Endocytosis-mediated siderophore uptake as a strategy for Fe acquisition in diatoms
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
29774236
PubMed Central
PMC5955625
DOI
10.1126/sciadv.aar4536
PII: aar4536
Knihovny.cz E-zdroje
- MeSH
- chloroplasty metabolismus MeSH
- druhová specificita MeSH
- endocytóza * MeSH
- genový knockdown MeSH
- rozsivky fyziologie MeSH
- siderofory metabolismus MeSH
- transport proteinů MeSH
- vodní organismy metabolismus MeSH
- železo metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- siderofory MeSH
- železo MeSH
Phytoplankton growth is limited in vast oceanic regions by the low bioavailability of iron. Iron fertilization often results in diatom blooms, yet the physiological underpinnings for how diatoms survive in chronically iron-limited waters and outcompete other phytoplankton when iron becomes available are unresolved. We show that some diatoms can use siderophore-bound iron, and exhibit a species-specific recognition for siderophore types. In Phaeodactylum tricornutum, hydroxamate siderophores are taken up without previous reduction by a high-affinity mechanism that involves binding to the cell surface followed by endocytosis-mediated uptake and delivery to the chloroplast. The affinity recorded is the highest ever described for an iron transport system in any eukaryotic cell. Collectively, our observations suggest that there are likely a variety of iron uptake mechanisms in diatoms besides the well-established reductive mechanism. We show that iron starvation-induced protein 1 (ISIP1) plays an important role in the uptake of siderophores, and through bioinformatics analyses we deduce that this protein is largely diatom-specific. We quantify expression of ISIP1 in the global ocean by querying the Tara Oceans atlas of eukaryotic genes and show a link between the abundance and distribution of diatom-associated ISIP1 with ocean provinces defined by chronic iron starvation.
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Morrissey J., Bowler C., Iron utilization in marine cyanobacteria and eukaryotic algae. Front. Microbiol. 3, 43 (2012). PubMed PMC
Raven J. A., Evans M. C. W., Korb R. E., The role of trace metals in electron transport in O2-evolving organisms. Photosynth. Res. 60, 111–150 (1999).
Boyd P. W., Jickells T., Law C. S., Blain S., Boyle E. A., Buesseler K. O., Coale K. H., Cullen J. J., de Baar H. J. W., Follows M., Harvey M., Lancelot C., Levasseur M., Owens N. P. J., Pollard R., Rivkin R. B., Sarmiento J., Schoemann V., Smetacek V., Takeda S., Tsuda A., Turner S., Watson A. J., Mesoscale iron enrichment experiments 1993–2005: Synthesis and future directions. Science 315, 612–617 (2007). PubMed
Coale K. H., Johnson K. S., Chavez F. P., Buesseler K. O., Barber R. T., Brzezinski M. A., Cochlan W. P., Millero F. J., Falkowski P. G., Bauer J. E., Wanninkhof R. H., Kudela R. M., Altabet M. A., Hales B. E., Takahashi T., Landry M. R., Bidigare R. R., Wang X., Chase Z., Strutton P. G., Friederich G. E., Gorbunov M. Y., Lance V. P., Hilting A. K., Hiscock M. R., Demarest M., Hiscock W. T., Sullivan K. F., Tanner S. J., Gordon R. M., Hunter C. N., Elrod V. A., Fitzwater S. E., Jones J. L., Tozzi S., Koblizek M., Roberts A. E., Herndon J., Brewster J., Ladizinsky N., Smith G., Cooper D., Timothy D., Brown S. L., Selph K. E., Sheridan C. C., Twining B. S., Johnson Z. I., Southern Ocean iron enrichment experiment: Carbon cycling in high- and low-Si waters. Science 304, 408–414 (2004). PubMed
Granum E., Raven J. A., Leegood R. C., How do marine diatoms fix 10 billion tonnes of inorganic carbon per year? Can. J. Bot. 83, 898–908 (2005).
