Molecular evidence of iron limitation and availability in the global diazotroph Trichodesmium

ISME Journal

Volumn 6, Issue 9, 2012, Pages 1728-1739

  Chappell, Phoebe Dreux ^a   Moffett, James W ^b   Hynes, Annette M ^a   Webb, Eric A ^b  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Cyanobacteria; diazotrophs; iron; marine; nitrogen fixation

Indexed keywords

IRON;

BIOACTIVITY; CARBON CYCLE; COLONY; COMPLEXATION; CYANOBACTERIUM; DOMINANCE; GROWTH RATE; IRON; MARINE ECOSYSTEM; MOLECULAR ANALYSIS; NITROGEN CYCLE; NITROGEN FIXATION; NUTRIENT AVAILABILITY; NUTRIENT LIMITATION; OPEN OCEAN;

ARTICLE; ATLANTIC OCEAN; BACTERIAL GENE; BIOAVAILABILITY; CLASSIFICATION; CYANOBACTERIUM; ENVIRONMENT; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PACIFIC OCEAN; PHYLOGENY; PHYSIOLOGICAL STRESS;

ATLANTIC OCEAN; BIOLOGICAL AVAILABILITY; CYANOBACTERIA; ENVIRONMENT; GENES, BACTERIAL; IRON; PACIFIC OCEAN; PHYLOGENY; STRESS, PHYSIOLOGICAL; WATER MICROBIOLOGY;

ATLANTIC OCEAN; PACIFIC OCEAN;

CYANOBACTERIA; TRICHODESMIUM; TRICHODESMIUM TENUE;

EID: 84865315768     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2012.13     Document Type: Article

References (62)

