Photolysis of iron-siderophore chelates promotes bacterial-algal mutualism

Shady Amin, David H. Green, Mark C. Hart, Frithjof C. Küpper, William G. Sunda, Carl J. Carrano

Research output: Contribution to journalArticle

Abstract

Marine microalgae support world fisheries production and influence climate through various mechanisms. They are also responsible for harmful blooms that adversely impact coastal ecosystems and economies. Optimal growth and survival of many bloom-forming microalgae, including climatically important dinoflagellates and coccolithophores, requires the close association of specific bacterial species, but the reasons for these associations are unknown. Here, we report that several clades of Marinobacter ubiquitously found in close association with dinoflagellates and coccolithophores produce an unusual lower-affinity dicitrate siderophore, vibrioferrin (VF). Fe-VF chelates undergo photolysis at rates that are 10-20 times higher than siderophores produced by free-living marine bacteria, and unlike the latter, the VF photoproduct has no measurable affinity for iron. While both an algal-associated bacterium and a representative dinoflagellate partner, Scrippsiella trochoidea, used iron from Fe-VF chelates in the dark, in situ photolysis of the chelates in the presence of attenuated sunlight increased bacterial iron uptake by 70% and algal uptake by >20-fold. These results suggest that the bacteria promote algal assimilation of iron by facilitating photochemical redox cycling of this critical nutrient. Also, binary culture experiments and genomic evidence suggest that the algal cells release organic molecules that are used by the bacteria for growth. Such mutualistic sharing of iron and fixed carbon has important implications toward our understanding of the close beneficial interactions between marine bacteria and phytoplankton, and the effect of these interactions on algal blooms and climate.

Original languageEnglish (US)
Pages (from-to)17071-17076
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume106
Issue number40
DOIs
StatePublished - Oct 6 2009

Fingerprint

Iron Chelating Agents
Siderophores
Symbiosis
Photolysis
Dinoflagellida
Iron
Bacteria
Microalgae
Climate
Marinobacter
Eutrophication
Phytoplankton
Fisheries
Sunlight
Growth
Oxidation-Reduction
Ecosystem
Carbon
Food
vibrioferrin

Keywords

  • Algal blooms
  • Iron acquisition
  • Marinobacter
  • Photochemistry
  • Vibrioferrin

ASJC Scopus subject areas

  • General

Cite this

Photolysis of iron-siderophore chelates promotes bacterial-algal mutualism. / Amin, Shady; Green, David H.; Hart, Mark C.; Küpper, Frithjof C.; Sunda, William G.; Carrano, Carl J.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 106, No. 40, 06.10.2009, p. 17071-17076.

Research output: Contribution to journalArticle

Amin, Shady ; Green, David H. ; Hart, Mark C. ; Küpper, Frithjof C. ; Sunda, William G. ; Carrano, Carl J. / Photolysis of iron-siderophore chelates promotes bacterial-algal mutualism. In: Proceedings of the National Academy of Sciences of the United States of America. 2009 ; Vol. 106, No. 40. pp. 17071-17076.
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