Metal limitation of cyanobacterial N2 fixation and implications for the Precambrian nitrogen cycle

Geobiology

Volumn 4, Issue 4, 2006, Pages 285-297

  Zerkle, A L ^a   House, C H ^a   Cox, R P ^b   Canfield, D E ^b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

AIR-SEA INTERACTION; ARCHEAN; CYANOBACTERIUM; IRON; MOLYBDENUM; NITROGEN CYCLE; NITROGEN FIXATION; PRECAMBRIAN; PROTEROZOIC; REDOX CONDITIONS;

CYANOBACTERIA; PROKARYOTA;

EID: 33751207685     PISSN: 14724677     EISSN: 14724669     Source Type: Journal    
DOI: 10.1111/j.1472-4669.2006.00082.x     Document Type: Conference Paper

References (136)

1. Anbar AD, Knoll AH (2002) Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science 297, 1137-1142.
2. Arnold GL, Anbar AD, Barling J, Lyons TW (2004) Molybdenum isotope evidence for widespread anoxia in mid-Proterozoic oceans. Science 304, 87-90.
3. Arrigo KR (2005) Marine microorganisms and global nutrient cycles. Nature 437, 349-455.
4. Averill BA (1996) Dissimilatory nitrite and nitric oxide reductases. Chemical Review 96, 2951-2964.
5. Bekker A, Holland HD, Wang PL, Rumble D, Stein HJ, Hannah JL, Coetzee LL, Beukes NJ (2004) Dating the rise of atmospheric oxygen. Geochimica et Cosmochimica Acta 68, A780-A780.
6. Bergman B, Gallon JR, Rai AN, Stal LJ (1997) N-2 fixation by non-heterocystous cyanobacteria. FEMS Microbiology Review 19, 139-185.
7. Berman-Frank I, Lundgren P, Chen YB, Kupper H, Kolber Z, Bergman B, Falkowski P (2001) Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium Trichodesmium. Science 294, 1534-1537.
8. Berman-Frank I, Lundgren P, Falkowski P (2003) Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Research in Microbiology 154, 157-164.
9. Berman-Frank I, Chen YB, Gerchman Y, Dismukes GC, Falkowski P (2005) Inhibition of nitrogenase by oxygen in marine cyanobacteria controls the global nitrogen and oxygen cycles. Biogeosciences Discussions 2, 261-273.
10. Beukes NJ, Klein C (1990) Geochemistry and sedimentology of a facies transition from microbanded to granular iron-formation. the early Proterozoic Transvaal Supergroup, South Africa. Precambrian Research 47, 99-139.
11. Bishop PE, Jarlenski DML, Hetherington DR (1982) Expression of an alternative nitrogen-fixation system in Azotobacter vinelandii. Journal of Bacteriology 150, 1244-1251.
12. Bjerrum CJ, Canfield DE (2002) Ocean productivity before about 1.9 Gyr ago limited by phosphorous adsorption onto iron oxides. Nature 417, 159-162.
13. Brocks JJ, Logan GA, Buick R, Summons RE (1999) Archean molecular fossils and the early rise of eukaryotes. Science 285, 1033-1036.
14. Brocks JJ, Love GD, Summons RE, Knoll AH, Logan GA, Bowden SA (2005) Biomarker evidence for green and purple sulphur bacteria in a stratified Palaeoproterozoic sea. Nature 437, 866-870.
15. Broda E, Peschek GA (1983) Nitrogen-fixation as evidence for the reducing nature of the early biosphere. Biosystems 16, 1-8.
16. Bruland KW, Donat JR, Hutchins DA (1991) Interactive influences of bioactive trace metals on biological production in oceanic waters. Limnology and Oceanography 36, 1555-1577.
17. Buick R (1992) The antiquity of oxygenic photosynthesis - evidence from stromatolites in sulfate-deficient Archean lakes. Science 255, 74-77.
18. Burris RH (1991) Nitrogenases. Journal of Biological Chemistry 266, 9339-9342.
19. Canfield DE (1998) A new model for Proterozoic ocean chemistry. Nature 396, 450-453.
20. Canfield DE (2005) The early history of atmospheric oxygen: homage to Robert A. Garrels. Annual Review of Earth and Planetary Sciences 33, 1-36.
