Reduction-dependent siderophore assimilation in a model pennate diatom

. 2019 Nov 19 ; 116 (47) : 23609-23617. [epub] 20191104

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem, Research Support, U.S. Gov't, Non-P.H.S.

Perzistentní odkaz   https://www.medvik.cz/link/pmid31685631

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.

Zobrazit více v PubMed

Moore J. K., Doney S. C., Lindsay K., Upper ocean ecosystem dynamics and iron cycling in a global three-dimensional model. Global Biogeochem. Cycles 18, 1–21 (2004).

Behrenfeld M. J., Milligan A. J., Photophysiological expressions of iron stress in phytoplankton. Annu. Rev. Mar. Sci. 5, 217–246 (2013). PubMed

Raven J. A., Kübler J. E., New light on the scaling of metabolic rate with the size of algae. J. Phycol. 38, 11–16 (2002).

de Baar H. J. W., Synthesis of iron fertilization experiments: From the Iron Age in the Age of Enlightenment. J. Geophys. Res. 110, C09S16 (2005).

Hutchins D. A., Bruland K. W., Iron-limited diatom growth and Si:N uptake ratios in a coastal upwelling regime. Nature 393, 65–68 (1998).

McQuaid J. B., et al. , Carbonate-sensitive phytotransferrin controls high-affinity iron uptake in diatoms. Nature 555, 534–537 (2018). PubMed

Lis H., Shaked Y., Kranzler C., Keren N., Morel F. M. M., Iron bioavailability to phytoplankton: An empirical approach. ISME J. 9, 1003–1013 (2015). PubMed PMC

Gledhill M., Buck K. N., The organic complexation of iron in the marine environment: A review. Front. Microbiol. 3, 69 (2012). PubMed PMC

Laglera L. M., van den Berg C. M. G. G., Evidence for geochemical control of iron by humic substances in seawater. Limnol. Oceanogr. 54, 610–619 (2009).

Rue E. L., Bruland K. W., 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. Mar. Chem. 50, 117–138 (1995).

Mawji E., et al. , The GEOTRACES intermediate data product 2014. Mar. Chem. 177, 1–8 (2015).

Fitzsimmons J. N., et al. , Daily to decadal variability of size-fractionated iron and iron-binding ligands at the Hawaii Ocean Time-series Station ALOHA. Geochim. Cosmochim. Acta 171, 303–324 (2015).

Butler A., Theisen R. M., Iron(III)-siderophore coordination chemistry: Reactivity of marine siderophores. Coord. Chem. Rev. 254, 288–296 (2010). PubMed PMC

Hider R. C., Kong X., Chemistry and biology of siderophores. Nat. Prod. Rep. 27, 637–657 (2010). PubMed

Vraspir J. M., Butler A., Chemistry of marine ligands and siderophores. Annu. Rev. Mar. Sci. 1, 43–63 (2009). PubMed PMC

Martinez J. S., et al. , Self-assembling amphiphilic siderophores from marine bacteria. Science 287, 1245–1247 (2000). PubMed

Xu G., Martinez J. S., Groves J. T., Butler A., Membrane affinity of the amphiphilic marinobactin siderophores. J. Am. Chem. Soc. 124, 13408–13415 (2002). PubMed

Braun V., Braun M., Iron transport and signaling in Escherichia coli. FEBS Lett. 529, 78–85 (2002). PubMed

Maldonado M. T., Price N. M., Utilization of Fe bound to strong organic ligands by phytoplankton communities in the subarctic Pacific Ocean. Deep Sea Res II 46, 2447–2473 (1999).

Horstmann U., Soria-Dengg S., Ferrioxamines B and E as iron sources for the marine diatom Phaeodactylum tricornutum. Mar. Ecol. Prog. Ser. 127, 269–277 (1995).

Maldonado M. T., Strzepek R. F., Sander S., Boyd P. W., Acquisition of iron bound to strong organic complexes, with different Fe binding groups and photochemical reactivities, by plankton communities in Fe-limited subantarctic waters. Global Biogeochem. Cycles 19, GB4S23 (2005).

Martinez J. S., Haygood M. G., Butler A., Identification of a natural desferrioxamine siderophore produced by a marine bacterium. Limnol. Oceanogr. 46, 420–424 (2001).

