Single-cell genomics unveils a canonical origin of the diverse mitochondrial genomes of euglenozoans

There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

Abstract

Background

The supergroup Euglenozoa unites heterotrophic flagellates from three major clades, kinetoplastids, diplonemids, and euglenids, each of which exhibits extremely divergent mitochondrial characteristics. Mitochondrial genomes (mtDNAs) of euglenids comprise multiple linear chromosomes carrying single genes, whereas mitochondrial chromosomes are circular non-catenated in diplonemids, but circular and catenated in kinetoplastids. In diplonemids and kinetoplastids, mitochondrial mRNAs require extensive and diverse editing and/or trans-splicing to produce mature transcripts. All known euglenozoan mtDNAs exhibit extremely short mitochondrial small ( rns) and large ( rnl) subunit rRNA genes, and absence of tRNA genes. How these features evolved from an ancestral bacteria-like circular mitochondrial genome remains unanswered.

Results

We sequenced and assembled 20 euglenozoan single-cell amplified genomes (SAGs). In our phylogenetic and phylogenomic analyses, three SAGs were placed within kinetoplastids, 14 within diplonemids, one (EU2) within euglenids, and two SAGs with nearly identical small subunit rRNA gene (18S) sequences (EU17/18) branched as either a basal lineage of euglenids, or as a sister to all euglenozoans. Near-complete mitochondrial genomes were identified in EU2 and EU17/18. Surprisingly, both EU2 and EU17/18 mitochondrial contigs contained multiple genes and one tRNA gene. Furthermore, EU17/18 mtDNA possessed several features unique among euglenozoans including full-length rns and rnl genes, six mitoribosomal genes, and nad11, all likely on a single chromosome.

Conclusions

Our data strongly suggest that EU17/18 is an early-branching euglenozoan with numerous ancestral mitochondrial features. Collectively these data contribute to untangling the early evolution of euglenozoan mitochondria.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12915-021-01035-y.

Related collections

Most cited references 82

Record: found
Abstract: found
Article: found

Is Open Access

MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability

Kazutaka Katoh, Daron Standley (2013)

We report a major update of the MAFFT multiple sequence alignment program. This version has several new features, including options for adding unaligned sequences into an existing alignment, adjustment of direction in nucleotide alignment, constrained alignment and parallel processing, which were implemented after the previous major update. This report shows actual examples to explain how these features work, alone and in combination. Some examples incorrectly aligned by MAFFT are also shown to clarify its limitations. We discuss how to avoid misalignments, and our ongoing efforts to overcome such limitations.

0 comments Cited 10180 times – based on 0 reviews      Review now

Bookmark

Record: found
Abstract: found
Article: not found

Basic local alignment search tool.

Stephen F Altschul, Warren Gish, Webb Miller … (1990)

A new approach to rapid sequence comparison, basic local alignment search tool (BLAST), directly approximates alignments that optimize a measure of local similarity, the maximal segment pair (MSP) score. Recent mathematical results on the stochastic properties of MSP scores allow an analysis of the performance of this method as well as the statistical significance of alignments it generates. The basic algorithm is simple and robust; it can be implemented in a number of ways and applied in a variety of contexts including straightforward DNA and protein sequence database searches, motif searches, gene identification searches, and in the analysis of multiple regions of similarity in long DNA sequences. In addition to its flexibility and tractability to mathematical analysis, BLAST is an order of magnitude faster than existing sequence comparison tools of comparable sensitivity.

0 comments Cited 8803 times – based on 0 reviews      Review now

Bookmark

Record: found
Abstract: found
Article: found

Is Open Access

IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies

Lam-Tung Nguyen, Heiko Schmidt, Arndt von Haeseler … (2014)

Large phylogenomics data sets require fast tree inference methods, especially for maximum-likelihood (ML) phylogenies. Fast programs exist, but due to inherent heuristics to find optimal trees, it is not clear whether the best tree is found. Thus, there is need for additional approaches that employ different search strategies to find ML trees and that are at the same time as fast as currently available ML programs. We show that a combination of hill-climbing approaches and a stochastic perturbation method can be time-efficiently implemented. If we allow the same CPU time as RAxML and PhyML, then our software IQ-TREE found higher likelihoods between 62.2% and 87.1% of the studied alignments, thus efficiently exploring the tree-space. If we use the IQ-TREE stopping rule, RAxML and PhyML are faster in 75.7% and 47.1% of the DNA alignments and 42.2% and 100% of the protein alignments, respectively. However, the range of obtaining higher likelihoods with IQ-TREE improves to 73.3-97.1%.