21. Canfield DE, Teske A (1996) Late Proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulphur-isotope studies. Nature 382, 127-132.
22. Capone DG, Zehr JP, Paerl HW, Bergman B, Carpenter EJ (1997) Trichodesmium, a globally significant marine cyanobacterium. Science 276, 1221-1229.
23. Capone DG, Burns JA, Montoya JP, Subramaniam A, Mahaffey C, Gunderson T, Michaels AF, Carpenter EJ (2005) Nitrogen fixation by Trichodesmium spp. An important source of new nitrogen to the tropical and subtropical North Atlantic Ocean. Global Biogeochemical Cycles 19.
24. 2 fixing symbiotic association in the tropical Atlantic Ocean. Marine Ecology Progress Series 188, 273-283.
25. Carpenter EJ, Romans K (1991) Major role of the cyanobacterium Trichodesmium in nutrient cycling in the North-Atlantic Ocean. Science 254, 1356-1358.
26. Catling DC, Zahnle KJ, McKay CP (2001) Biogenic methane, hydrogen escape, and the irreversible oxidation of early Earth. Science 293, 839-843.
27. Chen YB, Dominic B, Mellon MT, Zehr JP (1998) Circadian rhythm of nitrogenase gene expression in the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp. strain IMS101. Journal of Bacteriology 180, 3598-3605.
28. Cole JJ, Lane JM, Marino R, Howarth RW (1993) Molybdenum assimilation by cyanobacteria and phytoplankton in freshwater and salt water. Limnology and Oceanography 38, 25-35.
29. Collier RW (1985) Molybdenum in the Northeast Pacific Ocean. Limnology and Oceanography 30, 1351-1354.
30. 2-fixing colonial cyanobacterium Trichodesmium. Science 312, 1517-1520.
31. Dean DR, Jacobson MR (1992) Biochemical genetics of nitrogenase. In Biological Nitrogen Fixation (eds Stacey G, Burris RH, Evans HJ). Chapman & Hall, New York, pp. 763-784.
32. Dilworth M (1967) Acetylene reduction by nitrogen-fixing preparations from Clostridium pasteurianum. Biochemica Biophysica Acta 127, 285-294.
33. Donat JR, Bruland KW (1995) Trace Elements in Natural Waters. CRC Press, Boca Raton, FL.
34. Dyhrman ST, Chappell PD, Haley ST, Moffett JW, Orchard ED, Waterbury JB, Webb EA (2006) Phosphonate utilization by the globally important marine diazotroph Trichodesmium. Nature 439, 68-71.
35. Eady RR (1996) Structure-function relationships of alternative nitrogenases. Chemical Review 96, 3013-3030.
36. Elbahloul Y, Steinbuchel A (2006) Engineering the genotype of Acinetobacter sp. strain ADP1 to enhance biosynthesis of cyanophycin. Applied and Environmental Microbiology 72, 1410-1419.
37. Elbahloul Y, Krehenbrink M, Reichelt R, Steinbuchel A (2005) Physiological conditions conducive to high cyanophycin content in biomass of Acinetobacter calcoaceticus strain ADP1. Applied and Environmental Microbiology 71, 858-866.
38. Emerson SR, Huested SS (1991) Ocean anoxia and the concentrations of molybdenum and vanadium in seawater. Marine Chemistry 34, 177-196.
39. Erdner DL, Price NM, Doucette GJ, Peleato ML, Anderson DM (1999) Characterization of ferrodoxin and flavodoxin as markers of iron limitation in marine phytoplankton. Marine Ecology Progress Series 184, 43-53.
40. 2 in the ocean. Nature 387, 272-275.
41. Fani R, Gallo R, Lio P (2000) Molecular evolution of nitrogen fixation: the evolutionary history of the nifD, nifK, nifE, and nifN genes. Journal of Molecular Evolution 51, 1-11.
42. Farquhar J, Bao HM, Thiemens M (2000) Atmospheric influence of Earth's earliest sulfur cycle. Science 289, 756-758.
43. Fennel K, Follows M, Falkowski P (2005) Biogeochemical signatures through time as inferred from whole microbial genomes. American Journal of Science 305, 526-545.