Bowler C., Allen A. E., Badger J. H., Grimwood J., Jabbari K., Kuo A., Maheswari U., Martens C., Maumus F., Otillar R. P., Rayko E., Salamov A., Vandepoele K., Beszteri B., Gruber A., Heijde M., Katinka M., Mock T., Valentin K., Verret F., Berges J. A., Brownlee C., Cadoret J.-P., Chiovitti A., Choi C. J., Coesel S., De Martino A., Detter J. C., Durkin C., Falciatore A., Fournet J., Haruta M., Huysman M. J. J., Jenkins B. D., Jiroutova K., Jorgensen R. E., Joubert Y., Kaplan A., Kröger N., Kroth P. G., La Roche J., Lindquist E., Lommer M., Martin-Jézéquel V., Lopez P. J., Lucas S., Mangogna M., McGinnis K., Medlin L. K., Montsant A., Oudot-Le Secq M.-P., Napoli C., Obornik M., Parker M. S., Petit J.-L., Porcel B. M., Poulsen N., Robison M., Rychlewski L., Rynearson T. A., Schmutz J., Shapiro H., Siaut M., Stanley M., Sussman M. R., Taylor A. R., Vardi A., von Dassow P., Vyverman W., Willis A., Wyrwicz L. S., Rokhsar D. S., Weissenbach J., Armbrust E. V., Green B. R., Van de Peer Y., Grigoriev I. V., The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456, 239–244 (2008). PubMed
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).
Cohen N. R., Ellis K. A., Lampe R. H., McNair H., Twining B. S., Maldonado M. T., Brzezinski M. A., Kuzminov F. I., Thamatrakoln K., Till C. P., Bruland K. W., Sunda W. G., Bargu S., Marchetti A., Diatom transcriptional and physiological responses to changes in iron bioavailability across ocean provinces. Front. Mar. Sci. 4, 360 (2017).
Allen A. E., LaRoche J., Maheswari U., Lommer M., Schauer N., Lopez P. J., Finazzi G., Fernie A. R., Bowler C., 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
Lommer M., Specht M., Roy A.-S., Kraemer L., Andreson R., Gutowska M. A., Wolf J., Bergner S. V., Schilhabel M. B., Klostermeier U. C., Beiko R. G., Rosenstiel P., Hippler M., LaRoche J., Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation. Genome Biol. 13, R66 (2012). PubMed PMC
Marchetti A., Schruth D. M., Durkin C. A., Parker M. S., Kodner R. B., Berthiaume C. T., Morales R., Allen A. E., Armbrust E. V., 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
Morrissey J., Sutak R., Paz-Yepes L., Tanaka A., Moustafa A., Velucham A., Thomas Y., Botebol H., Bouget F.-Y., McQuaid J. B., Tirichine L., Allen A. E., Lesuisse E., Bowler C., A novel protein, ubiquitous in marine phytoplankton, concentrates iron at the cell surface and facilitates uptake. Curr. Biol. 25, 364–371 (2015). PubMed
Anderson M. A., Morel F. M. M., The influence of aqueous iron chemistry on the uptake of iron by the coastal diatom Thalassiosira weissflogii. Limnol. Oceanogr. 27, 789–813 (1982).
McQuaid J. B., Kustka A. B., Oborník M., Horák A., McCrow J. P., Karas B. J., Zheng H., Kindeberg T., Andersson A. J., Barbeau K. A., Allen A. E., Carbonate sensitive phytotransferrin controls high affinity iron uptake in diatoms. Nature 555, 534–537 (2018). PubMed
Shaked Y., Lis H., Disassembling iron availability to phytoplankton. Front. Microbiol. 3, 123 (2012). PubMed PMC
Morel F. M. M., Kustka A. B., Shaked Y., The role of unchelated Fe in the iron nutrition of phytoplankton. Limnol. Oceanogr. 53, 400–404 (2008).
Gledhill M., Buck K. N., The organic complexation of iron in the marine environment: A review. Front. Microbiol. 3, 69 (2012). PubMed PMC
Buck K. N., Selph K. E., Barbeau K. A., Iron-binding ligand production and copper speciation in an incubation experiment of Antarctic Peninsula shelf waters from the Bransfield Strait, Southern Ocean. Mar. Chem. 122, 148–159 (2010).
