Siderophore-based microbial adaptations to iron scarcity across the eastern Pacific Ocean

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 50, 2016, Pages 14237-14242

  Boiteau, Rene M ^a,b   Mende, Daniel R ^c   Hawco, Nicholas J ^a,b   McIlvin, Matthew R ^a   Fitzsimmons, Jessica N ^b,d   Saito, Mak A ^a   Sedwick, Peter N ^e   Delong, Edward F ^c   Repeta, Daniel J ^a  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF HAWAII   (United States)

^d TEXAS A AND M UNIVERSITY   (United States)

^e Old Dominion University   (United States)

Author keywords

GEOTRACES; High nutrient low chlorophyll; Iron ligands; Marine microbes; Siderophores

Indexed keywords

IRON; SIDEROPHORE; LIGAND; SEA WATER;

BIOSYNTHESIS; CELL MEMBRANE; CONFERENCE PAPER; CONTROLLED STUDY; GAMMAPROTEOBACTERIA; HYDROPHILICITY; IRON TRANSPORT; MICROBIAL COMMUNITY; NONHUMAN; PACIFIC OCEAN; PHYLOGENY; PRIORITY JOURNAL; RETENTION TIME; SOLID PHASE EXTRACTION; SURFACE PROPERTY; ADAPTATION; BACTERIAL GENE; BIOAVAILABILITY; CLASSIFICATION; GENETICS; METABOLISM; MICROBIOLOGY;

ADAPTATION, PHYSIOLOGICAL; BIOLOGICAL AVAILABILITY; GAMMAPROTEOBACTERIA; GENES, BACTERIAL; IRON; LIGANDS; PACIFIC OCEAN; PHYLOGENY; SEAWATER; SIDEROPHORES; WATER MICROBIOLOGY;

EID: 85006043730     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1608594113     Document Type: Article

References (50)