1. Achilles KM, Church TM, Wilhelm SW, Luther GW, Hutchins DA. (2003). Bioavailability of iron to Tricho-desmium colonies in the western subtropical Atlantic Ocean. Limnol Oceanogr 48: 2250-2255. (Pubitemid 37538076)
2. Anderson MA, Morel FMM, Guillard RRL. (1978). Growth limitation of a coastal diatom by low zinc iron activity. Nature 276: 70-71.
3. Andrews SC, Robinson AK, Rodriguez-Quinones F. (2003). Bacterial iron homeostasis. FEMS Microbiol Rev 27: 215-237. (Pubitemid 36694657)
4. Barbeau K, Rue EL, Trick CG, Bruland KT, Butler A. (2003). Photochemical reactivity of siderophores produced by marine heterotrophic bacteria and cyano-bacteria based on characteristic Fe(III) binding groups. Limnol Oceanogr 48: 1069-1078. (Pubitemid 36631948)
5. Batchelli S, Muller FLL, Chang KC, Lee CL. (2010). Evidence for strong but dynamic iron-humic colloidal associations in humic-rich coastal waters. Environ Sci Technol 44: 8485-8490.
6. Benporath J, Carpenter EJ, Zehr J. (1993). Genotypic relationships in Trichodesmium (Cyanophyceae) based on nifH sequence comparisons. J Phycol 29: 806-810. (Pubitemid 2038720)
7. Berman-Frank I, Cullen JT, Shaked Y, Sherrell RM, Falkowski PG. (2001). Iron availability, cellular iron quotas, and nitrogen fixation in Trichodesmium. Limnol Oceanogr 46: 1249-1260. (Pubitemid 32824603)
8. Berman-Frank I, Quigg A, Finkel ZV, Irwin AJ, Haramaty L. (2007). Nitrogen-fixation strategies and Fe requirements in cyanobacteria. Limnol Oceanogr 52: 2260-2269. (Pubitemid 47612147)
9. Bonnet S, Guieu C, Bruyant F, Prasil O, Van WF, Raimbault P et al. (2008). Nutrient limitation of primary productivity in the Southeast Pacific (BIOSOPE cruise). Biogeosciences 5: 215-225. (Pubitemid 351303274)
10. Breitbarth E, Oschilies A, LaRoche J. (2007). Physiological constraints on the global distribution of Tr i c h o d e s m i u m-effect of temperature on diazotrophy. Biogeosciences 4: 53-61. (Pubitemid 46129288)
11. Breitbarth E, Wohlers J, Klas J, LaRoche J, Peeken I. (2008). Nitrogen fixation and growth rates of Trichodesmium IMS-101 as a function of light intensity. Mar Ecol Prog Ser 359: 25-36. (Pubitemid 351798227)
12. Capone DG. (1993). Determination of nitrogenase activity in aquatic samples using the acetylene reduction procedure. In: Kemp PF, Sherr BF, Sherr EB, Cole J (eds). Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers: Boca Raton, FL, pp 621-631.
13. Capone DG, Burns JA, Montoya JP, Subramaniam A, Mahaffey C, Gunderson T et al. (2005). Nitrogen fixation by Trichodesmium spp.: an important source of new nitrogen to the tropical and subtropical North Atlantic Ocean. Global Biogeochem Cycles 19: GB2024.
14. Capone DG, Zehr JP, Paerl HW, Bergman B, Carpenter EJ. (1997). Trichodesmium, a globally significant marine cyanobacterium. Science 276: 1221-1229.
15. Carpenter EJ, O'Neil JM, Dawson R, Capone DG, Siddiqui PJA, Roenneberg T et al. (1993). The tropical diazotrophic phytoplankter Trichodesmium: biological characteristics of two common species. Mar Ecol Prog Ser 95: 295-304. (Pubitemid 24412380)
16. Carpenter EJ, Price CC. (1977). Nitrogen fixation, distribution and production of Oscillatoria (Trichodesmium) spp. in the Western Sargasso and Caribbean Seas. Limnol Oceanogr 22: 60-72.
17. Chappell PD. (2009) Iron and nitrogen fixation in Tricho-desmium spp. MIT/WHOI Joint Program PhD thesis, Cambridge, MA.
18. Chappell PD, Webb EA. (2010). A molecular assessment of the iron stress response in the two phylogenetic clades of Trichodesmium. Environ Microbiol 12: 13-27.
19. Coles VJ, Hood RR. (2007). Modeling the impact of iron and phosphorus limitations on nitrogen fixation in the Atlantic Ocean. Biogeosciences 4: 455-479. (Pubitemid 47151113)
20. Cutter GA, Andersson P, Codispoti L, Croot PL, Francois R, Lohan M et al. (2010). Sampling and sample-handling protocols for GEOTRACES cruises. http://www.jodc.go. jp/geotraces/docs/GEOTRACES-IPYProtocols-Final.pdf.
