Cited by 149Paleontology and Stratigraphy of FossilsMetalloenzymes and iron-sulfur proteinsMarine and coastal ecosystems

Metal limitation of cyanobacterial N2fixation and implications for the Precambrian nitrogen cycle

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ZERKLE, A. L., HOUSE, C. H., COX, R. P., CANFIELD, D. E.·2006·Geobiology

Abstract

ABSTRACT Nitrogen fixation is a critical part of the global nitrogen cycle, replacing biologically available reduced nitrogen lost by denitrification. The redox‐sensitive trace metals Fe and Mo are key components of the primary nitrogenase enzyme used by cyanobacteria (and other prokaryotes) to fix atmospheric N2into bioessential compounds. Progressive oxygenation of the Earth's atmosphere has forced changes in the redox state of the oceans through geologic time, from anoxic Fe‐enriched waters in the Archean to partially sulfidic deep waters by the mid‐Proterozoic. This development of ocean redox chemistry during the Precambrian led to fluctuations in Fe and Mo availability that could have significantly impacted the ability of prokaryotes to fix nitrogen. It has been suggested that metal limitation of nitrogen fixation and nitrate assimilation, along with increased rates of denitrification, could have resulted in globally reduced rates of primary production and nitrogen‐starved oceans through much of the Proterozoic. To test the first part of this hypothesis, we grew N2‐fixing cyanobacteria in cultures with metal concentrations reflecting an anoxic Archean ocean (high Fe, low Mo), a sulfidic Proterozoic ocean (low Fe, moderate Mo), and an oxic Phanerozoic ocean (low Fe, high Mo). We measured low rates of cellular N2fixation under [Fe] and [Mo] estimated for the Archean ocean. With decreased [Fe] and higher [Mo] representing sulfidic Proterozoic conditions, N2fixation, growth, and biomass C:N were similar to those observed with metal concentrations of the fully oxygenated oceans that likely developed in the Phanerozoic. Our results raise the possibility that an initial rise in atmospheric oxygen could actually have enhanced nitrogen fixation rates to near modern marine levels, providing that phosphate was available and rising O2levels did not markedly inhibit nitrogenase activity.

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Crossref · 10.1111/j.1472-4669.2006.00082.x

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  • This scenario is supported by culture studies of Zerkle et al. (2006) and Glass et al. (2009).

    “This is a scenario supported by the culture studies of Zerkle et al. (2006) and Glass et al. (2009).”

    From Trace elements at the intersection of marine biological and geochemical evolution (2016) · cites this paper as Zerkle et al., 2006

  • Zerkle et al. (2006) and Glass et al. (2009) have shown that very low Mo concentrations can support near modern levels of nitrogen fixation.

    “although Zerkle et al. (2006) and Glass et al. (2009) have both shown that very low Mo concentrations are capable of supporting near modern levels of nitrogen fixation.”

    From Trace elements at the intersection of marine biological and geochemical evolution (2016) · cites this paper as Zerkle et al., 2006

  • In laboratory cultures with freshwater cyanobacteria, Zerkle et al. (2006) suggest nitrogen assimilation through molybdenum-nitrogenase can occur at Mo levels as low as 5 nM, suggesting these enzymes can be active over a broad range of concentrations.

    “In laboratory cultures with freshwater cyanobacteria, Zerkle et al. (2006) suggest that nitrogen assimilation through molybdenum-nitrogenase can occur at Mo levels as low as 5 nM, suggesting that these enzymes can be active over a broad range of concentrations.”

    From Trace elements at the intersection of marine biological and geochemical evolution (2016) · cites this paper as Zerkle et al., 2006

  • Mo-nitrogenase activity at very low Mo levels is physiologically consistent with culture studies.

    “This would be physiologically consistent with observations of Mo-nitrogenase activity at very low Mo levels in culture studies”

    From Trace elements at the intersection of marine biological and geochemical evolution (2016) · cites this paper as Zerkle et al., 2006

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Research works printed but not linked: 7

  1. Frausto da Silva JJR, Williams RJP (2001) The Biological Chemistry of the Elements. Oxford University Press, New York.
  2. Miller RW, Eady RR (1988) Molybdenum and vanadium nitrogenases of Azotobacter chroococcum. Biochemistry Journal of 256, 429 -432.
  3. 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.
  4. 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.
  5. 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.
  6. 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.
  7. Zerkle AL, House CH, Brantley SL (2005) Biogeochemical signatures through time as inferred from whole microbial genomes. American Journal of Science 305, 467 -502.

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Authors
ZERKLE, A. L., HOUSE, C. H., COX, R. P., & CANFIELD, D. E.
Affiliations
  • Pennsylvania State University (US)
  • University of Southern Denmark (DK)
Corresponding author
ZERKLE, A. L.
Venue
Geobiology
Publisher
Wiley
Published
2006-10-16
Volume
4
Issue
4
Pages
285-297
ISSN
  • 1472-4669 (ISSN-L)
  • 1472-4677
OpenAlex
W1991117724
Cited by
149
References
138
Citations by year
2026: 5 · 2025: 13 · 2024: 11 · 2023: 7 · 2022: 2 · 2021: 5 · 2020: 8 · 2019: 7 · 2018: 7 · 2017: 13 · 2016: 12 · 2015: 8 · 2014: 4 · 2013: 9 · 2012: 7
FWCI
4.49
Type
journal article
Language
en
Open access
Locations
  • Geobiology (publishedVersion)
  • University of Southern Denmark Research Portal (University of Southern Denmark) (submittedVersion)
Funders
  • National Science Foundation (9972759)
  • National Aeronautics and Space Administration
  • University of Pennsylvania
  • Pennsylvania State University
  • NASA Astrobiology Institute (DGE-9972759)
Topics
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Stratigraphy of Fossils
  • Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Metalloenzymes and iron-sulfur proteins
  • Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine and coastal ecosystems
Keywords
nitrogen fixation, cyanobacteria, metal limitation, iron, molybdenum, nitrogenase, Archean ocean, atmospheric oxygenation, denitrification, nitrate assimilation, ocean anoxia

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