44. Ferreira F, Straus NA (1994) Iron deprivation in cyanobacteria. Journal of Applied Phycology 6, 199-210.
45. Flynn KJ, Hipkin CR (1999) Interactions between iron, light, ammonium, and nitrate: insights from the construction of a dynamic model of algal physiology. Journal of Phycology 35, 66-69.
46. Frausto da Silva JJR, Williams RJP (2001) The Biological Chemistry of the Elements. Oxford University Press, New York.
47. 2-fixing system. Journal of Bacteriology 174, 6840-6843.
48. 2 fixation and oxygen. New Phytology 122, 571-609.
49. Gordon RM, Martin JH, Knauer GA (1982) Iron in north-east Pacific waters. Nature 299, 611-612.
50. Gourse RL, Gaal T, Bartlett MS, Appleman JA, Ross W (1996) rRNA transcription and growth rate-dependent regulation of ribosome synthesis in Escherichia coli. Annual Review of Microbiology 50, 645-677.
51. Haury JF, Spiller H (1981) Fructose uptake and influence on growth of and nitrogen fixation by Anabaena variabilis. Journal of Bacteriology 147, 227-235.
52. Helz GR, Miller CV, Charnock JM, Mosselmans JFW, Pattrick RAD, Garner CD, Vaughan DJ (1996) Mechanism of molybdenum removal from the sea and its concentration in black shales: EXAFS evidence. Geochimica et Cosmochimica Acta 60, 3631-3642.
53. Hille R (1996) The mononuclear molybdenum enzymes. Chemical Review 96.
54. Holland HD (1973) The Oceans: a possible source of iron in iron-formations. Economic Geology and the Bulletin of the Society of Economic Geologists 68, 1169-1172.
55. Holland HD (1984) The Chemical Evolution of the Atmosphere and Oceans. Princeton University Press, Princeton, NJ.
56. Howard JB, Rees DC (1996) Structural basis of biological nitrogen fixation. Chemical Review 96, 2965-2982.
57. Howarth RW, Cole JJ (1985) Molybdenum availability, nitrogen limitation, and phytoplankton growth in natural waters. Science 229, 653-655.
58. Isley AE, Abbott DH (1999) Plume-related mafic volcanism and the deposition of banded iron formation. Journal of Geophysical Research-Solid Earth 104, 15461-15477.
59. Jacobitz S, Bishop PE (1992) Regulation of nitrogenase-2 in Azotobacter vinelandii by ammonium, molybdenum, and vanadium. Journal of Bacteriology 174, 3884-3888.
60. Jacobson MR, Premakumar R, Bishop PE (1986) Transcriptional regulation of nitrogen-fixation by molybdenum in Azotobacter vinelandii. Journal of Bacteriology 167, 480-486.
61. Joerger RD, Bishop PE (1988) Bacterial alternative nitrogen-fixation systems. CRC Critical Review in Microbiology 16, 1-14.
62. Kah LC, Lyons TW, Frank TD (2004) Low marine sulphate and protracted oxygenation of the proterozoic biosphere. Nature 431, 834-838.
63. Karl D, Leteller R, Tupas L, Dore J, Christian J, Hebel D (1997) The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature 388, 533-538.
64. Karl D, Michaels A, Bergman B, Capone D, Carpenter E, Letelier R, Lipschultz F, Paerl H, Sigman D, Stal L (2002) Dinitrogen fixation in the world's oceans. Biogeochemistry 57/58, 47-98.
65. Kasting JF, Siefert JL (2001) The nitrogen fix. Nature 412, 26-27.
66. Kasting JF, Siefert JL (2002) Life and the evolution of Earth's atmosphere. Science 296, 1066-1068.
67. Kerry A, Laudenbach DE, Trick CG (1988) Influence of iron limitation and nitrogen-source on growth and siderophore production by cyanobacteria. Journal of Phycology 24, 566-571.
68. Kessler PS, McLarnan J, Leigh JA (1997) Nitrogenase phylogeny and the molybdenum dependence of nitrogen fixation in Methanococcus maripaludis. Journal of Bacteriology 179, 541-543.
69. Kisker C, Schindelin H, Rees DC (1997) Molybdenum-cofactor-containing enzymes: structure and mechanism. Annual Review in Biochemistry 66, 233-267.
