Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites

The eukaryotic phylum Apicomplexa encompasses thousands of obligate intracellular parasites of humans and animals with immense socio-economic and health impacts. We sequenced nuclear genomes of Chromera velia and Vitrella brassicaformis, free-living non-parasitic photosynthetic algae closely related...

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Published ineLife Vol. 4; p. e06974
Main Authors Woo, Yong H, Ansari, Hifzur, Otto, Thomas D, Klinger, Christen M, Kolisko, Martin, Michálek, Jan, Saxena, Alka, Shanmugam, Dhanasekaran, Tayyrov, Annageldi, Veluchamy, Alaguraj, Ali, Shahjahan, Bernal, Axel, del Campo, Javier, Cihlář, Jaromír, Flegontov, Pavel, Gornik, Sebastian G, Hajdušková, Eva, Horák, Aleš, Janouškovec, Jan, Katris, Nicholas J, Mast, Fred D, Miranda-Saavedra, Diego, Mourier, Tobias, Naeem, Raeece, Nair, Mridul, Panigrahi, Aswini K, Rawlings, Neil D, Padron-Regalado, Eriko, Ramaprasad, Abhinay, Samad, Nadira, Tomčala, Aleš, Wilkes, Jon, Neafsey, Daniel E, Doerig, Christian, Bowler, Chris, Keeling, Patrick J, Roos, David S, Dacks, Joel B, Templeton, Thomas J, Waller, Ross F, Lukeš, Julius, Oborník, Miroslav, Pain, Arnab
Format Journal Article
LanguageEnglish
Published England eLife Sciences Publications Ltd 15.07.2015
eLife Sciences Publications, Ltd
Subjects
Algae
Alveolata - genetics
Apicomplexa
Biology
Chromera velia
College campuses
Deoxyribonucleic acid
DNA
DNA, Algal - chemistry
DNA, Algal - genetics
Environmental conditions
evolution of parasitism
Evolution, Molecular
Flagella
Gene expression
Gene Expression Profiling
Genes
Genomes
Genomics
Genomics and Evolutionary Biology
Intracellular
Laboratories
malaria
Metabolic pathways
Microbiology and Infectious Disease
Molecular Sequence Data
Parasites
Parasitism
Parasitology
Phylogenetics
Plasmodium
Protein families
Reptiles & amphibians
Ribonucleic acid
RNA
RNA-binding protein
Science
Sequence Analysis, DNA
toxoplasmosis
Vitrella brassicaformis
Chromera velia
evolutionary biology
infectious disease
toxoplasmosis
evolution of parasitism
Vitrella brassicaformis
microbiology
genomics
malaria
Online AccessGet full text

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Abstract The eukaryotic phylum Apicomplexa encompasses thousands of obligate intracellular parasites of humans and animals with immense socio-economic and health impacts. We sequenced nuclear genomes of Chromera velia and Vitrella brassicaformis, free-living non-parasitic photosynthetic algae closely related to apicomplexans. Proteins from key metabolic pathways and from the endomembrane trafficking systems associated with a free-living lifestyle have been progressively and non-randomly lost during adaptation to parasitism. The free-living ancestor contained a broad repertoire of genes many of which were repurposed for parasitic processes, such as extracellular proteins, components of a motility apparatus, and DNA- and RNA-binding protein families. Based on transcriptome analyses across 36 environmental conditions, Chromera orthologs of apicomplexan invasion-related motility genes were co-regulated with genes encoding the flagellar apparatus, supporting the functional contribution of flagella to the evolution of invasion machinery. This study provides insights into how obligate parasites with diverse life strategies arose from a once free-living phototrophic marine alga.
AbstractList The eukaryotic phylum Apicomplexa encompasses thousands of obligate intracellular parasites of humans and animals with immense socio-economic and health impacts. We sequenced nuclear genomes of Chromera velia and Vitrella brassicaformis, free-living non-parasitic photosynthetic algae closely related to apicomplexans. Proteins from key metabolic pathways and from the endomembrane trafficking systems associated with a free-living lifestyle have been progressively and non-randomly lost during adaptation to parasitism. The free-living ancestor contained a broad repertoire of genes many of which were repurposed for parasitic processes, such as extracellular proteins, components of a motility apparatus, and DNA- and RNA-binding protein families. Based on transcriptome analyses across 36 environmental conditions, Chromera orthologs of apicomplexan invasion-related motility genes were co-regulated with genes encoding the flagellar apparatus, supporting the functional contribution of flagella to the evolution of invasion machinery. This study provides insights into how obligate parasites with diverse life strategies arose from a once free-living phototrophic marine alga.
