Differential gene expression analysis and cytological evidence reveal a sexual stage of an amoeba with multiparental cellular and nuclear fusion
Sex is a hallmark of eukaryotes but its evolution in microbial eukaryotes is poorly elucidated. Recent genomic studies revealed microbial eukaryotes possess a genetic toolkit necessary for sexual reproduction. However, the mechanism of sexual development in a majority of microbial eukaryotes includi...
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| creator | Tekle, Yonas I Wang, Fang Heidari, Alireza Stewart, Alanna Johnson |
| description | Sex is a hallmark of eukaryotes but its evolution in microbial eukaryotes is poorly elucidated. Recent genomic studies revealed microbial eukaryotes possess a genetic toolkit necessary for sexual reproduction. However, the mechanism of sexual development in a majority of microbial eukaryotes including amoebozoans is poorly characterized. The major hurdle in studying sex in microbial eukaryotes is a lack of observational evidence, primarily due to its cryptic nature. In this study, we used a tractable fusing amoeba, Cochliopodium, to investigate sexual development using stage-specific Differential Gene Expression (DGE) and cytological analyses. Both DGE and cytological results showed that most of the meiosis and sex-related genes are upregulated in Cochliopodium undergoing fusion in laboratory culture. Relative gene ontology (GO) category representations in unfused and fused cells revealed a functional skew of the fused transcriptome toward DNA metabolism, nucleus and ligases that are suggestive of a commitment to sexual development. However, the GO categories of unfused cells were dominated by metabolic pathways and other processes indicative of a vegetative phase. Our study provides strong evidence that the fused cells represent a sexual stage in Cochliopodium. Our findings have further implications in understanding the evolution and mechanism of inheritance involving multiparents in other eukaryotes with a similar reproductive strategy. |
| doi_str_mv | 10.1371/journal.pone.0235725 |
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Recent genomic studies revealed microbial eukaryotes possess a genetic toolkit necessary for sexual reproduction. However, the mechanism of sexual development in a majority of microbial eukaryotes including amoebozoans is poorly characterized. The major hurdle in studying sex in microbial eukaryotes is a lack of observational evidence, primarily due to its cryptic nature. In this study, we used a tractable fusing amoeba, Cochliopodium, to investigate sexual development using stage-specific Differential Gene Expression (DGE) and cytological analyses. Both DGE and cytological results showed that most of the meiosis and sex-related genes are upregulated in Cochliopodium undergoing fusion in laboratory culture. Relative gene ontology (GO) category representations in unfused and fused cells revealed a functional skew of the fused transcriptome toward DNA metabolism, nucleus and ligases that are suggestive of a commitment to sexual development. However, the GO categories of unfused cells were dominated by metabolic pathways and other processes indicative of a vegetative phase. Our study provides strong evidence that the fused cells represent a sexual stage in Cochliopodium. Our findings have further implications in understanding the evolution and mechanism of inheritance involving multiparents in other eukaryotes with a similar reproductive strategy.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0235725</identifier><identifier>PMID: 33147262</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amoeba ; Amoeba - genetics ; Amoeba - physiology ; Amoebas ; Analysis ; Asexuality ; Biology and Life Sciences ; Cell culture ; Cellular biology ; Cysts ; Deoxyribonucleic acid ; Developmental stages ; DNA ; Eukaryotes ; Evolution ; Gene expression ; Gene Expression Profiling - methods ; Gene Expression Regulation ; Genetic aspects ; Genetic engineering ; Genomes ; Heredity ; Knowledge representation ; Laboratories ; Laboratory culture ; Meiosis ; Metabolic pathways ; Metabolism ; Microorganisms ; Nuclear Fusion ; Nuclei (cytology) ; Physiological aspects ; Reproduction (biology) ; Reproduction, Asexual - physiology ; Reproductive strategy ; Sequence Analysis, RNA ; Sex ; Sexual reproduction ; Single-Cell Analysis ; Toolkits</subject><ispartof>PloS one, 2020-11, Vol.15 (11), p.e0235725-e0235725</ispartof><rights>COPYRIGHT 2020 Public Library of Science</rights><rights>2020 Tekle et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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Recent genomic studies revealed microbial eukaryotes possess a genetic toolkit necessary for sexual reproduction. However, the mechanism of sexual development in a majority of microbial eukaryotes including amoebozoans is poorly characterized. The major hurdle in studying sex in microbial eukaryotes is a lack of observational evidence, primarily due to its cryptic nature. In this study, we used a tractable fusing amoeba, Cochliopodium, to investigate sexual development using stage-specific Differential Gene Expression (DGE) and cytological analyses. Both DGE and cytological results showed that most of the meiosis and sex-related genes are upregulated in Cochliopodium undergoing fusion in laboratory culture. Relative gene ontology (GO) category representations in unfused and fused cells revealed a functional skew of the fused transcriptome toward DNA metabolism, nucleus and ligases that are suggestive of a commitment to sexual development. However, the GO categories of unfused cells were dominated by metabolic pathways and other processes indicative of a vegetative phase. Our study provides strong evidence that the fused cells represent a sexual stage in Cochliopodium. Our findings have further implications in understanding the evolution and mechanism of inheritance involving multiparents in other eukaryotes with a similar reproductive strategy.</description><subject>Amoeba</subject><subject>Amoeba - genetics</subject><subject>Amoeba - physiology</subject><subject>Amoebas</subject><subject>Analysis</subject><subject>Asexuality</subject><subject>Biology and Life Sciences</subject><subject>Cell culture</subject><subject>Cellular biology</subject><subject>Cysts</subject><subject>Deoxyribonucleic acid</subject><subject>Developmental stages</subject><subject>DNA</subject><subject>Eukaryotes</subject><subject>Evolution</subject><subject>Gene expression</subject><subject>Gene Expression Profiling - methods</subject><subject>Gene Expression Regulation</subject><subject>Genetic aspects</subject><subject>Genetic engineering</subject><subject>Genomes</subject><subject>Heredity</subject><subject>Knowledge representation</subject><subject>Laboratories</subject><subject>Laboratory culture</subject><subject>Meiosis</subject><subject>Metabolic pathways</subject><subject>Metabolism</subject><subject>Microorganisms</subject><subject>Nuclear Fusion</subject><subject>Nuclei (cytology)</subject><subject>Physiological aspects</subject><subject>Reproduction (biology)</subject><subject>Reproduction, Asexual - 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However, the GO categories of unfused cells were dominated by metabolic pathways and other processes indicative of a vegetative phase. Our study provides strong evidence that the fused cells represent a sexual stage in Cochliopodium. Our findings have further implications in understanding the evolution and mechanism of inheritance involving multiparents in other eukaryotes with a similar reproductive strategy.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>33147262</pmid><doi>10.1371/journal.pone.0235725</doi><tpages>e0235725</tpages><orcidid>https://orcid.org/0000-0003-2781-2351</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Amoeba Amoeba - genetics Amoeba - physiology Amoebas Analysis Asexuality Biology and Life Sciences Cell culture Cellular biology Cysts Deoxyribonucleic acid Developmental stages DNA Eukaryotes Evolution Gene expression Gene Expression Profiling - methods Gene Expression Regulation Genetic aspects Genetic engineering Genomes Heredity Knowledge representation Laboratories Laboratory culture Meiosis Metabolic pathways Metabolism Microorganisms Nuclear Fusion Nuclei (cytology) Physiological aspects Reproduction (biology) Reproduction, Asexual - physiology Reproductive strategy Sequence Analysis, RNA Sex Sexual reproduction Single-Cell Analysis Toolkits |
| title | Differential gene expression analysis and cytological evidence reveal a sexual stage of an amoeba with multiparental cellular and nuclear fusion |
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