Reduced plastid genomes of colorless facultative pathogens Prototheca (Chlorophyta) are retained for membrane transport genes

Abstract Background Plastids are usually involved in photosynthesis, but the secondary loss of this function is a widespread phenomenon in various lineages of algae and plants. In addition to the loss of genes associated with photosynthesis, the plastid genomes of colorless algae are frequently redu...

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Main Authors: Kacper Maciszewski, Gabriela Wilga, Tomasz Jagielski, Zofia Bakuła, Jan Gawor, Robert Gromadka, Anna Karnkowska
Format: Article
Language:English
Published: BMC 2024-12-01
Series:BMC Biology
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Online Access:https://doi.org/10.1186/s12915-024-02089-4
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author Kacper Maciszewski
Gabriela Wilga
Tomasz Jagielski
Zofia Bakuła
Jan Gawor
Robert Gromadka
Anna Karnkowska
author_facet Kacper Maciszewski
Gabriela Wilga
Tomasz Jagielski
Zofia Bakuła
Jan Gawor
Robert Gromadka
Anna Karnkowska
author_sort Kacper Maciszewski
collection DOAJ
description Abstract Background Plastids are usually involved in photosynthesis, but the secondary loss of this function is a widespread phenomenon in various lineages of algae and plants. In addition to the loss of genes associated with photosynthesis, the plastid genomes of colorless algae are frequently reduced further. To understand the pathways of reductive evolution associated with the loss of photosynthesis, it is necessary to study a number of closely related strains. Prototheca, a chlorophyte genus of facultative pathogens, provides an excellent opportunity to study this process with its well-sampled array of diverse colorless strains. Results We have sequenced the plastid genomes of 13 Prototheca strains and reconstructed a comprehensive phylogeny that reveals evolutionary patterns within the genus and among its closest relatives. Our phylogenomic analysis revealed three independent losses of photosynthesis among the Prototheca strains and varied protein-coding gene content in their ptDNA. Despite this diversity, all Prototheca strains retain the same key plastid functions. These include processes related to gene expression, as well as crucial roles in fatty acid and cysteine biosynthesis, and membrane transport. Conclusions The retention of vestigial genomes in colorless plastids is typically associated with the biosynthesis of secondary metabolites. In contrast, the remarkable conservation of plastid membrane transport system components in the nonphotosynthetic genera Prototheca and Helicosporidium provides an additional constraint against the loss of ptDNA in this lineage. Furthermore, these genes can potentially serve as targets for therapeutic intervention, indicating their importance beyond the evolutionary context.
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spelling doaj-art-717008b926eb45d8824544b7d84981a82024-12-22T12:48:03ZengBMCBMC Biology1741-70072024-12-0122111310.1186/s12915-024-02089-4Reduced plastid genomes of colorless facultative pathogens Prototheca (Chlorophyta) are retained for membrane transport genesKacper Maciszewski0Gabriela Wilga1Tomasz Jagielski2Zofia Bakuła3Jan Gawor4Robert Gromadka5Anna Karnkowska6Institute of Evolutionary Biology, Faculty of Biology, Biological and Chemical Research Centre, University of WarsawInstitute of Evolutionary Biology, Faculty of Biology, Biological and Chemical Research Centre, University of WarsawDepartment of Medical Microbiology, Institute of Microbiology, Faculty of Biology, University of WarsawDepartment of Medical Microbiology, Institute of Microbiology, Faculty of Biology, University of WarsawDNA Sequencing and Synthesis Facility, Institute of Biochemistry and Biophysics, Polish Academy of SciencesDNA Sequencing and Synthesis Facility, Institute of Biochemistry and Biophysics, Polish Academy of SciencesInstitute of Evolutionary Biology, Faculty of Biology, Biological and Chemical Research Centre, University of WarsawAbstract Background Plastids are usually involved in photosynthesis, but the secondary loss of this function is a widespread phenomenon in various lineages of algae and plants. In addition to the loss of genes associated with photosynthesis, the plastid genomes of colorless algae are frequently reduced further. To understand the pathways of reductive evolution associated with the loss of photosynthesis, it is necessary to study a number of closely related strains. Prototheca, a chlorophyte genus of facultative pathogens, provides an excellent opportunity to study this process with its well-sampled array of diverse colorless strains. Results We have sequenced the plastid genomes of 13 Prototheca strains and reconstructed a comprehensive phylogeny that reveals evolutionary patterns within the genus and among its closest relatives. Our phylogenomic analysis revealed three independent losses of photosynthesis among the Prototheca strains and varied protein-coding gene content in their ptDNA. Despite this diversity, all Prototheca strains retain the same key plastid functions. These include processes related to gene expression, as well as crucial roles in fatty acid and cysteine biosynthesis, and membrane transport. Conclusions The retention of vestigial genomes in colorless plastids is typically associated with the biosynthesis of secondary metabolites. In contrast, the remarkable conservation of plastid membrane transport system components in the nonphotosynthetic genera Prototheca and Helicosporidium provides an additional constraint against the loss of ptDNA in this lineage. Furthermore, these genes can potentially serve as targets for therapeutic intervention, indicating their importance beyond the evolutionary context.https://doi.org/10.1186/s12915-024-02089-4ProtothecaPlastid genomesColorless plastidsChlorophyta
spellingShingle Kacper Maciszewski
Gabriela Wilga
Tomasz Jagielski
Zofia Bakuła
Jan Gawor
Robert Gromadka
Anna Karnkowska
Reduced plastid genomes of colorless facultative pathogens Prototheca (Chlorophyta) are retained for membrane transport genes
BMC Biology
Prototheca
Plastid genomes
Colorless plastids
Chlorophyta
title Reduced plastid genomes of colorless facultative pathogens Prototheca (Chlorophyta) are retained for membrane transport genes
title_full Reduced plastid genomes of colorless facultative pathogens Prototheca (Chlorophyta) are retained for membrane transport genes
title_fullStr Reduced plastid genomes of colorless facultative pathogens Prototheca (Chlorophyta) are retained for membrane transport genes
title_full_unstemmed Reduced plastid genomes of colorless facultative pathogens Prototheca (Chlorophyta) are retained for membrane transport genes
title_short Reduced plastid genomes of colorless facultative pathogens Prototheca (Chlorophyta) are retained for membrane transport genes
title_sort reduced plastid genomes of colorless facultative pathogens prototheca chlorophyta are retained for membrane transport genes
topic Prototheca
Plastid genomes
Colorless plastids
Chlorophyta
url https://doi.org/10.1186/s12915-024-02089-4
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