The eukaryotic phylum Apicomplexa encompasses thousands of obligate intracellular parasites of humans and animals with immense socio-economic and health impacts. We sequenced nuclear genomes of Chromera velia and Vitrella brassicaformis, free-living non-parasitic photosynthetic algae closely related to apicomplexans. Proteins from key metabolic pathways and from the endomembrane trafficking systems associated with a free-living lifestyle have been progressively and non-randomly lost during adaptation to parasitism. The free-living ancestor contained a broad repertoire of genes many of which were repurposed for parasitic processes, such as extracellular proteins, components of a motility apparatus, and DNA- and RNA-binding protein families. Based on transcriptome analyses across 36 environmental conditions, Chromera orthologs of apicomplexan invasion-related motility genes were co-regulated with genes encoding the flagellar apparatus, supporting the functional contribution of flagella to the evolution of invasion machinery. This study provides insights into how obligate parasites with diverse life strategies arose from a once free-living phototrophic marine alga. Single-celled parasites cause many severe diseases in humans and animals. The apicomplexans form probably the most successful group of these parasites and include the parasites that cause malaria. Apicomplexans infect a broad range of hosts, including humans, reptiles, birds, and insects, and often have complicated life cycles. For example, the malaria-causing parasites spread by moving from humans to female mosquitoes and then back to humans. Despite significant differences amongst apicomplexans, these single-celled parasites also share a number of features that are not seen in other living species. How and when these features arose remains unclear. It is known from previous work that apicomplexans are closely related to single-celled algae. But unlike apicomplexans, which depend on a host animal to survive, these algae live freely in their environment, often in close association with corals. Woo et al. have now sequenced the genomes of two photosynthetic algae that are thought to be close living relatives of the apicomplexans. These genomes were then compared to each other and to the genomes of other algae and apicomplexans. These comparisons reconfirmed that the two algae that were studied were close relatives of the apicomplexans. Further analyses suggested that thousands of genes were lost as an ancient free-living algae evolved into the apicomplexan ancestor, and further losses occurred as these early parasites evolved into modern species. The lost genes were typically those that are important for free-living organisms, but are either a hindrance to, or not needed in, a parasitic lifestyle. Some of the ancestor's genes, especially those that coded for the building blocks of flagella (structures which free-living algae use to move around), were repurposed in ways that helped the apicomplexans to invade their hosts. Understanding this repurposing process in greater detail will help to identify key molecules in these deadly parasites that could be targeted by drug treatments. It will also offer answers to one of the most fascinating questions in evolutionary biology: how parasites have evolved from free-living organisms.
The eukaryotic phylum Apicomplexa encompasses thousands of obligate intracellular parasites of humans and animals with immense socio-economic and health impacts. We sequenced nuclear genomes of Chromera velia and Vitrella brassicaformis, free-living non-parasitic photosynthetic algae closely related to apicomplexans. Proteins from key metabolic pathways and from the endomembrane trafficking systems associated with a free-living lifestyle have been progressively and non-randomly lost during adaptation to parasitism. The free-living ancestor contained a broad repertoire of genes many of which were repurposed for parasitic processes, such as extracellular proteins, components of a motility apparatus, and DNA- and RNA-binding protein families. Based on transcriptome analyses across 36 environmental conditions, Chromera orthologs of apicomplexan invasion-related motility genes were co-regulated with genes encoding the flagellar apparatus, supporting the functional contribution of flagella to the evolution of invasion machinery. This study provides insights into how obligate parasites with diverse life strategies arose from a once free-living phototrophic marine alga.DOI: http://dx.doi.org/10.7554/eLife.06974.001
The eukaryotic phylum Apicomplexa encompasses thousands of obligate intracellular parasites of humans and animals with immense socio-economic and health impacts. We sequenced nuclear genomes of Chromera velia and Vitrella brassicaformis , free-living non-parasitic photosynthetic algae closely related to apicomplexans. Proteins from key metabolic pathways and from the endomembrane trafficking systems associated with a free-living lifestyle have been progressively and non-randomly lost during adaptation to parasitism. The free-living ancestor contained a broad repertoire of genes many of which were repurposed for parasitic processes, such as extracellular proteins, components of a motility apparatus, and DNA- and RNA-binding protein families. Based on transcriptome analyses across 36 environmental conditions, Chromera orthologs of apicomplexan invasion-related motility genes were co-regulated with genes encoding the flagellar apparatus, supporting the