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Complex Evolution of Light-Dependent Protochlorophyllide Oxidoreductases in Aerobic Anoxygenic Phototrophs: Origin, Phylogeny, and Function

Light-dependent protochlorophyllide oxidoreductase (LPOR) and dark-operative protochlorophyllide oxidoreductase are evolutionary and structurally distinct enzymes that are essential for the synthesis of (bacterio)chlorophyll, the primary pigment needed for both anoxygenic and oxygenic photosynthesis...

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Autores principales: Chernomor, Olga, Peters, Lena, Schneidewind, Judith, Loeschcke, Anita, Knieps-Grünhagen, Esther, Schmitz, Fabian, von Lieres, Eric, Kutta, Roger Jan, Svensson, Vera, Jaeger, Karl-Erich, Drepper, Thomas, von Haeseler, Arndt, Krauss, Ulrich
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7947762/
https://www.ncbi.nlm.nih.gov/pubmed/32931580
http://dx.doi.org/10.1093/molbev/msaa234
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author Chernomor, Olga
Peters, Lena
Schneidewind, Judith
Loeschcke, Anita
Knieps-Grünhagen, Esther
Schmitz, Fabian
von Lieres, Eric
Kutta, Roger Jan
Svensson, Vera
Jaeger, Karl-Erich
Drepper, Thomas
von Haeseler, Arndt
Krauss, Ulrich
author_facet Chernomor, Olga
Peters, Lena
Schneidewind, Judith
Loeschcke, Anita
Knieps-Grünhagen, Esther
Schmitz, Fabian
von Lieres, Eric
Kutta, Roger Jan
Svensson, Vera
Jaeger, Karl-Erich
Drepper, Thomas
von Haeseler, Arndt
Krauss, Ulrich
author_sort Chernomor, Olga
collection PubMed
description Light-dependent protochlorophyllide oxidoreductase (LPOR) and dark-operative protochlorophyllide oxidoreductase are evolutionary and structurally distinct enzymes that are essential for the synthesis of (bacterio)chlorophyll, the primary pigment needed for both anoxygenic and oxygenic photosynthesis. In contrast to the long-held hypothesis that LPORs are only present in oxygenic phototrophs, we recently identified a functional LPOR in the aerobic anoxygenic phototrophic bacterium (AAPB) Dinoroseobacter shibae and attributed its presence to a single horizontal gene transfer event from cyanobacteria. Here, we provide evidence for the more widespread presence of genuine LPOR enzymes in AAPBs. An exhaustive bioinformatics search identified 36 putative LPORs outside of oxygenic phototrophic bacteria (cyanobacteria) with the majority being AAPBs. Using in vitro and in vivo assays, we show that the large majority of the tested AAPB enzymes are genuine LPORs. Solution structural analyses, performed for two of the AAPB LPORs, revealed a globally conserved structure when compared with a well-characterized cyanobacterial LPOR. Phylogenetic analyses suggest that LPORs were transferred not only from cyanobacteria but also subsequently between proteobacteria and from proteobacteria to Gemmatimonadetes. Our study thus provides another interesting example for the complex evolutionary processes that govern the evolution of bacteria, involving multiple horizontal gene transfer events that likely occurred at different time points and involved different donors.
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spelling pubmed-79477622021-03-16 Complex Evolution of Light-Dependent Protochlorophyllide Oxidoreductases in Aerobic Anoxygenic Phototrophs: Origin, Phylogeny, and Function Chernomor, Olga Peters, Lena Schneidewind, Judith Loeschcke, Anita Knieps-Grünhagen, Esther Schmitz, Fabian von Lieres, Eric Kutta, Roger Jan Svensson, Vera Jaeger, Karl-Erich Drepper, Thomas von Haeseler, Arndt Krauss, Ulrich Mol Biol Evol Discoveries Light-dependent protochlorophyllide oxidoreductase (LPOR) and dark-operative protochlorophyllide oxidoreductase are evolutionary and structurally distinct enzymes that are essential for the synthesis of (bacterio)chlorophyll, the primary pigment needed for both anoxygenic and oxygenic photosynthesis. In contrast to the long-held hypothesis that LPORs are only present in oxygenic phototrophs, we recently identified a functional LPOR in the aerobic anoxygenic phototrophic bacterium (AAPB) Dinoroseobacter shibae and attributed its presence to a single horizontal gene transfer event from cyanobacteria. Here, we provide evidence for the more widespread presence of genuine LPOR enzymes in AAPBs. An exhaustive bioinformatics search identified 36 putative LPORs outside of oxygenic phototrophic bacteria (cyanobacteria) with the majority being AAPBs. Using in vitro and in vivo assays, we show that the large majority of the tested AAPB enzymes are genuine LPORs. Solution structural analyses, performed for two of the AAPB LPORs, revealed a globally conserved structure when compared with a well-characterized cyanobacterial LPOR. Phylogenetic analyses suggest that LPORs were transferred not only from cyanobacteria but also subsequently between proteobacteria and from proteobacteria to Gemmatimonadetes. Our study thus provides another interesting example for the complex evolutionary processes that govern the evolution of bacteria, involving multiple horizontal gene transfer events that likely occurred at different time points and involved different donors. Oxford University Press 2020-09-15 /pmc/articles/PMC7947762/ /pubmed/32931580 http://dx.doi.org/10.1093/molbev/msaa234 Text en © The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Discoveries
Chernomor, Olga
Peters, Lena
Schneidewind, Judith
Loeschcke, Anita
Knieps-Grünhagen, Esther
Schmitz, Fabian
von Lieres, Eric
Kutta, Roger Jan
Svensson, Vera
Jaeger, Karl-Erich
Drepper, Thomas
von Haeseler, Arndt
Krauss, Ulrich
Complex Evolution of Light-Dependent Protochlorophyllide Oxidoreductases in Aerobic Anoxygenic Phototrophs: Origin, Phylogeny, and Function
title Complex Evolution of Light-Dependent Protochlorophyllide Oxidoreductases in Aerobic Anoxygenic Phototrophs: Origin, Phylogeny, and Function
title_full Complex Evolution of Light-Dependent Protochlorophyllide Oxidoreductases in Aerobic Anoxygenic Phototrophs: Origin, Phylogeny, and Function
title_fullStr Complex Evolution of Light-Dependent Protochlorophyllide Oxidoreductases in Aerobic Anoxygenic Phototrophs: Origin, Phylogeny, and Function
title_full_unstemmed Complex Evolution of Light-Dependent Protochlorophyllide Oxidoreductases in Aerobic Anoxygenic Phototrophs: Origin, Phylogeny, and Function
title_short Complex Evolution of Light-Dependent Protochlorophyllide Oxidoreductases in Aerobic Anoxygenic Phototrophs: Origin, Phylogeny, and Function
title_sort complex evolution of light-dependent protochlorophyllide oxidoreductases in aerobic anoxygenic phototrophs: origin, phylogeny, and function
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7947762/
https://www.ncbi.nlm.nih.gov/pubmed/32931580
http://dx.doi.org/10.1093/molbev/msaa234
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