0 comments Cited 6465 times – based on 0 reviews      Review now

Bookmark

All references

Author and article information

Contributors

Julius Lukeš: jula@paru.cas.cz

Jeremy G. Wideman:

ORCID: http://orcid.org/0000-0002-4426-9533

jeremy.wideman@asu.edu

Journal

Journal ID (nlm-ta): BMC Biol

Journal ID (iso-abbrev): BMC Biol

Title: BMC Biology

Publisher: BioMed Central (London )

ISSN (Electronic): 1741-7007

Publication date (Electronic): 17 May 2021

Publication date PMC-release: 17 May 2021

Publication date Collection: 2021

Volume: 19

Electronic Location Identifier: 103

Affiliations

[1 ]GRID grid.418095.1, ISNI 0000 0001 1015 3316, Institute of Parasitology, Biology Centre, , Czech Academy of Sciences, ; České Budějovice (Budweis), Czech Republic

[2 ]GRID grid.4491.8, ISNI 0000 0004 1937 116X, Faculty of Science, , Charles University, BIOCEV, ; Vestec, Czech Republic

[3 ]GRID grid.17091.3e, ISNI 0000 0001 2288 9830, Department of Botany, , University of British Columbia, ; Vancouver, Canada

[4 ]GRID grid.215654.1, ISNI 0000 0001 2151 2636, Center for Mechanisms of Evolution, Biodesign Institute, School of Life Sciences, , Arizona State University, ; Tempe, USA

[5 ]GRID grid.4991.5, ISNI 0000 0004 1936 8948, Department of Zoology, , University of Oxford, ; Oxford, UK

[6 ]GRID grid.14509.39, ISNI 0000 0001 2166 4904, Faculty of Sciences, University of South Bohemia, ; České Budějovice (Budweis), Czech Republic

Author information

Jeremy G. Wideman http://orcid.org/0000-0002-4426-9533

Article

Publisher ID: 1035

DOI: 10.1186/s12915-021-01035-y

PMC ID: 8130358

PubMed ID: 34001130

SO-VID: 5a3ff9a9-eec6-4340-99bc-8f38c8644686

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 1 March 2021

Date accepted : 22 April 2021

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001824, Grantová Agentura České Republiky;

Award ID: 20-07186S

Award Recipient : Julius Lukeš

Funded by: FundRef http://dx.doi.org/10.13039/501100001823, Ministerstvo Školství, Mládeže a Tělovýchovy;

Award ID: ERC CZ LL1601

Award Recipient : Julius Lukeš

Funded by: Royal Society

Award ID: URF\R\191005

Award Recipient : Thomas A. Richards

Funded by: Czech Ministry of Education

Award ID: 16_019/0000759

Award Recipient : Julius Lukeš

Custom metadata

ScienceOpen disciplines: Life sciences

Keywords: single-cell amplified genome,evolution,mitochondrial ribosome,phylogeny

Data availability:

ScienceOpen disciplines: Life sciences

Keywords: single-cell amplified genome, evolution, mitochondrial ribosome, phylogeny

Single-cell genomics unveils a canonical origin of the diverse mitochondrial genomes of euglenozoans

Read this article at

Abstract

Background

Results

Conclusions

Supplementary Information

Related collections

Coleoptera

Most cited references 82

MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability

Basic local alignment search tool.

IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies

Author and article information

Contributors

Journal

Affiliations

Author information

Article

History

Funding

Categories

Custom metadata

Comments

Comment on this article

Similar content 125

Cited by 7

Most referenced authors 1,614