Single-Cell Transcriptomics Reveal a Correlation between Genome Architecture and Gene Family Evolution in Ciliates

ABSTRACT Ciliates, a eukaryotic clade that is over 1 billion years old, are defined by division of genome function between transcriptionally inactive germline micronuclei and functional somatic macronuclei. To date, most analyses of gene family evolution have been limited to cultivable model lineage...

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Autores principales:	Ying Yan, Xyrus X. Maurer-Alcalá, Rob Knight, Sergei L. Kosakovsky Pond, Laura A. Katz
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	transcriptomics gene family evolution genetic code evolution phylogenomics Ciliophora uncultivable microbes Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/13f22fde26c34e10b225d8b3ec3aa544
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spelling	oai:doaj.org-article:13f22fde26c34e10b225d8b3ec3aa5442021-11-15T15:54:45ZSingle-Cell Transcriptomics Reveal a Correlation between Genome Architecture and Gene Family Evolution in Ciliates10.1128/mBio.02524-192150-7511https://doaj.org/article/13f22fde26c34e10b225d8b3ec3aa5442019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02524-19https://doaj.org/toc/2150-7511ABSTRACT Ciliates, a eukaryotic clade that is over 1 billion years old, are defined by division of genome function between transcriptionally inactive germline micronuclei and functional somatic macronuclei. To date, most analyses of gene family evolution have been limited to cultivable model lineages (e.g., Tetrahymena, Paramecium, Oxytricha, and Stylonychia). Here, we focus on the uncultivable Karyorelictea and its understudied sister class Heterotrichea, which represent two extremes in genome architecture. Somatic macronuclei within the Karyorelictea are described as nearly diploid, while the Heterotrichea have hyperpolyploid somatic genomes. Previous analyses indicate that genome architecture impacts ciliate gene family evolution as the most diverse and largest gene families are found in lineages with extensively processed somatic genomes (i.e., possessing thousands of gene-sized chromosomes). To further assess ciliate gene family evolution, we analyzed 43 single-cell transcriptomes from 33 ciliate species representing 10 classes. Focusing on conserved eukaryotic genes, we use estimates of transcript diversity as a proxy for the number of paralogs in gene families among four focal clades: Karyorelictea, Heterotrichea, extensive fragmenters (with gene-size somatic chromosomes), and non-extensive fragmenters (with more traditional somatic chromosomes), the latter two within the subphylum Intramacronucleata. Our results show that (i) the Karyorelictea have the lowest average transcript diversity, while Heterotrichea are highest among the four groups; (ii) proteins in Karyorelictea are under the highest functional constraints, and the patterns of selection in ciliates may reflect genome architecture; and (iii) stop codon reassignments vary among members of the Heterotrichea and Spirotrichea but are conserved in other classes. IMPORTANCE To further our understanding of genome evolution in eukaryotes, we assess the relationship between patterns of molecular evolution within gene families and variable genome structures found among ciliates. We combine single-cell transcriptomics with bioinformatic tools, focusing on understudied and uncultivable lineages selected from across the ciliate tree of life. Our analyses show that genome architecture correlates with patterns of protein evolution as lineages with more canonical somatic genomes, such as the class Karyorelictea, have more conserved patterns of molecular evolution compared to other classes. This study showcases the power of single-cell transcriptomics for investigating genome architecture and evolution in uncultivable microbial lineages and provides transcriptomic resources for further research on genome evolution.Ying YanXyrus X. Maurer-AlcaláRob KnightSergei L. Kosakovsky PondLaura A. KatzAmerican Society for Microbiologyarticletranscriptomicsgene family evolutiongenetic code evolutionphylogenomicsCiliophorauncultivable microbesMicrobiologyQR1-502ENmBio, Vol 10, Iss 6 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	transcriptomics gene family evolution genetic code evolution phylogenomics Ciliophora uncultivable microbes Microbiology QR1-502
spellingShingle	transcriptomics gene family evolution genetic code evolution phylogenomics Ciliophora uncultivable microbes Microbiology QR1-502 Ying Yan Xyrus X. Maurer-Alcalá Rob Knight Sergei L. Kosakovsky Pond Laura A. Katz Single-Cell Transcriptomics Reveal a Correlation between Genome Architecture and Gene Family Evolution in Ciliates
description	ABSTRACT Ciliates, a eukaryotic clade that is over 1 billion years old, are defined by division of genome function between transcriptionally inactive germline micronuclei and functional somatic macronuclei. To date, most analyses of gene family evolution have been limited to cultivable model lineages (e.g., Tetrahymena, Paramecium, Oxytricha, and Stylonychia). Here, we focus on the uncultivable Karyorelictea and its understudied sister class Heterotrichea, which represent two extremes in genome architecture. Somatic macronuclei within the Karyorelictea are described as nearly diploid, while the Heterotrichea have hyperpolyploid somatic genomes. Previous analyses indicate that genome architecture impacts ciliate gene family evolution as the most diverse and largest gene families are found in lineages with extensively processed somatic genomes (i.e., possessing thousands of gene-sized chromosomes). To further assess ciliate gene family evolution, we analyzed 43 single-cell transcriptomes from 33 ciliate species representing 10 classes. Focusing on conserved eukaryotic genes, we use estimates of transcript diversity as a proxy for the number of paralogs in gene families among four focal clades: Karyorelictea, Heterotrichea, extensive fragmenters (with gene-size somatic chromosomes), and non-extensive fragmenters (with more traditional somatic chromosomes), the latter two within the subphylum Intramacronucleata. Our results show that (i) the Karyorelictea have the lowest average transcript diversity, while Heterotrichea are highest among the four groups; (ii) proteins in Karyorelictea are under the highest functional constraints, and the patterns of selection in ciliates may reflect genome architecture; and (iii) stop codon reassignments vary among members of the Heterotrichea and Spirotrichea but are conserved in other classes. IMPORTANCE To further our understanding of genome evolution in eukaryotes, we assess the relationship between patterns of molecular evolution within gene families and variable genome structures found among ciliates. We combine single-cell transcriptomics with bioinformatic tools, focusing on understudied and uncultivable lineages selected from across the ciliate tree of life. Our analyses show that genome architecture correlates with patterns of protein evolution as lineages with more canonical somatic genomes, such as the class Karyorelictea, have more conserved patterns of molecular evolution compared to other classes. This study showcases the power of single-cell transcriptomics for investigating genome architecture and evolution in uncultivable microbial lineages and provides transcriptomic resources for further research on genome evolution.
format	article
author	Ying Yan Xyrus X. Maurer-Alcalá Rob Knight Sergei L. Kosakovsky Pond Laura A. Katz
author_facet	Ying Yan Xyrus X. Maurer-Alcalá Rob Knight Sergei L. Kosakovsky Pond Laura A. Katz
author_sort	Ying Yan
title	Single-Cell Transcriptomics Reveal a Correlation between Genome Architecture and Gene Family Evolution in Ciliates
title_short	Single-Cell Transcriptomics Reveal a Correlation between Genome Architecture and Gene Family Evolution in Ciliates
title_full	Single-Cell Transcriptomics Reveal a Correlation between Genome Architecture and Gene Family Evolution in Ciliates
title_fullStr	Single-Cell Transcriptomics Reveal a Correlation between Genome Architecture and Gene Family Evolution in Ciliates
title_full_unstemmed	Single-Cell Transcriptomics Reveal a Correlation between Genome Architecture and Gene Family Evolution in Ciliates
title_sort	single-cell transcriptomics reveal a correlation between genome architecture and gene family evolution in ciliates
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/13f22fde26c34e10b225d8b3ec3aa544
work_keys_str_mv	AT yingyan singlecelltranscriptomicsrevealacorrelationbetweengenomearchitectureandgenefamilyevolutioninciliates AT xyrusxmaureralcala singlecelltranscriptomicsrevealacorrelationbetweengenomearchitectureandgenefamilyevolutioninciliates AT robknight singlecelltranscriptomicsrevealacorrelationbetweengenomearchitectureandgenefamilyevolutioninciliates AT sergeilkosakovskypond singlecelltranscriptomicsrevealacorrelationbetweengenomearchitectureandgenefamilyevolutioninciliates AT lauraakatz singlecelltranscriptomicsrevealacorrelationbetweengenomearchitectureandgenefamilyevolutioninciliates
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Single-Cell Transcriptomics Reveal a Correlation between Genome Architecture and Gene Family Evolution in Ciliates

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