King A. L., Buck K. N., Barbeau K. A., Quasi-Lagrangian drifter studies of iron speciation and cycling off Point Conception, California. Mar. Chem. 128–129, 1–12 (2012).
Sutak R., Lesuisse E., Tachezy J., Richardson D. R., Crusade for iron: Iron uptake in unicellular eukaryotes and its significance for virulence. Trends Microbiol. 16, 261–268 (2008). PubMed
Lesuisse E., Simon-Casteras M., Labbe P., Siderophore-mediated iron uptake in Saccharomyces cerevisiae: The SIT1 gene encodes a ferrioxamine B permease that belongs to the major facilitator superfamily. Microbiology 144, 3455–3462 (1998). PubMed
Chu B. C., Garcia-Herrero A., Johanson T. H., Krewulak K. D., Lau C. K., Peacock R. S., Vogel H. J., Siderophore uptake in bacteria and the battle for iron with the host; a bird’s eye view. Biometals 23, 601–611 (2010). PubMed
Kustka A. B., Jones B. M., Hatta M., Field M. P., Milligan A. J., The influence of iron and siderophores on eukaryotic phytoplankton growth rates and community composition in the Ross Sea. Mar. Chem. 173, 195–207 (2015).
Soria-Dengg S., Horstmann U.. Ferrioxamines B and E as iron sources for the marine diatom Phaeodactylum tricornutum. Mar. Ecol. Prog. Ser. 127, 269–277 (1995).
Maldonado M. T., Price N. M., Reduction and transport of organically bound iron by Thalassiosira oceanica (Bacillariophyceae). J. Phycol. 37, 298–310 (2001).
Shaked Y., Kustka A. B., Morel F. M. M., A general kinetic model for iron acquisition by eukaryotic phytoplankton. Limnol. Oceanogr. 50, 872–882 (2005).
Griffin A. S., West S. A., Buckling A., Cooperation and competition in pathogenic bacteria. Nature 430, 1024–1027 (2004). PubMed
Keeling P. J., Burki F., Wilcox H. M., Allam B., Allen E. E., Amaral-Zettler L. A., Armbrust E. V., Archibald J. M., Bharti A. K., Bell C. J., Beszteri B., Bidle K. D., Cameron C. T., Campbell L., Caron D. A., Cattolico R. A., Collier J. L., Coyne K., Davy S. K., Deschamps P., Dyhrman S. T., Edvardsen B., Gates R. D., Gobler C. J., Greenwood S. J., Guida S. M., Jacobi J. L., Jakobsen K. S., James E. R., Jenkins B., John U., Johnson M. D., Juhl A. R., Kamp A., Katz L. A., Kiene R., Kudryavtsev A., Leander B. S., Lin S., Lovejoy C., Lynn D., Marchetti A., McManus G., Nedelcu A. M., Menden-Deuer S., Miceli C., Mock T., Montresor M., Moran M. A., Murray S., Nadathur G., Nagai S., Ngam P. B., Palenik B., Pawlowski J., Petroni G., Piganeau G., Posewitz M. C., Rengefors K., Romano G., Rumpho M. E., Rynearson T., Schilling K. B., Schroeder D. C., Simpson A. G. B., Slamovits C. H., Smith D. R., Smith G. J., Smith S. R., Sosik H. M., Stief P., Theriot E., Twary S. N., Umale P. E., Vaulot D., Wawrik B., Wheeler G. L., Wilson W. H., Xu Y., Zingone A., Worden A. Z., The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): Illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLOS Biol. 12, e1001889 (2014). PubMed PMC
Carradec Q., Pelletier E., Da Silva C., Alberti A., Seeleuthner Y., Blanc-Mathieu R., Lima-Mendez G., Rocha F., Tirichine L., Labadie K., Kirilovsky A., Bertrand A., Engelen S., Madoui M.-A., Méheust R., Poulain J., Romac S., Richter D. J., Yoshikawa G., Dimier C., Kandels-Lewis S., Picheral M., Searson S.; Tara Oceans Coordinators, Jaillon O., Aury J.-M., Karsenti E., Sullivan M. B., Sunagawa S., Bork P., Not F., Hingamp P., Raes J., Guidi L., Ogata H., de Vargas C., Iudicone D., Bowler C., Wincker P., A global ocean atlas of eukaryotic genes. Nat. Commun. 9, 373 (2018). PubMed PMC
