On the trail of iron uptake in ancestral Cyanobacteria on early Earth

Tristan C Enzingmüller-Bleyl, Joanne S Boden, Achim J Herrmann, Katharina W Ebel, Patricia Sánchez-Baracaldo, Nicole Frankenberg-Dinkel, Michelle M Gehringer*

*Corresponding author for this work

Research output: Contribution to journalArticle (Academic Journal)peer-review

3 Citations (Scopus)
27 Downloads (Pure)

Abstract

Cyanobacteria oxygenated Earth's atmosphere ~2.4 billion years ago, during the Great Oxygenation Event (GOE), through oxygenic photosynthesis. Their high iron requirement was presumably met by high levels of Fe(II) in the anoxic Archean environment. We found that many deeply branching Cyanobacteria, including two Gloeobacter and four Pseudanabaena spp., cannot synthesize the Fe(II) specific transporter, FeoB. Phylogenetic and relaxed molecular clock analyses find evidence that FeoB and the Fe(III) transporters, cFTR1 and FutB, were present in Proterozoic, but not earlier Archaean lineages of Cyanobacteria. Furthermore Pseudanabaena sp. PCC7367, an early diverging marine, benthic strain grown under simulated Archean conditions, constitutively expressed cftr1, even after the addition of Fe(II). Our genetic profiling suggests that, prior to the GOE, ancestral Cyanobacteria may have utilized alternative metal iron transporters such as ZIP, NRAMP, or FicI, and possibly also scavenged exogenous siderophore bound Fe(III), as they only acquired the necessary Fe(II) and Fe(III) transporters during the Proterozoic. Given that Cyanobacteria arose 3.3-3.6 billion years ago, it is possible that limitations in iron uptake may have contributed to the delay in their expansion during the Archean, and hence the oxygenation of the early Earth.

Original languageEnglish
Pages (from-to)776-789
Number of pages14
JournalGeobiology
Volume20
Issue number6
Early online date30 Jul 2022
DOIs
Publication statusPublished - 17 Oct 2022

Bibliographical note

Funding Information:
This project was funded by the German Research Foundation SPP1833, DFG, Grant numbers: GE2558/3‐1 & GE2558/4‐1 awarded to MMG, a University of Bristol Graduate Teaching Scholarship awarded to J.S.B. and a Royal Society University Research Fellowship awarded to P.S‐B. Open Access funding enabled and organized by Projekt DEAL.

Publisher Copyright:
© 2022 The Authors. Geobiology published by John Wiley & Sons Ltd.

Keywords

  • Cyanobacteria/genetics
  • Ferrous Compounds/metabolism
  • Iron/metabolism
  • Oxygen/metabolism
  • Photosynthesis
  • Phylogeny
  • Siderophores

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