Boiteau R. M., et al. , Siderophore-based microbial adaptations to iron scarcity across the eastern Pacific Ocean. Proc. Natl. Acad. Sci. U.S.A. 113, 14237–14242 (2016). PubMed PMC

Boiteau R. M., et al. , Patterns of iron and siderophore distributions across the California current system. Limnol. Oceanogr. 64, 376–389 (2018).

Krewulak K. D., Vogel H. J., Structural biology of bacterial iron uptake. Biochim. Biophys. Acta 1778, 1781–1804 (2008). PubMed

Sutcliffe I. C., Russell R. R., Lipoproteins of gram-positive bacteria. J. Bacteriol. 177, 1123–1128 (1995). PubMed PMC

Miethke M., Marahiel M. A., Siderophore-based iron acquisition and pathogen control. Microbiol. Mol. Biol. Rev. 71, 413–451 (2007). PubMed PMC

Blaby-Haas C. E., Merchant S. S., The ins and outs of algal metal transport. Biochim. Biophys. Acta 1823, 1531–1552 (2012). PubMed PMC

Lesuisse E., Labbe P., Reductive and non-reductive mechanisms of iron assimilation by the yeast Saccharomyces cerevisiae. J. Gen. Microbiol. 135, 257–263 (1989). PubMed

Zhang X., Krause K. H., Xenarios I., Soldati T., Boeckmann B., Evolution of the ferric reductase domain (FRD) superfamily: Modularity, functional diversification, and signature motifs. PLoS One 8, e58126 (2013). PubMed PMC

Suzuki N., et al. , Respiratory burst oxidases: The engines of ROS signaling. Curr. Opin. Plant Biol. 14, 691–699 (2011). PubMed

Jeong J., et al. , Chloroplast Fe(III) chelate reductase activity is essential for seedling viability under iron limiting conditions. Proc. Natl. Acad. Sci. U.S.A. 105, 10619–10624 (2008). PubMed PMC

Singh A., Kaur N., Kosman D. J., The metalloreductase Fre6p in Fe-efflux from the yeast vacuole. J. Biol. Chem. 282, 28619–28626 (2007). PubMed

Maldonado M. T., Price N. M., Reduction and transport of organically bound iron by Thalassiosira oceanica (Bacillariophyceae). J. Phycol. 37, 298–309 (2001).

Maldonado M. T., et al. , Copper-dependent iron transport in coastal and oceanic diatoms. Limnol. Oceanogr. 51, 1729–1743 (2006).

Kazamia E., et al. , Endocytosis-mediated siderophore uptake as a strategy for Fe acquisition in diatoms. Sci. Adv. 4, eaar4536 (2018). PubMed PMC

Kustka A. B., Allen A. E., Morel F. M. M., Sequence analysis and transcriptional regulation of iron acquisition genes in two marine diatoms. J. Phycol. 43, 715–729 (2007).

Allen A. E., et al. , Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. Proc. Natl. Acad. Sci. U.S.A. 105, 10438–10443 (2008). PubMed PMC

Smith S. R., et al. , Transcriptional orchestration of the global cellular response of a model pennate diatom to diel light cycling under iron limitation. PLoS Genet. 12, e1006490 (2016). PubMed PMC

Lommer M., et al. , Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation. Genome Biol. 13, R66 (2012). PubMed PMC

Cohen N. R., et al. , Transcriptomic and proteomic responses of the oceanic diatom Pseudo-nitzschia granii to iron limitation. Environ. Microbiol. 20, 3109–3126 (2018). PubMed

Mock T., et al. , Whole-genome expression profiling of the marine diatom Thalassiosira pseudonana identifies genes involved in silicon bioprocesses. Proc. Natl. Acad. Sci. U.S.A. 105, 1579–1584 (2008). PubMed PMC

Marchetti A., et al. , Comparative metatranscriptomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability. Proc. Natl. Acad. Sci. U.S.A. 109, E317–E325 (2012). PubMed PMC

Chappell P. D., et al. , Genetic indicators of iron limitation in wild populations of Thalassiosira oceanica from the northeast Pacific Ocean. ISME J. 9, 592–602 (2015). PubMed PMC

Groussman R. D., Parker M. S., Armbrust E. V., Diversity and evolutionary history of iron metabolism genes in diatoms. PLoS One 10, e0129081 (2015). PubMed PMC

Bowler C., et al. , The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456, 239–244 (2008). PubMed

Nymark M., Sharma A. K., Sparstad T., Bones A. M., Winge P., A CRISPR/Cas9 system adapted for gene editing in marine algae. Sci. Rep. 6, 24951 (2016). PubMed PMC