70. Kolodny NH, Bauer D, Bryce K, Klucevsek K, Lane A, Medeiros L, Mercer W, Moin S, Park D, Petersen J, Wright J, Yuen C, Wolfson AJ, Allen MM (2006) Effect of nitrogen source on cyanophycin synthesis in Synechocystis sp. strain PCC 6308. Journal of Bacteriology 188, 934-940.
71. Kump LR, Pavlov A, Arthur MA (2005) Massive release of hydrogen sulfide to the surface ocean and atmosphere during intervals of oceanic anoxia. Geology 33, 397-400.
72. Kustka A, Carpenter EJ, Sañudo-Wilhelmy SA (2002) Iron and marine nitrogen fixation: progress and future directions. Research in Microbiology 153, 255-262.
73. Kustka A, Sañudo-Wilhelmy SA, Carpenter EJ, Capone DG, Raven JA (2003) A revised estimate of the iron use efficiency of nitrogen fixation, with special reference to the marine cyanobacterium Trichodesmium spp. (Cyanophyta). Journal of Phycology 39, 12-25.
74. Landing WM, Bruland KW (1987) The contrasting biogeochemistry of iron and manganese in the Pacific Ocean. Geochimica et Cosmochimica Acta 51, 29-43.
75. Lewis BL, Landing WM (1991) The biogeochemistry of manganese and iron in the Black Sea. Deep-Sea Research 38, 773-803.
76. Li H, Sherman DM, Bao SL, Sherman LA (2001) Pattern of cyanophycin accumulation in nitrogen-fixing and non-nitrogen-fixing cyanobacteria. Archives of Microbiology 176, 9-18.
77. Liermann LJ, Guynn RL, Anbar A, Brantley SL (2005) Production of a molybdophore during metal-targeted dissolution of silicates by soil bacteria. Chemical Geology 220, 285-302.
78. Lin SJ, Henze S, Lundgren P, Bergman B, Carpenter EJ (1998) Whole-cell immunolocalization of nitrogenase in marine diazotrophic cyanobacteria, Trichodesmium spp. Applied and Environmental Microbiology 64, 3052-3058.
79. Lobo AL, Zinder SH (1988) Diazotrophy and nitrogenase activity in the Archaebacterium Methanosarcina barkeri 227. Applied and Environmental Microbiology 54, 1656-1661.
80. 2 fixation. American Journal of Science 305, 546-595.
81. Malcolm SJ (1985) Early diagenesis of molybdenum in estuarine sediments. Marine Chemistry 16, 216-225.
82. Marino R, Howarth RW, Shamess J, Prepas E (1990) Molybdenum and sulfate as controls on the abundance of nitrogen-fixing cyanobacteria in saline lakes in Alberta. Limnology and Oceanography 35, 245-259.
83. Marino R, Howarth RW, Chan F, Cole JJ, Likens GE (2003) Sulfate inhibition of molybdenum-dependent nitrogen fixation by planktonic cyanobacteria under seawater conditions: a nonreversible effect. Hydrobiologia 500, 277-293.
84. Martin JH, Gordon RM (1988) Northeast Pacific iron distributions in relation to phytoplankton productivity. Deep-Sea Research 35, 177-196.
85. Martinez-Argudo I, Little R, Shearer N, Johnson P, Dixon R (2004) The NifL-NifA system: a multidomain transcriptional regulatory complex that integrates environmental signals. Journal of Bacteriology 186, 601-610.
86. Miller RW, Eady RR (1988) Molybdenum and vanadium nitrogenases of Azotobacter chroococcum. Biochemistry Journal of 256, 429-432.
87. Miller AF, Orme-Johnson WH (1992) The dependence on iron availability of allocation of iron to nitrogenase components in Klebsiella pneumoniae and Escherichia coli. Journal of Biological Chemistry 267, 9398-9408.
88. Mills MM, Ridame C, Davey M, La Roche J, Geider RJ (2004) Iron and phosphorous co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429, 292-294.
89. 2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean. Nature 430, 1027-1031.
90. Morel FMM, Rueter JG, Anderson DM, Guillard RRL (1979) Aquil: a chemically defined phytoplankton culture medium for trace metal studies. Journal of Phycology 15, 135-141.
91. Morford JL, Emerson S (1999) The geochemistry of redox sensitive trace metals in sediments. Geochimica et Cosmochimica Acta 63, 1735-1750.