21. Dyhrman ST, Chappell PD, Haley ST, Moffett JW, Orchard ED, Waterbury JB et al. (2006). Phosphonate utilization by the globally important marine diazotroph Trichodesmium. Nature 439: 68-71. (Pubitemid 43053629)
22. Edgar RC. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797. (Pubitemid 38832724)
23. Ehrenreich IM, Waterbury JB, Webb EA. (2005). Distribution and diversity of natural product genes in marine and freshwater cyanobacterial cultures and genomes. Appl Environ Microbiol 71: 7401-7413. (Pubitemid 43194234)
24. 2 in the ocean. Nature 387: 272-275. (Pubitemid 27220759)
25. 2 fixation and photosynthesis in a cyanobacterium, Trichodesmium sp., under Fe stress. Biotechnol Lett 25: 645-649. (Pubitemid 36536569)
26. Gruber N, Sarmiento JL. (1997). Global patterns of marine nitrogen fixation and denitrification. Global Biogeo-chem Cycles 11: 235-266.
27. Hassler CS, Twiss MR. (2006). Bioavailability of iron sensed by a phytoplanktonic Fe-bioreporter. Environ Sci Technol 40: 2544-2551.
28. Herbland A, Lebouteiller A, Raimbault P. (1985). Size structure of phytoplankton biomass in the equatorial Atlantic Ocean. Deep-Sea Res 32: 819-836.
29. Hudson RJM, Morel FMM. (1993). Trace-metal transport by marine microorganisms-implications of metal coordination kinetics. Deep-Sea Res (1 Oceanogr Res Pap) 40: 129-150.
30. 2 fixation, photosynthesis, growth rates, and elemental ratios: implications for past, present, and future ocean biogeochemistry. Limnol Oceanogr 52: 1293-1304. (Pubitemid 47121544)
31. Hynes AM. (2009) Diversity of the marine Cyano-bacterium Trichodesmium: characterization of the Woods Hole culture collection and quantification of field populations. MIT/WHOI Joint Program PhD thesis, Cambridge, MA.
32. Hynes AM, Chappell PD, Dyhrman ST, Doney SC, Webb EA. (2009). Cross-basin comparison of phosphorus stress and nitrogen fixation in Trichodesmium. Limnol Oceanogr 54: 1438-1448.
33. Hynes AM, Webb EA, Doney SC, Waterbury JB. (2012). Comparison of cultured Trichodesmium (Cyano-phyceae) with species characterized from the field. J Phycol 48: 196-210.
34. Jakuba RW, Moffett JW, Dyhrman ST. (2008). Evidence for the linked biogeochemical cycling of zinc, cobalt, and phosphorus in the western North Atlantic Ocean. Global Biogeochem Cycles 22: ARTN GB4012.
35. Janson S, Bergman B, Carpenter EJ, Giovannoni SJ, Vergin K. (1999). Genetic analysis of natural populations of the marine diazotrophic cyanobacterium Trichodes-mium. FEMS Microbiol Ecol 30: 57-65. (Pubitemid 29393015)
36. Kolber ZS, Barber RT, Coale KH, Fitzwater SE, Greene RM, Johnson KS et al. (1994). Iron limitation of phyto-plankton photosynthesis in the Equatorial Pacific Ocean. Nature 371: 145-149. (Pubitemid 24284011)
37. Krishnamurthy A, Moore JK, Zender CS, Luo C. (2007). Effects of atmospheric inorganic nitrogen deposition on ocean biogeochemistry. J Geophys Res 112: ARTN G02019.
38. Kupper H, Setlik I, Seibert S, Prasil O, Setlikova E, Strittmatter M et al. (2008). Iron limitation in the marine cyanobacterium Trichodesmium reveals new insights into regulation of photosynthesis and nitrogen fixation. New Phytol 179: 784-798.
39. Kustka A, Sanudo-Wilhelmy S, Carpenter EJ, Capone DG, Raven JA. (2003a). A revised estimate of the iron use efficiency of nitrogen fixation, with special reference to the marine cyanobacterium Trichodesmium spp. (Cyanophyta). J Phycol 39: 12-25. (Pubitemid 36229964)
40. Kustka AB, Sanudo-Wilhelmy SA, Carpenter EJ, Capone D, Burns J, Sunda WG. (2003b). Iron requirements for dinitrogen-and ammonium-supported growth in cultures of Trichodesmium (IMS 101): Comparison with nitrogen fixation rates and iron: carbon ratios of field populations. Limnol Oceanogr 48: 1869-1884. (Pubitemid 37207593)
41. LaRoche J, Boyd PW, McKay RML, Geider RJ. (1996). Flavodoxin as an in situ marker for iron stress in phytoplankton. Nature 382: 802-805. (Pubitemid 26299561)
42. 2 enhances nitrogen fixation and growth in the marine cyano-bacterium Trichodesmium. Global Change Biol 13: 531-538. (Pubitemid 46232007)
43. Lundgren P, Janson S, Jonasson S, Singer A, Bergman B. (2005). Unveiling of novel radiations within Tricho-desmium cluster by hetR gene sequence analysis. Appl Environ Microbiol 71: 190-196. (Pubitemid 40116267)
44. Mahowald NM, Engelstaedter S, Luo C, Sealy A, Artaxo P, Benitez-Nelson C et al. (2009). Atmospheric iron deposition: global distribution, variability, and human perturbations. Annu Rev Mar Sci 1: 245-278.
45. Maldonado MT, Price NM. (2001). Reduction and transport of organically bound iron by Thalassiosira oceanica (Bacillariophyceae). J Phycol 37: 298-309. (Pubitemid 32391879)
46. Mills MM, Ridame C, Davey M, La Roche J, Geider RJ. (2004). Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429: 292-294. (Pubitemid 38684813)
47. Moore CM, Mills MM, Achterberg EP, Geider RJ, La Roche J, Lucas MI et al. (2009). Large-scale distribution of Atlantic nitrogen fixation controlled by iron availability. Nature Geosci 2: 867-871.
48. Moore JK, Doney SC. (2007). Iron availability limits the ocean nitrogen inventory stabilizing feedbacks between marine denitrification and nitrogen fixation. Global Biogeochem Cycles 21: ARTN GB2001.
49. Moore JK, Doney SC, Lindsay K. (2004). Upper ocean ecosystem dynamics and iron cycling in a global three-dimensional model. Global Biogeochem Cycles 18: ARTN GB4028.
50. Moutin T, Van Den Broeck N, Beker B, Dupouy C, Rimmelin P, Le Bouteiller A. (2005). Phosphate availability controls Trichodesmium spp. biomass in the SW Pacific Ocean. Mar Ecol Prog Ser 297: 15-21. (Pubitemid 41215411)
51. Orcutt KM, Rasmussen U, Webb EA, Waterbury JB, Gundersen K, Bergman B. (2002). Characterization of Trichodesmium spp. by genetic techniques. Appl Environ Microbiol 68: 2236-2245. (Pubitemid 34477817)
52. Ramos JBe, Biswas H, Schulz KG, Laroche J, Riebesell U. (2007). Effect of rising atmospheric carbon dioxide on the marine nitrogen fixer Trichodesmium. Global Biogeochem Cycles 21: GB2028.
53. Rivers AR, Jakuba RW, Webb EA. (2009). Iron stress genes in marine Synechococcus and the development of a flow cytometric iron stress assay. Environ Microbiol 11: 382-396.
54. Rubin M, Berman-Frank I, Shaked Y. (2011). Dust-and mineral-iron utilization by the marine dinitrogen-fixer Trichodesmium. Nat Geosci 4: 529-534.
55. Rue EL, Bruland KW. (1995). 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. (Pubitemid 26463192)
56. 2 preconcentration inductively coupled plasma mass spectrometry (ICP-MS) method for high-throughput analysis of open-ocean Fe and Mn in seawater. Anal Chim Acta 565: 222-233.
57. Sanudo-Wilhelmy SA, Kustka AB, Gobler CJ, Hutchins DA, Yang M, Lwiza K et al. (2001). Phosphorus limitation of nitrogen fixation by Trichodesmium in the central Atlantic Ocean. Nature 411: 66-69. (Pubitemid 32428189)
58. Shi T, Sun Y, Falkowski PG. (2007). Effects of iron limitation on the expression of metabolic genes in the marine cyanobacterium Trichodesmium ery-thraeum IMS 101. Environ Microbiol 9: 2945-2956. (Pubitemid 350076285)
59. Sohm JA, Mahaffey C, Capone DG. (2008). Assessment of relative phosphorus limitation of Trichodesmium spp. in the North Pacific, North Atlantic, and the north coast of Australia. Limnol Oceanogr 53: 2495-2502.
60. Webb EA, Jakuba RW, Moffett JW, Dyhrman ST. (2007). Molecular assessment of phosphorus and iron physiology in Trichodesmium populations from the western Central and western South Atlantic. Limnol Oceanogr 52: 2221-2232. (Pubitemid 47612144)
61. Webb EA, Moffett JW, Waterbury JB. (2001). Iron stress in open-ocean cyanobacteria (Synechococcus, Trichodes-mium, and Crocosphaera spp.): identification of the IdiA protein. Appl Environ Microbiol 67: 5444-5452. (Pubitemid 33640974)
62. Wu J, Boyle E, Sunda W, Wen L. (2001). Soluble and colloidal iron in the oligotrophic North Atlantic and North Pacific. Science 293: 847-849. (Pubitemid 32743971)