Karas B. J., et al. , Designer diatom episomes delivered by bacterial conjugation. Nat. Commun. 6, 6925 (2015). PubMed PMC

Yun C. W., Bauler M., Moore R. E., Klebba P. E., Philpott C. C., The role of the FRE family of plasma membrane reductases in the uptake of siderophore-iron in Saccharomyces cerevisiae. J. Biol. Chem. 276, 10218–10223 (2001). PubMed

Coulton J. W., Mason P., Allatt D. D., fhuC and fhuD genes for iron (III)-ferrichrome transport into Escherichia coli K-12. J. Bacteriol. 169, 3844–3849 (1987). PubMed PMC

Roberts A. A., Schultz A. W., Kersten R. D., Dorrestein P. C., Moore B. S., Iron acquisition in the marine actinomycete genus Salinispora is controlled by the desferrioxamine family of siderophores. FEMS Microbiol. Lett. 335, 95–103 (2012). PubMed PMC

Yoshinaga R., Niwa-Kubota M., Matsui H., Matsuda Y., Characterization of iron-responsive promoters in the marine diatom Phaeodactylum tricornutum. Mar. Genomics 16, 55–62 (2014). PubMed

Sander J. D., Joung J. K., CRISPR-Cas systems for editing, regulating and targeting genomes. Nat. Biotechnol. 32, 347–355 (2014). PubMed PMC

Price N. M., et al. , Preparation and chemistry of the artificial algal culture medium Aquil. Biol. Oceanogr. 6, 443–461 (1989).

Sunda W., Huntsman S., Effect of pH, light, and temperature on Fe–EDTA chelation and Fe hydrolysis in seawater. Mar. Chem. 84, 35–47 (2003).

Philpott C. C., Protchenko O., Response to iron deprivation in Saccharomyces cerevisiae. Eukaryot. Cell 7, 20–27 (2008). PubMed PMC

Johnson K., Chavez F., Friederich G., Continental-shelf sediment as a primary source of iron for coastal phytoplankton. Nature 398, 697–700 (1999).

Biller D. V., Coale T. H., Till R. C., Smith G. J., Bruland K. W., Coastal iron and nitrate distributions during the spring and summer upwelling season in the central California current upwelling regime. Cont. Shelf Res. 66, 58–72 (2013).

Eckhardt U., Buckhout T. J., Iron assimilation in Chlamydomonas reinhardtii involves ferric reduction and is similar to strategy I higher plants. J. Exp. Bot. 49, 1219–1226 (1998).

Strzepek R. F., Maldonado M. T., Hunter K. A., Frew R. D., Boyd P. W., Adaptive strategies by southern ocean phytoplankton to lessen iron limitation: Uptake of organically complexed iron and reduced cellular iron requirements. Limnol. Oceanogr. 56, 1983–2002 (2011).

Cooper L. H. N., Iron in the sea and in marine plankton. Proc. R. Soc. Lond. 118, 419–438 (1935).

Gordon R. M., Martin J. H., Knauer G. A., Iron in north-east Pacific waters. Nature 299, 611 (1982).

Patel P., Song L., Challis G. L., Distinct extracytoplasmic siderophore binding proteins recognize ferrioxamines and ferricoelichelin in Streptomyces coelicolor A3(2). Biochemistry 49, 8033–8042 (2010). PubMed

Stintzi A., Barnes C., Xu J., Raymond K. N., Microbial iron transport via a siderophore shuttle: A membrane ion transport paradigm. Proc. Natl. Acad. Sci. U.S.A. 97, 10691–10696 (2000). PubMed PMC

Martinez J. S., Butler A., Marine amphiphilic siderophores: Marinobactin structure, uptake, and microbial partitioning. J. Inorg. Biochem. 101, 1692–1698 (2007). PubMed PMC

Miethke M., Hou J., Marahiel M. A., The siderophore-interacting protein YqjH acts as a ferric reductase in different iron assimilation pathways of Escherichia coli. Biochemistry 50, 10951–10964 (2011). PubMed

Anderson M. A., Morel F. M., Uptake of Fe (II) by a diatom in oxic culture medium. Mar. Biol. Lett. 1, 263–268 (1980).

Shaked Y., Kustka A. B., Morel F. M. M., Erel Y., Simultaneous determination of iron reduction and uptake by phytoplankton. Limnol. Oceanogr. Methods 2, 137–145 (2004).