92. Navarro-Gonzalez R, McKay CP, Mvondo DN (2001) A possible nitrogen crisis for Archaean life due to reduced nitrogen fixation by lightning. Nature 412, 61-64.
93. Neilands JB (1981) Microbial iron compounds. Annual Review of Biochemistry 50, 715-732.
94. Normand P, Bousquet J (1989) Phylogeny of the nitrogenase sequences in Frankia and other nitrogen-fixing microorganisms. Journal of Molecular Evolution 29, 436-447.
95. 2 fixation by Trichodesmium spp. at the Bermuda Atlantic Time-Series Study (BATS) site. Deep-Sea Research Part II-Topical Studies in Oceanography 48, 1583-1608.
96. 2 fixation in coastal marine waters - relative importance of molybdenum, iron, phosphorus, and organic-matter availability. Limnology and Oceanography 32, 525-536.
97. 2 fixation and growth in natural and cultured populations of the planktonic marine cyanobacteria Trichodesmium spp. Applied and Environmental Microbiology 60, 1044-1047.
98. Paulsen DM, Paerl HW, Bishop PE (1991) Evidence that molybdenum-dependent nitrogen-fixation is not limited by high sulfate concentrations in marine environments. Limnology and Oceanography 36, 1325-1334.
99. 4 in the atmosphere of early Earth. Journal of Geophysical Research-Planets 105, 11981-11990.
100. Postgate JR, Eady RR (1988) The evolution of biological nitrogen fixation. In Nitrogen Fixation: One Hundred Years After (eds Both H, DeBruijn FJ, Newton WE). Fischer, Stuttgart, Germany, pp. 31-40.
101. Poulton SW, Fralick PW, Canfield DE (2004) The transition to a sulphidic ocean ∼1.84 billion years ago. Nature 431, 173-177.
102. Premakumar R, Lemos EM, Bishop PE (1984) Evidence for 2 dinitrogenase reductases under regulatory control by molybdenum in Azotobacter vinelandii. Biochimica et Biophysica Acta 797, 64-70.
103. Raven JA (1988) The iron and molybdenum use efficiencies of plant growth with different energy, carbon and nitrogen sources. New Phytologist 109, 279-287.
104. Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Molecular Biology and Evolution 21, 541-554.
105. Redfield AC, Ketchum BH, Richards FA (1963) The influence of organisms on the composition of sea-water. In The Sea (ed. Hill MN). John Wiley & Sons, pp. 26-77.
106. 2 by a molybdenum-CO dehydrogenase. Journal of Biological Chemistry 272, 26627-26633.
107. Rouxel OJ, Bekker A, Edwards KJ (2005) Iron isotope constraints on the Archean and Paleoproterozoic ocean redox state. Science 307, 1088-1091.
108. Rueter JG (1988) Iron stimulation of photosynthesis and nitrogen fixation in Anabaena 7120 and Trichodesmium (Cyanophyceae). Journal of Phycology 24, 249-254.
109. Rueter JG, Ohki K, Fujita Y (1990) The effect of iron nutrition on photosynthesis and nitrogen fixation in cultures of Trichodesmium (Cyanophyceae). Journal of Phycology 26, 30-35.
110. Rye R, Holland HD (1998) Paleosols and the evolution of atmospheric oxygen: a critical review. American Journal of Science 298, 621-672.
111. Saito MA, Sigman DM, Morel FMM (2003) The bioinorganic chemistry of the ancient ocean: the co-evolution of cyanobacterial metal requirements and biogeochemical cycles at the Archean-Proterozoic boundary? Inorganica Chimica Acta 356, 308-318.
112. Sañudo-Wilhelmy SA, Kustka AB, Gobler CJ, Hutchins DA, Yang M, Lwiza K, Burns J, Capone DG, Raven JA, Carpenter EJ (2001) Phosphorous limitation of nitrogen fixation by Trichodesmium in the central Atlantic Ocean. Nature 411, 66-69.
113. 2 fixation. Proceedings of the National Academy of Sciences of the United States of America 58, 213-216.
114. Shen Y, Canfield DE, Knoll AH (2002) Middle Proterozoic ocean chemistry: evidence from the McArthur Basin, Northern Australia. American Journal of Science 302, 81-109.
115. Shen Y, Knoll AH, Walter MR (2003) Evidence for low sulphate and anoxia in a mid-Proterozoic marine basin. Nature 423, 632-635.