Kosman D. J., Molecular mechanisms of iron uptake in fungi. Mol. Microbiol. 47, 1185–1197 (2003). PubMed
Ouchetto H., Dias M., Mornet R., Lesuisse E., Camadro J.-M., A new route to trihydroxamate-containing artificial siderophores and synthesis of a new fluorescent probe. Bioorg. Med. Chem. 13, 1799–1803 (2005). PubMed
De Martino A., Bartual A., Willis A., Meichenin A., Villazán B., Maheswari U., Bowler C., Physiological and molecular evidence that environmental changes elicit morphological interconversion in the model diatom Phaeodactylum tricornutum. Protist 162, 462–481 (2011). PubMed
Barberon M., Zelazny E., Robert S., Conéjéro G., Curie C., Friml J., Vert G., Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) transporter controls iron uptake in plants. Proc. Natl. Acad. Sci. U.S.A. 108, E450–E458 (2011). PubMed PMC
van Gisbergen P. A. C., Esseling-Ozdoba A., Vos J. W., Microinjecting FM4-64 validates it as a marker of the endocytic pathway in plants. J. Microsc. 231, 284–290 (2008). PubMed
Matringe M., Camadro J. M., Labbe P., Scalla R., Protoporphyrinogen oxidase as a molecular target for diphenyl ether herbicides. Biochem. J. 260, 231–235 (1989). PubMed PMC
Bullmann L., Haarmann R., Mirus O., Bredemeier R., Hempel F., Maier U. G., Schleiff E., Filling the gap, evolutionarily conserved Omp85 in plastids of chromalveolates. J. Biol. Chem. 285, 6848–6856 (2010). PubMed PMC
Gruber A., Rocap G., Kroth P. G., Armbrust E. V., Mock T., Plastid proteome prediction for diatoms and other algae with secondary plastids of the red lineage. Plant J. 81, 519–528 (2015). PubMed PMC
Rastogi A., Maheswari U., Dorrell R. G., Vieira F. R. J., Maumus F., Kustka A., McCarthy J., Allen A. E., Kersey P., Bowler C., Tirichine L., Integrative analysis of large scale transcriptome data draws a comprehensive landscape of Phaeodactylum tricornutum genome and evolutionary origin of diatoms. Sci. Rep. 8, 4834 (2018). PubMed PMC
Lamb C. A., Dooley H. C., Tooze S. A., Endocytosis and autophagy: Shared machinery for degradation. Bioessays 35, 34–45 (2013). PubMed
Springer T. A., An extracellular β-propeller module predicted in lipoprotein scavenger receptors, tyrosine kinases, epidermal growth factor precursor, and extracellular matrix components. J. Mol. Biol. 283, 837–862 (1998). PubMed
Dorrell R. G., Gile G., McCallum G., Méheust R., Bapteste E. P., Klinger C. M., Brillet-Guéguen L., Freeman K. D., Richter D. J., Bowler C., Chimeric origins of ochrophytes and haptophytes revealed through an ancient plastid proteome. eLife 6, e23717 (2017). PubMed PMC
Marchetti A., Maldonado M. T., Lane E. S., Harrison P. J., Iron requirements of the pennate diatom Pseudo-nitzschia: Comparison of oceanic (high-nitrate, low-chlorophyll waters) and coastal species. Limnol. Oceanogr. 51, 2092–2101 (2006).
Hutchins D. A., Witter A. E., Butler A., Luther G. W. III, Competition among marine phytoplankton for different chelated iron species. Nature 400, 858–861 (1999).