Müller G., Raymond K. N., Specificity and mechanism of ferrioxamine-mediated iron transport in Streptomyces pilosus. J. Bacteriol. 160, 304–312 (1984). PubMed PMC

McKie A. T., et al. , An iron-regulated ferric reductase associated with the absorption of dietary iron. Science 291, 1755–1759 (2001). PubMed

Ohgami R. S., et al. , Identification of a ferrireductase required for efficient transferrin-dependent iron uptake in erythroid cells. Nat. Genet. 37, 1264–1269 (2005). PubMed PMC

Ciechanover A., Schwartz A. L., Dautry-Varsat A., Lodish H. F., Kinetics of internalization and recycling of transferrin and the transferrin receptor in a human hepatoma cell line. Effect of lysosomotropic agents. J. Biol. Chem. 258, 9681–9689 (1983). PubMed

Harrington J. M., Crumbliss A. L., The redox hypothesis in siderophore-mediated iron uptake. Biometals 22, 679–689 (2009). PubMed

Marschner H., Treeby M., Römheld V., Role of root‐induced changes in the rhizosphere for iron acquisition in higher plants. Zeitschrift für Pflanzenernährung und Bodenkd 152, 197–204 (1989).

Biller D. V., Bruland K. W., The central California current transition zone: A broad region exhibiting evidence for iron limitation. Prog. Oceanogr. 120, 370–382 (2014).

King A. L., Barbeau K. A., Dissolved iron and macronutrient distributions in the southern California current system. J. Geophys. Res. Oceans 116, 1–18 (2011).

Bundy R. M., Biller D. V., Buck K. N., Bruland K. W., Barbeau K. A., Distinct pools of dissolved iron-binding ligands in the surface and benthic boundary layer of the California current. Limnol. Oceanogr. 59, 769–787 (2014).

Leventhal G. E., Ackermann M., Schiessl K. T., Why microbes secrete molecules to modify their environment: The case of iron-chelating siderophores. J. R. Soc. Interface 16, 20180674 (2019). PubMed PMC

Kraemer S. M., Butler A., Borer P., Cervini-Silva J., Siderophores and the dissolution of iron-bearing minerals in marine systems. Rev. Mineral. Geochem. 59, 53–84 (2005).

McDaniel L. D., et al. , High frequency of horizontal gene transfer in the oceans. Science 330, 50 (2010). PubMed

Malmstrom R. R., et al. , Ecology of uncultured Prochlorococcus clades revealed through single-cell genomics and biogeographic analysis. ISME J. 7, 184–198 (2013). PubMed PMC

Lesuisse E., Blaiseau P. L., Dancis A., Camadro J. M., Siderophore uptake and use by the yeast Saccharomyces cerevisiae. Microbiology 147, 289–298 (2001). PubMed

Kim Y., Yun C. W., Philpott C. C., Ferrichrome induces endosome to plasma membrane cycling of the ferrichrome transporter, Arn1p, in Saccharomyces cerevisiae. EMBO J. 21, 3632–3642 (2002). PubMed PMC

Egue F., et al. , Expression of the retrotransposons Surcouf and Blackbeard in the marine diatom Phaeodactylum tricornutum under thermal stress. Phycologia 54, 617–627 (2015).

Maumus F., et al. , Potential impact of stress activated retrotransposons on genome evolution in a marine diatom. BMC Genomics 10, 624 (2009). PubMed PMC

Kominek J., et al. , Eukaryotic acquisition of a bacterial operon. Cell 176, 1356–1366.e10 (2019). PubMed PMC

Schallenberg C., Davidson A. B., Simpson K. G., Miller L. A., Cullen J. T., Iron(II) variability in the northeast subarctic Pacific Ocean. Mar. Chem. 177, 33–44 (2015).

Traxler M. F., Seyedsayamdost M. R., Clardy J., Kolter R., Interspecies modulation of bacterial development through iron competition and siderophore piracy. Mol. Microbiol. 86, 628–644 (2012). PubMed PMC

Amin S. A., et al. , Photolysis of iron-siderophore chelates promotes bacterial-algal mutualism. Proc. Natl. Acad. Sci. U.S.A. 106, 17071–17076 (2009). PubMed PMC

Weyman P. D., et al. , Inactivation of Phaeodactylum tricornutum urease gene using transcription activator-like effector nuclease-based targeted mutagenesis. Plant Biotechnol. J. 13, 460–470 (2015). PubMed

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace