Proteorhodopsin photosystem gene expression enables photophosphorylation in a heterologous host

A. Martinez, A. S. Bradley, J. R. Waldbauer, R. E. Summons, E. F. DeLong

Research output: Contribution to journalArticlepeer-review

161 Scopus citations

Abstract

Proteorhodopsins (PRs) are retinal-containing proteins that catalyze light-activated proton efflux across the cell membrane. These photoproteins are known to be globally distributed in the ocean's photic zone, and they are found in a diverse array of Bacteria and Archaea. Recently, light-enhanced growth rates and yields have been reported in at least one PR-containing marine bacterium, but the physiological basis of light-activated growth stimulation has not yet been determined. To describe more fully PR photosystem genetics and biochemistry, we functionally surveyed a marine picoplankton large-insert genomic library for recombinant clones expressing PR photosystems in vivo. Our screening approach exploited transient increases in vector copy number that significantly enhanced the sensitivity of phenotypic detection. Two genetically distinct recombinants, initially identified by their orange pigmentation, expressed a small cluster of genes encoding a complete PR-based photosystem. Genetic and biochemical analyses of transposon mutants verified the function of gene products in the photopigment and opsin biosynthetic pathways. Heterologous expression of six genes, five encoding photopigment biosynthetic proteins and one encoding a PR, generated a fully functional PR photosystem that enabled photophosphorylation in recombinant Escherichia coli cells exposed to light. Our results demonstrate that a single genetic event can result in the acquisition of phototrophic capabilities in an otherwise chemoorganotrophic microorganism, and they explain in part the ubiquity of PR photosystems among diverse microbial taxa.

Original languageEnglish
Pages (from-to)5590-5595
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume104
Issue number13
DOIs
StatePublished - Mar 27 2007

Keywords

  • Lateral gene transfer
  • Marine
  • Metagenomics
  • Photoheterotrophy
  • Rhodopsin

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