Discovery of the first light-dependent protochlorophyllide oxidoreductase in anoxygenic phototrophic bacteria

Marco Kaschner, Anita Loeschcke, Judith Krause, Bui Quang Minh, Achim Heck, Stephan Endres, Vera Svensson, Astrid Wirtz, Arndt von Haeseler, Karl Erich Jaeger, Thomas Drepper, Ulrich Krauss*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

39 Citations (Scopus)

Abstract

Summary: In all photosynthetic organisms, chlorophylls function as light-absorbing photopigments allowing the efficient harvesting of light energy. Chlorophyll biosynthesis recurs in similar ways in anoxygenic phototrophic proteobacteria as well as oxygenic phototrophic cyanobacteria and plants. Here, the biocatalytic conversion of protochlorophyllide to chlorophyllide is catalysed by evolutionary and structurally distinct protochlorophyllide reductases (PORs) in anoxygenic and oxygenic phototrophs. It is commonly assumed that anoxygenic phototrophs only contain oxygen-sensitive dark-operative PORs (DPORs), which catalyse protochlorophyllide reduction independent of the presence of light. In contrast, oxygenic phototrophs additionally (or exclusively) possess oxygen-insensitive but light-dependent PORs (LPORs). Based on this observation it was suggested that light-dependent protochlorophyllide reduction first emerged as a consequence of increased atmospheric oxygen levels caused by oxygenic photosynthesis in cyanobacteria. Here, we provide experimental evidence for the presence of an LPOR in the anoxygenic phototrophic α-proteobacterium Dinoroseobacter shibaeDFL12T. In vitro and in vivo functional assays unequivocally prove light-dependent protochlorophyllide reduction by this enzyme and reveal that LPORs are not restricted to cyanobacteria and plants. Sequence-based phylogenetic analyses reconcile our findings with current hypotheses about the evolution of LPORs by suggesting that the light-dependent enzyme of D. shibaeDFL12T might have been obtained from cyanobacteria by horizontal gene transfer.

Original languageEnglish
Pages (from-to)1066-1078
Number of pages13
JournalMolecular Microbiology
Volume93
Issue number5
DOIs
Publication statusPublished - Sept 2014
Externally publishedYes

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