116. Simon RD (1971) Cyanophycin granules from the blue-green alga Anabaena cylindrica: a reserve material consisting of copolymers of aspartic acid and arginine. Proceedings of the National Academy of Sciences of the United States of America 68, 265-267.
117. Sterner RW, Elser JJ (2002) Ecological Stoichiometry: the Biology of Elements from Molecules to the Biosphere. Princeton University Press, Princeton.
118. Sunda WG, Huntsman SA (1995) Iron uptake and growth limitation in oceanic and coastal phytoplankton. Marine Chemistry 50, 189-206.
119. Thiel T (1988) Phosphate-transport and arsenate resistance in the cyanobacterium Anabaena variabilis. Journal of Bacteriology 170, 1143-1147.
120. Thiel T (1993) Characterization of genes for an alternative nitrogenase in the cyanobacterium Anabaena variabilis. Journal of Bacteriology 175, 6276-6286.
121. Thiel T, Pratte B (2001) Effect on heterocyst differentiation of nitrogen fixation in vegetative cells of the cyanobacterium Anabaena variabilis ATCC 29413. Journal of Bacteriology 183, 280-286.
122. Thiel T, Lyons EM, Erker JC, Ernst A (1995) A 2nd nitrogenase in vegetative cells of a heterocyst-forming cyanobacterium. Proceedings of the National Academy of Sciences of the United States of America 92, 9358-9362.
123. Thiel T, Lyons EM, Erker JC (1997) Characterization of genes for a second Mo-dependent nitrogenase in the cyanobacterium Anabaena variabilis. Journal of Bacteriology 179, 5222-5225.
124. Thiel T, Pratte B, Zahalak M (2002) Transport of molybdate in the cyanobacterium Anabaena variabilis ATCC 29413. Archives of Microbiology 179, 50-56.
125. Tomitani A, Knoll AH, Cavanaugh CM, Ohno T (2006) The evolutionary diversification of cyanobacteria: molecular-phylogenetic and paleontological perspectives. Proceedings of the National Academy of Sciences 103, 5442-5447.
126. Tuit C, Waterbury JB, Ravizza G (2004) Diel variation of molybdenum and iron in marine diazotrophic cyanobacteria. Limnology and Oceanography 49, 978-990.
127. Young JPW (1992) Phylogenetic classification of nitrogen-fixing organisms. In Biological Nitrogen Fixation (eds Stacey G, Burris RH, Evans HJ). Chapman & Hall, Routledge, pp. 43-86.
128. Zahalak M, Pratte B, Werth KJ, Thiel T (2004) Molybdate transport and its effect on nitrogen utilization in the cyanobacterium Anabaena variabilis ATCC 29413. Molecular Microbiology 51, 539-549.
129. Zahnle KJ (1986) Photochemistry of methane and the formation of hydrocyanic acid (HCN) in th earth's early atmosphere. Journal of Geophysical Research 91, 2819-2834.
130. Zehr JP, Turner PJ (2001) Nitrogen fixation: nitrogenase genes and gene expression. In Methods in Microbiology, Vol 30 (ed. pp. 271-286.
131. Zehr JP, Mellon M, Braun S, Litaker W, Steppe T, Paerl HW (1995) Diversity of heterotrophic nitrogen-fixation genes in a marine cyanobacterial mat. Applied and Environmental Microbiology 61, 2527-2532.
132. Zehr JP, Mellon MT, Hiorns WD (1997) Phylogeny of cyanobacterial nifH genes: evolutionary implications and potential applications to natural assemblages. Microbiology-UK 143, 1443-1450.
133. Zehr JP, Mellon MT, Zani S (1998) New nitrogen-fixing microorganisms detected in oligotrophic oceans by amplification of nitrogenase (nifH) genes. Applied and Environmental Microbiology 64, 3444-3450.
134. Zehr JP, Carpenter EJ, Villareal TA (2000) New perspectives on nitrogen-fixing microorganisms in tropical and subtropical oceans. Trends in Microbiology 8, 68-73.
135. 2 in the subtropical North Pacific Ocean. Nature 412, 635-638.
136. Zerkle AL, House CH, Brantley SL (2005) Biogeochemical signatures through time as inferred from whole microbial genomes. American Journal of Science 305, 467-502.