Quest for Ancestors of Eukaryal Cells Based on Phylogenetic Analyses of Aminoacyl-tRNA Synthetases

Ryutaro Furukawa, Mizuho Nakagawa, Takuya Kuroyanagi, Shin Ichi Yokobori, Akihiko Yamagishi

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

The three-domain phylogenetic system of life has been challenged, particularly with regard to the position of Eukarya. The recent increase of known genome sequences has allowed phylogenetic analyses of all extant organisms using concatenated sequence alignment of universally conserved genes; these data supported the two-domain hypothesis, which place eukaryal species as ingroups of the Domain Archaea. However, the origin of Eukarya is complicated: the closest archaeal species to Eukarya differs in single-gene phylogenetic analyses depending on the genes. In this report, we performed molecular phylogenetic analyses of 23 aminoacyl-tRNA synthetases (ARS). Cytoplasmic ARSs in 12 trees showed a monophyletic Eukaryotic branch. One ARS originated from TACK superphylum. One ARS originated from Euryarchaeota and three originated from DPANN superphylum. Four ARSs originated from different bacterial species. The other 8 cytoplasmic ARSs were split into two or three groups in respective trees, which suggested that the cytoplasmic ARSs were replaced by secondary ARSs, and the original ARSs have been lost during evolution of Eukarya. In these trees, one original cytoplasmic ARS was derived from Euryarchaeota and three were derived from DPANN superphylum. Our results strongly support the two-domain hypothesis. We discovered that rampant-independent lateral gene transfers from several archaeal species of DPANN superphylum have contributed to the formation of Eukaryal cells. Based on our phylogenetic analyses, we proposed a model for the establishment of Eukarya.

Original languageEnglish
Pages (from-to)51-66
Number of pages16
JournalJournal of Molecular Evolution
Volume84
Issue number1
DOIs
Publication statusPublished - 2017 Jan 1
Externally publishedYes

Fingerprint

aminoacyl tRNA ligases
Amino Acyl-tRNA Synthetases
Eukaryota
ancestry
phylogenetics
Euryarchaeota
phylogeny
cells
gene
Genes
Horizontal Gene Transfer
genes
Sequence Alignment
gene transfer
Archaea
sequence alignment
genome
Genome
organisms

Keywords

  • Aminoacyl-tRNA synthetase
  • DPANN superphylum
  • Last eukaryal common ancestor (LECA)
  • Phylogenetic analysis

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics

Cite this

Quest for Ancestors of Eukaryal Cells Based on Phylogenetic Analyses of Aminoacyl-tRNA Synthetases. / Furukawa, Ryutaro; Nakagawa, Mizuho; Kuroyanagi, Takuya; Yokobori, Shin Ichi; Yamagishi, Akihiko.

In: Journal of Molecular Evolution, Vol. 84, No. 1, 01.01.2017, p. 51-66.

Research output: Contribution to journalArticle

Furukawa, Ryutaro ; Nakagawa, Mizuho ; Kuroyanagi, Takuya ; Yokobori, Shin Ichi ; Yamagishi, Akihiko. / Quest for Ancestors of Eukaryal Cells Based on Phylogenetic Analyses of Aminoacyl-tRNA Synthetases. In: Journal of Molecular Evolution. 2017 ; Vol. 84, No. 1. pp. 51-66.
@article{7f543c82a75f49f09c72453416d89927,
title = "Quest for Ancestors of Eukaryal Cells Based on Phylogenetic Analyses of Aminoacyl-tRNA Synthetases",
abstract = "The three-domain phylogenetic system of life has been challenged, particularly with regard to the position of Eukarya. The recent increase of known genome sequences has allowed phylogenetic analyses of all extant organisms using concatenated sequence alignment of universally conserved genes; these data supported the two-domain hypothesis, which place eukaryal species as ingroups of the Domain Archaea. However, the origin of Eukarya is complicated: the closest archaeal species to Eukarya differs in single-gene phylogenetic analyses depending on the genes. In this report, we performed molecular phylogenetic analyses of 23 aminoacyl-tRNA synthetases (ARS). Cytoplasmic ARSs in 12 trees showed a monophyletic Eukaryotic branch. One ARS originated from TACK superphylum. One ARS originated from Euryarchaeota and three originated from DPANN superphylum. Four ARSs originated from different bacterial species. The other 8 cytoplasmic ARSs were split into two or three groups in respective trees, which suggested that the cytoplasmic ARSs were replaced by secondary ARSs, and the original ARSs have been lost during evolution of Eukarya. In these trees, one original cytoplasmic ARS was derived from Euryarchaeota and three were derived from DPANN superphylum. Our results strongly support the two-domain hypothesis. We discovered that rampant-independent lateral gene transfers from several archaeal species of DPANN superphylum have contributed to the formation of Eukaryal cells. Based on our phylogenetic analyses, we proposed a model for the establishment of Eukarya.",
keywords = "Aminoacyl-tRNA synthetase, DPANN superphylum, Last eukaryal common ancestor (LECA), Phylogenetic analysis",
author = "Ryutaro Furukawa and Mizuho Nakagawa and Takuya Kuroyanagi and Yokobori, {Shin Ichi} and Akihiko Yamagishi",
year = "2017",
month = "1",
day = "1",
doi = "10.1007/s00239-016-9768-2",
language = "English",
volume = "84",
pages = "51--66",
journal = "Journal of Molecular Evolution",
issn = "0022-2844",
publisher = "Springer New York",
number = "1",

