Shared ancestry of algal symbiosis and chloroplast sequestration in foraminifera

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Abstract

Foraminifera are unicellular organisms that established the most diverse algal symbioses in the marine realm. Endosymbiosis repeatedly evolved in several lineages, while some engaged in the sequestration of chloroplasts, known as kleptoplasty. So far, kleptoplasty has been documented exclusively in the rotaliid clade. Here, we report the discovery of kleptoplasty in the species Hauerina diversa that belongs to the miliolid clade. The existence of kleptoplasty in the two main clades suggests that it is more widespread than previously documented. We observed chloroplasts in clustered structures within the foraminiferal cytoplasm and confirmed their functionality. Phylogenetic analysis of 18 S ribosomal RNA gene sequences showed that H. diversa branches next to symbiont-bearing Alveolinidae. This finding represents evidence of of a relationship between kleptoplastic and symbiotic foraminifera.. Analysis of ribosomal genes and metagenomics revealed that alveolinid symbionts and kleptoplasts belong to the same clade, which suggests a common ancestry.

Abstract

Phylogeny reveals a common origin for chloroplast sequestration and algal symbiosis in foraminifera.

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New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.

Stéphane Guindon, Jean-François Dufayard, Vincent Lefort … (2010)

PhyML is a phylogeny software based on the maximum-likelihood principle. Early PhyML versions used a fast algorithm performing nearest neighbor interchanges to improve a reasonable starting tree topology. Since the original publication (Guindon S., Gascuel O. 2003. A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704), PhyML has been widely used (>2500 citations in ISI Web of Science) because of its simplicity and a fair compromise between accuracy and speed. In the meantime, research around PhyML has continued, and this article describes the new algorithms and methods implemented in the program. First, we introduce a new algorithm to search the tree space with user-defined intensity using subtree pruning and regrafting topological moves. The parsimony criterion is used here to filter out the least promising topology modifications with respect to the likelihood function. The analysis of a large collection of real nucleotide and amino acid data sets of various sizes demonstrates the good performance of this method. Second, we describe a new test to assess the support of the data for internal branches of a phylogeny. This approach extends the recently proposed approximate likelihood-ratio test and relies on a nonparametric, Shimodaira-Hasegawa-like procedure. A detailed analysis of real alignments sheds light on the links between this new approach and the more classical nonparametric bootstrap method. Overall, our tests show that the last version (3.0) of PhyML is fast, accurate, stable, and ready to use. A Web server and binary files are available from http://www.atgc-montpellier.fr/phyml/.

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metaSPAdes: a new versatile metagenomic assembler

Sergey Nurk, Dmitry Meleshko, Anton Korobeynikov … (2017)

While metagenomics has emerged as a technology of choice for analyzing bacterial populations, the assembly of metagenomic data remains challenging, thus stifling biological discoveries. Moreover, recent studies revealed that complex bacterial populations may be composed from dozens of related strains, thus further amplifying the challenge of metagenomic assembly. metaSPAdes addresses various challenges of metagenomic assembly by capitalizing on computational ideas that proved to be useful in assemblies of single cells and highly polymorphic diploid genomes. We benchmark metaSPAdes against other state-of-the-art metagenome assemblers and demonstrate that it results in high-quality assemblies across diverse data sets.

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SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building.

Manolo Gouy, Stéphane Guindon, Olivier Gascuel (2010)

We present SeaView version 4, a multiplatform program designed to facilitate multiple alignment and phylogenetic tree building from molecular sequence data through the use of a graphical user interface. SeaView version 4 combines all the functions of the widely used programs SeaView (in its previous versions) and Phylo_win, and expands them by adding network access to sequence databases, alignment with arbitrary algorithm, maximum-likelihood tree building with PhyML, and display, printing, and copy-to-clipboard of rooted or unrooted, binary or multifurcating phylogenetic trees. In relation to the wide present offer of tools and algorithms for phylogenetic analyses, SeaView is especially useful for teaching and for occasional users of such software. SeaView is freely available at http://pbil.univ-lyon1.fr/software/seaview.

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Author and article information

Contributors

Doron Pinko:

ORCID: https://orcid.org/0000-0001-9904-1168

Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draft

Eyal Rahav: Role: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: ValidationRole: Visualization

Natalia Belkin:

ORCID: https://orcid.org/0009-0006-8883-9944

Role: MethodologyRole: ResourcesRole: Validation

Maxim Rubin-Blum:

ORCID: https://orcid.org/0000-0003-2953-3161

Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: VisualizationRole: Writing - review & editing

Michal Kucera:

ORCID: https://orcid.org/0000-0002-7817-9018

Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: SupervisionRole: Writing - review & editing

Raphaël Morard:

ORCID: https://orcid.org/0000-0002-1181-5358

Role: ConceptualizationRole: Validation

Maria Holzmann:

ORCID: https://orcid.org/0000-0003-2460-6210

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: ValidationRole: Writing - original draftRole: Writing - review & editing

Uri Abdu:

ORCID: https://orcid.org/0000-0003-1226-0750

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Journal

Journal ID (nlm-ta): Sci Adv

Journal ID (iso-abbrev): Sci Adv

Journal ID (publisher-id): sciadv

Journal ID (hwp): advances

Title: Science Advances

Publisher: American Association for the Advancement of Science

ISSN (Electronic): 2375-2548

Publication date Collection: 13 October 2023

Publication date (Electronic, pub): 12 October 2023

Volume: 9

Issue: 41

Electronic Location Identifier: eadi3401

Affiliations

[ ¹ ]Department of Earth and Environmental Science, Ben-Gurion University of the Negev, Beer Sheva, Israel.

[ ² ]National Institute of Oceanography, Israel Oceanographic and Limnological Research, Haifa, Israel.

[ ³ ]MARUM-Center for Marine Environmental Sciences, University of Bremen, Bremen, Germany.

[ ⁴ ]Department of Genetics and Evolution, University of Geneva, Quai Ernest Ansermet 30, Geneva 4 1211, Switzerland.

[ ⁵ ]Department of Life Science, Ben-Gurion University of the Negev, Beer Sheva, Israel.

Author notes

[* ]Corresponding author. Email: sigalabr@ 123456bgu.ac.il (S.A.); abdu@ 123456bgu.ac.il (U.A.)

Author information

Doron Pinko https://orcid.org/0000-0001-9904-1168

Sigal Abramovich https://orcid.org/0000-0003-3124-1387

Natalia Belkin https://orcid.org/0009-0006-8883-9944

Maxim Rubin-Blum https://orcid.org/0000-0003-2953-3161

Michal Kucera https://orcid.org/0000-0002-7817-9018

Raphaël Morard https://orcid.org/0000-0002-1181-5358

Maria Holzmann https://orcid.org/0000-0003-2460-6210

Uri Abdu https://orcid.org/0000-0003-1226-0750

Article

Publisher ID: adi3401

DOI: 10.1126/sciadv.adi3401

PMC ID: 10569721

PubMed ID: 37824622

SO-VID: 8bfd41ee-7da6-4179-a87c-0859eec97ee3

Copyright © Copyright © 2023 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution License 4.0 (CC BY).

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution license, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

History

Date received : 19 April 2023

Date accepted : 07 September 2023

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100003977, Israel Science Foundation;

Award ID: 941/17

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Copyeditor Vivian Hernandez

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Shared ancestry of algal symbiosis and chloroplast sequestration in foraminifera

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Most cited references 52

New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.

metaSPAdes: a new versatile metagenomic assembler

SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building.

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