron in Saccharomyces cerevisiae journal December 2000
Respiratory burst oxidases: the engines of ROS signaling journal December 2011
Photophysiological Expressions of Iron Stress in Phytoplankton journal January 2013
Photolysis of iron-siderophore chelates promotes bacterial-algal mutualism journal September 2009
Carbonate-sensitive phytotransferrin controls high-affinity iron uptake in diatoms journal March 2018
The Phaeodactylum genome reveals the evolutionary history of diatom genomes journal October 2008
Distinct pools of dissolved iron-binding ligands in the surface and benthic boundary layer of the California Current journal April 2014
Iron(II) variability in the northeast subarctic Pacific Ocean journal December 2015
The GEOTRACES Intermediate Data Product 2014 journal December 2015
Preparation and Chemistry of the Artificial Algal Culture Medium Aquil journal January 1989
Complexation of iron(III) by natural organic ligands in the Central North Pacific as determined by a new competitive ligand equilibration/adsorptive cathodic stripping voltammetric method journal August 1995
The redox hypothesis in siderophore-mediated iron uptake journal April 2009
Microbial iron transport via a siderophore shuttle: A membrane ion transport paradigm journal September 2000
Interspecies modulation of bacterial development through iron competition and siderophore piracy: Xenosiderophores alter development in actinomycetes journal September 2012
Ferrichrome induces endosome to plasma membrane cycling of the ferrichrome transporter, Arn1p, in Saccharomyces cerevisiae journal July 2002
Evolution of the Ferric Reductase Domain (FRD) Superfamily: Modularity, Functional Diversification, and Signature Motifs journal March 2013
Iron bioavailability to phytoplankton: an empirical approach journal October 2014
Siderophore-Based Iron Acquisition and Pathogen Control journal September 2007
Endocytosis-mediated siderophore uptake as a strategy for Fe acquisition in diatoms journal May 2018
CRISPR-Cas systems for editing, regulating and targeting genomes journal March 2014
Iron acquisition in the marine actinomycete genus Salinispora is controlled by the desferrioxamine family of siderophores journal August 2012
Upper ocean ecosystem dynamics and iron cycling in a global three-dimensional model: GLOBAL ECOSYSTEM-BIOGEOCHEMICAL MODEL journal December 2004
High Frequency of Horizontal Gene Transfer in the Oceans journal September 2010
Transcriptomic and proteomic responses of the oceanic diatom Pseudo-nitzschia granii to iron limitation journal August 2018
The central California Current transition zone: A broad region exhibiting evidence for iron limitation journal January 2014
New Light on the Scaling of Metabolic rate with the size of Algae journal February 2002
Acquisition of iron bound to strong organic complexes, with different Fe binding groups and photochemical reactivities, by plankton communities in Fe-limited subantarctic waters: Fe UPTAKE FROM MODEL AND IN SITU LIGANDS BY PLANKTON journal October 2005
Patterns of iron and siderophore distributions across the California Current System: Siderophore distributions across the CCS journal November 2018
Dissolved iron and macronutrient distributions in the southern California Current System journal January 2011
Utilization of iron bound to strong organic ligands by plankton communities in the subarctic Pacific Ocean journal November 1999
Inactivation of Phaeodactylum tricornutum urease gene using transcription activator-like effector nuclease-based targeted mutagenesis journal October 2014
An Iron-Regulated Ferric Reductase Associated with the Absorption of Dietary Iron journal February 2001
REDUCTION AND TRANSPORT OF ORGANICALLY BOUND IRON BY THALASSIOSIRA OCEANICA (BACILLARIOPHYCEAE) journal April 2001
Evidence for geochemical control of iron by humic substances in seawater journal March 2009
Daily to decadal variability of size-fractionated iron and iron-binding ligands at the Hawaii Ocean Time-series Station ALOHA journal December 2015
The Siderophore-Interacting Protein YqjH Acts as a Ferric Reductase in Different Iron Assimilation Pathways of Escherichia coli journal December 2011
Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation journal July 2008
Whole-genome expression profiling of the marine diatom Thalassiosira pseudonana identifies genes involved in silicon bioprocesses journal January 2008
Distinct Extracytoplasmic Siderophore Binding Proteins Recognize Ferrioxamines and Ferricoelichelin in Streptomyces coelicolor A3(2) journal September 2010
Membrane Affinity of the Amphiphilic Marinobactin Siderophores journal November 2002
Diversity and Evolutionary History of Iron Metabolism Genes in Diatoms journal June 2015
Specificity and mechanism of ferrioxamine-mediated iron transport in Streptomyces pilosus. journal January 1984
Kinetics of internalization and recycling of transferrin and the transferrin receptor in a human hepatoma cell line. Effect of lysosomotropic agents. journal August 1983
The ins and outs of algal metal transport journal September 2012
Ecology of uncultured Prochlorococcus clades revealed through single-cell genomics and biogeographic analysis journal August 2012
Self-Assembling Amphiphilic Siderophores from Marine Bacteria journal February 2000
Chemistry and biology of siderophores journal January 2010
A CRISPR/Cas9 system adapted for gene editing in marine algae journal April 2016
Eukaryotic Acquisition of a Bacterial Operon journal March 2019
Why microbes secrete molecules to modify their environment: the case of iron-chelating siderophores journal January 2019
The organic complexation of iron in the marine environment: a review journal January 2012
Genetic indicators of iron limitation in wild populations of Thalassiosira oceanica from the northeast Pacific Ocean journal October 2014
Synthesis of iron fertilization experiments: From the Iron Age in the Age of Enlightenment journal January 2005
Copper-dependent iron transport in coastal and oceanic diatoms journal July 2006
Iron(III)–siderophore coordination chemistry: Reactivity of marine siderophores journal February 2010
Marine amphiphilic siderophores: Marinobactin structure, uptake, and microbial partitioning journal November 2007
Ferrioxamines B and E as iron sources for the marine diatom Phaeodactylum tricornutum journal January 1995
Chloroplast Fe(III) chelate reductase activity is essential for seedling viability under iron limiting conditions journal July 2008
Designer diatom episomes delivered by bacterial conjugation journal April 2015
Role of root-induced changes in the rhizosphere for iron acquisition in higher plants journal January 1989
Characterization of iron-responsive promoters in the marine diatom Phaeodactylum tricornutum journal August 2014
Effect of pH, light, and temperature on Fe–EDTA chelation and Fe hydrolysis in seawater journal December 2003
Chemistry of Marine Ligands and Siderophores journal January 2009
Transcriptional Orchestration of the Global Cellular Response of a Model Pennate Diatom to Diel Light Cycling under Iron Limitation journal December 2016
Adaptive strategies by Southern Ocean phytoplankton to lessen iron limitation: Uptake of organically complexed iron and reduced cellular iron requirements journal September 2011
Identification of a natural desferrioxamine siderophore produced by a marine bacterium journal March 2001
Simultaneous determination of iron reduction and uptake by phytoplankton: Iron reduction and uptake determination journal May 2004
Potential impact of stress activated retrotransposons on genome evolution in a marine diatom journal January 2009
Siderophore-based microbial adaptations to iron scarcity across the eastern Pacific Ocean journal December 2016