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
Tagliabue A., Bowie A. R., Boyd P. W., Buck K. N., Johnson K. S., Saito M. A., The integral role of iron in ocean biogeochemistry. Nature 543, 51–59 (2017). PubMed
Marchetti A., Moreno C. M., Cohen N. R., Oleinikov I., deLong K., Twining B. S., Armbrust E. V., Lampe R. H., Development of a molecular-based index for assessing iron status in bloom-forming pennate diatoms. J. Phycol. 53, 820–832 (2017). PubMed
Vraspir J. M., Butler A., Chemistry of marine ligands and siderophores. Ann. Rev. Mar. Sci. 1, 43–63 (2009). PubMed PMC
Mawji E., Gledhill M., Milton J. A., Tarran G. A., Ussher S., Thompson A., Wolff G. A., Worsfold P. J., Achterberg E. P., Hydroxamate siderophores: Occurrence and importance in the Atlantic Ocean. Environ. Sci. Technol. 42, 8675–8680 (2008). PubMed
Boiteau R. M., Mende D. R., Hawco N. J., McIlvin M. R., Fitzsimmons J. N., Saito M. A., Sedwick P. N., DeLong E. F., Repeta D. J., 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
Tréguer P., Bowler C., Moriceau B., Dutkiewicz S., Gehlen M., Aumont O., Bittner L., Dugdale R., Finkel Z., Iudicone D., Jahn O., Guidi L., Lasbleiz M., Leblanc K., Levy M., Pondaven P., Influence of diatom diversity on the ocean biological carbon pump. Nat. Geosci. 11, 27–37 (2017).
Siaut M., Heijde M., Mangogna M., Montsant A., Coesel S., Allen A., Manfredonia A., Falciatore A., Bowler C., Molecular toolbox for studying diatom biology in Phaeodactylum tricornutum. Gene 406, 23–35 (2007). PubMed
Falciatore A., Casotti R., Leblanc C., Abrescia C., Bowler C., Transformation of nonselectable reporter genes in marine diatoms. Mar. Biotechnol. 1, 239–251 (1999). PubMed
Livak K. J., Schmittgen T. D., Analysis of relative gene expression data using real-time quantitative PCR and the PubMed
Pfaffl M. W., Tichopad A., Prgomet C., Neuvians T. P., Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper—Excel-based tool using pair-wise correlations. Biotechnol. Lett. 26, 509–515 (2004). PubMed
Smith S. R., Gillard J. T. F., Kustka A. B., McCrow J. P., Badger J. H., Zheng H., New A. M., Dupont C. L., Obata T., Fernie A. R., Allen A. E., Transcriptional orchestration of the global cellular response of a model pennate diatom to diel light cycling under iron limitation. PLOS Genet. 13, e1006688 (2017). PubMed PMC
Sunda W. G., Price N. M., Morel F. M. M., Trace metal ion buffers and their use in culture studies. Algal Cult. Tech. 4, 35–63 (2005).
Tang D., Morel F. M. M., Distinguishing between cellular and Fe-oxide-associated trace elements in phytoplankton. Mar. Chem. 98, 18–30 (2006).
Sutak R., Botebol H., Blaiseau P.-L., Léger T., Bouget F.-Y., Camadro J.-M., Lesuisse E., A comparative study of iron uptake mechanisms in marine microalgae: Iron binding at the cell surface is a critical step. Plant Physiol. 160, 2271–2284 (2012). PubMed PMC
Mistry J., Finn R. D., Eddy S. R., Bateman A., Punta M., Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions. Nucleic Acids Res. 41, e121 (2013). PubMed PMC
Sorhannus U., A nuclear-encoded small-subunit ribosomal RNA timescale for diatom evolution. Mar. Micropaleontol. 65, 1–12 (2007).
Kozik P., Francis R. W., Seaman M. N. J., Robinson M. S., A screen for endocytic motifs. Traffic 11, 843–855 (2010). PubMed PMC
Convergent evolution and horizontal gene transfer in Arctic Ocean microalgae
Complex Response of the Chlorarachniophyte Bigelowiella natans to Iron Availability
Iron Uptake Mechanisms in Marine Phytoplankton
Reduction-dependent siderophore assimilation in a model pennate diatom