}

TY - JOUR

T1 - Quest for Ancestors of Eukaryal Cells Based on Phylogenetic Analyses of Aminoacyl-tRNA Synthetases

AU - Furukawa, Ryutaro

AU - Nakagawa, Mizuho

AU - Kuroyanagi, Takuya

AU - Yokobori, Shin Ichi

AU - Yamagishi, Akihiko

PY - 2017/1/1

Y1 - 2017/1/1

N2 - The three-domain phylogenetic system of life has been challenged, particularly with regard to the position of Eukarya. The recent increase of known genome sequences has allowed phylogenetic analyses of all extant organisms using concatenated sequence alignment of universally conserved genes; these data supported the two-domain hypothesis, which place eukaryal species as ingroups of the Domain Archaea. However, the origin of Eukarya is complicated: the closest archaeal species to Eukarya differs in single-gene phylogenetic analyses depending on the genes. In this report, we performed molecular phylogenetic analyses of 23 aminoacyl-tRNA synthetases (ARS). Cytoplasmic ARSs in 12 trees showed a monophyletic Eukaryotic branch. One ARS originated from TACK superphylum. One ARS originated from Euryarchaeota and three originated from DPANN superphylum. Four ARSs originated from different bacterial species. The other 8 cytoplasmic ARSs were split into two or three groups in respective trees, which suggested that the cytoplasmic ARSs were replaced by secondary ARSs, and the original ARSs have been lost during evolution of Eukarya. In these trees, one original cytoplasmic ARS was derived from Euryarchaeota and three were derived from DPANN superphylum. Our results strongly support the two-domain hypothesis. We discovered that rampant-independent lateral gene transfers from several archaeal species of DPANN superphylum have contributed to the formation of Eukaryal cells. Based on our phylogenetic analyses, we proposed a model for the establishment of Eukarya.

AB - The three-domain phylogenetic system of life has been challenged, particularly with regard to the position of Eukarya. The recent increase of known genome sequences has allowed phylogenetic analyses of all extant organisms using concatenated sequence alignment of universally conserved genes; these data supported the two-domain hypothesis, which place eukaryal species as ingroups of the Domain Archaea. However, the origin of Eukarya is complicated: the closest archaeal species to Eukarya differs in single-gene phylogenetic analyses depending on the genes. In this report, we performed molecular phylogenetic analyses of 23 aminoacyl-tRNA synthetases (ARS). Cytoplasmic ARSs in 12 trees showed a monophyletic Eukaryotic branch. One ARS originated from TACK superphylum. One ARS originated from Euryarchaeota and three originated from DPANN superphylum. Four ARSs originated from different bacterial species. The other 8 cytoplasmic ARSs were split into two or three groups in respective trees, which suggested that the cytoplasmic ARSs were replaced by secondary ARSs, and the original ARSs have been lost during evolution of Eukarya. In these trees, one original cytoplasmic ARS was derived from Euryarchaeota and three were derived from DPANN superphylum. Our results strongly support the two-domain hypothesis. We discovered that rampant-independent lateral gene transfers from several archaeal species of DPANN superphylum have contributed to the formation of Eukaryal cells. Based on our phylogenetic analyses, we proposed a model for the establishment of Eukarya.

KW - Aminoacyl-tRNA synthetase

KW - DPANN superphylum

KW - Last eukaryal common ancestor (LECA)

KW - Phylogenetic analysis

UR - http://www.scopus.com/inward/record.url?scp=84997418648&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84997418648&partnerID=8YFLogxK

U2 - 10.1007/s00239-016-9768-2

DO - 10.1007/s00239-016-9768-2

M3 - Article

C2 - 27889804

AN - SCOPUS:84997418648

VL - 84

SP - 51

EP - 66

JO - Journal of Molecular Evolution

JF - Journal of Molecular Evolution

SN - 0022-2844

IS - 1

ER -