functional contribution of flagella to the evolution of invasion machinery. This study provides insights into how obligate parasites with diverse life strategies arose from a once free-living phototrophic marine alga. DOI: http://dx.doi.org/10.7554/eLife.06974.001 Single-celled parasites cause many severe diseases in humans and animals. The apicomplexans form probably the most successful group of these parasites and include the parasites that cause malaria. Apicomplexans infect a broad range of hosts, including humans, reptiles, birds, and insects, and often have complicated life cycles. For example, the malaria-causing parasites spread by moving from humans to female mosquitoes and then back to humans. Despite significant differences amongst apicomplexans, these single-celled parasites also share a number of features that are not seen in other living species. How and when these features arose remains unclear. It is known from previous work that apicomplexans are closely related to single-celled algae. But unlike apicomplexans, which depend on a host animal to survive, these algae live freely in their environment, often in close association with corals. Woo et al. have now sequenced the genomes of two photosynthetic algae that are thought to be close living relatives of the apicomplexans. These genomes were then compared to each other and to the genomes of other algae and apicomplexans. These comparisons reconfirmed that the two algae that were studied were close relatives of the apicomplexans. Further analyses suggested that thousands of genes were lost as an ancient free-living algae evolved into the apicomplexan ancestor, and further losses occurred as these early parasites evolved into modern species. The lost genes were typically those that are important for free-living organisms, but are either a hindrance to, or not needed in, a parasitic lifestyle. Some of the ancestor's genes, especially those that coded for the building blocks of flagella (structures which free-living algae use to move around), were repurposed in ways that helped the apicomplexans to invade their hosts. Understanding this repurposing process in greater detail will help to identify key molecules in these deadly parasites that could be targeted by drug treatments. It will also offer answers to one of the most fascinating questions in evolutionary biology: how parasites have evolved from free-living organisms. DOI: http://dx.doi.org/10.7554/eLife.06974.002
Author Saxena, Alka
Mast, Fred D
Oborník, Miroslav
Neafsey, Daniel E
Tomčala, Aleš
Samad, Nadira
Michálek, Jan
Veluchamy, Alaguraj
Klinger, Christen M
del Campo, Javier
Horák, Aleš
Templeton, Thomas J
Lukeš, Julius
Flegontov, Pavel
Otto, Thomas D
Wilkes, Jon
Tayyrov, Annageldi
Kolisko, Martin
Bowler, Chris
Panigrahi, Aswini K
Mourier, Tobias
Naeem, Raeece
Roos, David S
Nair, Mridul
Pain, Arnab
Shanmugam, Dhanasekaran
Ali, Shahjahan
Woo, Yong H
Doerig, Christian
Gornik, Sebastian G
Janouškovec, Jan
Cihlář, Jaromír
Bernal, Axel
Waller, Ross F
Padron-Regalado, Eriko
Ramaprasad, Abhinay
Hajdušková, Eva
Keeling, Patrick J
Katris, Nicholas J
Miranda-Saavedra, Diego
Rawlings, Neil D
Dacks, Joel B
Ansari, Hifzur
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/26175406$$D View this record in MEDLINE/PubMed
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Keywords Chromera velia
evolutionary biology
infectious disease
toxoplasmosis
evolution of parasitism
Vitrella brassicaformis
microbiology
genomics
malaria
Language English
License http://creativecommons.org/licenses/by/4.0
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Notes These authors contributed equally to this work.
Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research institute, Seattle, United States.
Biological and Environmental Sciences and Engineering Division, Center for Desert Agriculture, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
The Samuel Roberts Noble Foundation, Ardmore, United States.
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0000-0002-0338-6493
0000-0002-1755-2819
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Snippet The eukaryotic phylum Apicomplexa encompasses thousands of obligate intracellular parasites of humans and animals with immense socio-economic and health...
The eukaryotic phylum Apicomplexa encompasses thousands of obligate intracellular parasites of humans and animals with immense socio-economic and health...
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StartPage e06974
SubjectTerms Algae
Alveolata - genetics
Apicomplexa
Biology
Chromera velia
College campuses
Deoxyribonucleic acid
DNA
DNA, Algal - chemistry
DNA, Algal - genetics
Environmental conditions
evolution of parasitism
Evolution, Molecular
Flagella
Gene expression
Gene Expression Profiling
Genes
Genomes
Genomics
Genomics and Evolutionary Biology
Intracellular
Laboratories
malaria
Metabolic pathways
Microbiology and Infectious Disease
Molecular Sequence Data
Parasites
Parasitism
Parasitology
Phylogenetics
Plasmodium
Protein families
Reptiles & amphibians
Ribonucleic acid
RNA
RNA-binding protein
Science
Sequence Analysis, DNA
toxoplasmosis
Vitrella brassicaformis
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Title Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites
URI https://www.ncbi.nlm.nih.gov/pubmed/26175406
https://www.proquest.com/docview/1966515862
https://pubmed.ncbi.nlm.nih.gov/PMC4501334
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Volume 4
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