1. Morel FMM, Price NM (2003) The biogeochemical cycles of trace metals in the oceans. Science 300(5621):944-947.
2. Boyd PW, Ellwood MJ (2010) The biogeochemical cycle of iron in the ocean. Nat Geosci 3(10):675-682.
3. Resing JA, et al. (2015) Basin-scale transport of hydrothermal dissolved metals across the South Pacific Ocean. Nature 523(7559):200-203.
4. Hutchins DA, et al. (2002) Phytoplankton iron limitation in the Humboldt Current and Peru Upwelling. Limnol Oceanogr 47(4):997-1011.
5. Bruland KW, Rue EL, Smith GJ, DiTullio GR (2005) Iron, macronutrients and diatom blooms in the Peru upwelling regime: Brown and blue waters of Peru. Mar Chem 93(2-4):81-103.
6. Gledhill M, Buck KN (2012) The organic complexation of iron in the marine environment: A review. Front Microbiol 3:69.
7. Wells ML, Trick CG (2004) Controlling iron availability to phytoplankton in ironreplete coastal waters. Mar Chem 86(1-2):1-13.
8. Hassler CS, Schoemann V, Nichols CM, Butler ECV, Boyd PW (2011) Saccharides enhance iron bioavailability to Southern Ocean phytoplankton. Proc Natl Acad Sci USA 108(3):1076-1081.
9. Hopkinson BM, Barbeau KA (2012) Iron transporters in marine prokaryotic genomes and metagenomes. Environ Microbiol 14(1):114-128.
10. Toulza E, Tagliabue A, Blain S, Piganeau G (2012) Analysis of the global ocean sampling (GOS) project for trends in iron uptake by surface oceanmicrobes. PLoS One 7(2):e30931.
11. Völker C, Wolf-Gladrow DA (1999) Physical limits on iron uptake mediated by siderophores or surface reductases. Mar Chem 65(3-4):227-244.
12. Mawji E, et al. (2008) Hydroxamate siderophores: Occurrence and importance in the Atlantic Ocean. Environ Sci Technol 42(23):8675-8680.
13. Lis H, Shaked Y, Kranzler C, Keren N, Morel FMM (2015) Iron bioavailability to phytoplankton: An empirical approach. ISME J 9(4):1003-1013.
14. Baars O, Morel FMM, Perlman DH (2014) ChelomEx: Isotope-assisted discovery of metal chelates in complex media using high-resolution LC-MS. Anal Chem 86(22):11298-11305.
15. Akafia MM, Harrington JM, Bargar JR, Duckworth OW (2014) Metal oxyhydroxide dissolution as promoted by structurally diverse siderophores and oxalate. Geochim Cosmochim Acta 141:258-269.
16. Müller G, Raymond KN (1984) Specificity and mechanism of ferrioxamine-mediated iron transport in Streptomyces pilosus. J Bacteriol 160(1):304-312.
17. Smits THM, Duffy B (2011) Genomics of iron acquisition in the plant pathogen Erwinia amylovora: Insights in the biosynthetic pathway of the siderophore desferrioxamine E. Arch Microbiol 193(10):693-699.
18. Amin SA, Green DH, Al Waheeb D, Gärdes A, Carrano CJ (2012) Iron transport in the genus Marinobacter. Biometals 25(1):135-147.
19. Roberts AA, Schultz AW, Kersten RD, Dorrestein PC, Moore BS (2012) Iron acquisition in the marine actinomycete genus Salinispora is controlled by the desferrioxamine family of siderophores. FEMS Microbiol Lett 335(2):95-103.
20. Sunagawa S, et al.; Tara Oceans coordinators (2015) Ocean plankton. Structure and function of the global ocean microbiome. Science 348(6237):1261359.
21. Kem MP, Zane HK, Springer SD, Gauglitz JM, Butler A (2014) Amphiphilic siderophore production by oil-associating microbes. Metallomics 6(6):1150-1155.
22. Bachmann BO, Ravel J (2009) Chapter 8. Methods for in silico prediction of microbial polyketide and nonribosomal peptide biosynthetic pathways from DNA sequence data. Methods Enzymol 458(9):181-217.
23. Moore CM, et al. (2013) Processes and patterns of oceanic nutrient limitation. Nat Geosci 6(9):701-710.
24. Tagliabue A, et al. (2016) How well do global ocean biogeochemistry models simulate dissolved iron distributions? Global Biogeochem Cycles 30(2):149-174.
25. Keil RG, Kirchman DL (1999) Utilization of dissolved protein and amino acids in the northern Sargasso Sea. Aquat Microb Ecol 18(3):293-300.
26. Wei L, Ahner BA (2005) Sources and sinks of dissolved phytochelatin in natural seawater. Limnol Oceanogr 50(1):13-22.
27. Maldonado MT, et al. (2001) Iron uptake and physiological response of phytoplankton during a mesoscale Southern Ocean iron enrichment. Limnol Oceanogr 46(7):1802-1808.
28. Martinez JS, et al. (2003) Structure and membrane affinity of a suite of amphiphilic siderophores produced by a marine bacterium. Proc Natl Acad Sci USA 100(7): 3754-3759.
29. Hider RC, Kong X (2010) Chemistry and biology of siderophores. Nat Prod Rep 27(5): 637-657.
30. Williams KP, et al. (2010) Phylogeny of gammaproteobacteria. J Bacteriol 192(9): 2305-2314.
31. Malmstrom RR, et al. (2013) Ecology of uncultured Prochlorococcus clades revealed through single-cell genomics and biogeographic analysis. ISME J 7(1):184-198.
32. Rusch DB, Martiny AC, Dupont CL, Halpern AL, Venter JC (2010) Characterization of Prochlorococcus clades from iron-depleted oceanic regions. Proc Natl Acad Sci USA 107(37):16184-16189.
33. Boyd PW, et al. (2015) Why are biotic iron pools uniform across high- And low-iron pelagic ecosystems? Global Biogeochem Cycles 29(7):1028-1043.
34. Mawji E, et al. (2011) Production of siderophore type chelates in Atlantic Ocean waters enriched with different carbon and nitrogen sources. Mar Chem 124(1-4):90-99.
35. Twining BS, et al. (2011) Metal quotas of plankton in the equatorial Pacific Ocean. Deep Res Part II Top Stud Oceanogr 58(3-4):325-341.
36. Dugdale RC, Wilkerson FP (1991) Low specific nitrate uptake rate: A common feature of marine ecosystems. Limnol Oceanogr 36(8):1678-1688.
37. Sandy M, Butler A (2009) Microbial iron acquisition: Marine and terrestrial siderophores. Chem Rev 109(10):4580-4595.
38. Hydes D, et al. (2010) Determination of dissolved nutrients (N, P, Si) in seawater with high precision and inter-comparability using gas-segmented continuous flow analysers. The GO-SHIP Repeat Hydrography Manual: A Collection of Expert Reports and Guidelines (United Nations Educational, Scientific and Cultural Organization, Paris), IOCCP Report 14, ICPO Publication Series 134, pp 1-87.
39. Hooker SB, et al. (2005) The second SeaWiFS HPLC analysis round-robin experiment (SeaHARRE-2). NASA Tech Memo 2005-212785 (NASA Goddard Space Flight Center, Greenbelt, MD).
40. Boiteau RM, Fitzsimmons JN, Repeta DJ, Boyle EA (2013) Detection of iron ligands in seawater and marine cyanobacteria cultures by high-performance liquid chromatographyinductively coupled plasma-mass spectrometry. Anal Chem 85(9):4357-4362.
41. Boiteau RM, Repeta DJ (2015) An extended siderophore suite from Synechococcus sp. PCC 7002 revealed by LC-ICPMS-ESIMS. Metallomics 7(5):877-884.
42. Sedwick PN, Sohst BM, Ussher SJ, Bowie AR (2015) A zonal picture of the water column distribution of dissolved iron(II) during the U.S. GEOTRACES North Atlantic transect cruise (GEOTRACES GA03). Deep Res Part II Top Stud Oceanogr 116:166-175.
43. Vraspir JM, Holt PD, Butler A (2011) Identification of new members within suites of amphiphilic marine siderophores. Biometals 24(1):85-92.
44. Eddy SR (2011) Accelerated profile HMM searches. PLOS Comput Biol 7(10):e1002195.
45. Huerta-Cepas J, Dopazo J, Gabaldón T (2010) ETE: A Python environment for tree exploration. BMC Bioinformatics 11(1):24.
46. Sievers F, et al. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7(1):539.
47. Wallace IM, O'Sullivan O, Higgins DG, Notredame C (2006) M-Coffee: Combining multiple sequence alignment methods with T-Coffee. Nucleic Acids Res 34(6): 1692-1699.
48. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T (2009) trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25(15):1972-1973.
49. Guindon S, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst Biol 59(3):307-321.
50. Stamatakis A (2014) RAxML version 8: A tool for phylogenetic analysis and postanalysis of large phylogenies. Bioinformatics 30(9):1312-1313.