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Identification of a deep-branching lineage of algae using environmental plastid genomes

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Abstract

Marine algae underpin entire ocean ecosystems. Yet algae in culture poorly represent their large environmental diversity, and we have a limited understanding of their convoluted evolution by endosymbiosis. Here, we perform a phylogeny-guided plastid genome-resolved metagenomic survey of Tara Oceans expeditions. We present a curated resource of 660 new non-redundant plastid genomes of environmental marine algae, vastly expanding plastid genome diversity within major algal groups, including many without closely related reference genomes. Notably, we recover four plastid genomes, including one near-complete, forming a deep-branching plastid lineage of nano-size algae that we informally name leptophytes. This group is globally distributed and generally rare, although it can reach relatively high abundance in the Arctic. A near-complete mitochondrial genome showing strong co-occurrence with leptophyte plastids is also recovered and assigned to this group. Leptophytes encompass the enigmatic plastid group DPL2, one of the very few known plastid groups not clearly belonging to major algal groups and previously known only from 16S rDNA sequences. Comparative organellar genomics and phylogenomics indicate that leptophytes are sister to haptophytes, and raise the intriguing possibility that cryptophytes acquired their plastids from haptophytes. Collectively, our study demonstrates that metagenomics can reveal hidden organellar diversity, and improve models of plastid evolution.

Data availability

The 937 metagenomes from Tara Oceans used in the study are publicly available at the EBI under project PRJEB402. Data our study generated has been deposited in an online repository: https://doi.org/10.17044/scilifelab.2821217381. This link provides access to the individual FASTA files from each plastid and mitochondrial genome used in our study (including the 660 non-redundant ptMAGs and 34 mtMAGs), the co-assembly of the top six samples where Lepto-01 was most abundant, individual gene alignments, concatenated and trimmed alignments, and maximum-likelihood and Bayesian tree files for the phylogenomic dataset. Source Data for Fig. 4, Supplementary Figs. 10-12, and Supplementary Fig. 22 can be found on the linked GitHub repository, while source data for Supplementary Figs. 2-6 is provided as Supplementary Data 1.

Code availability

All scripts used for genome annotation and phylogenetic analyses are available on GitHub: https://github.com/burki-lab/ptMAGs with the identifier: 10.5281/zenodo.1763560482.

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Acknowledgements

We thank Shinichi Sunagawa for having facilitated the recovery of relevant data from the mOTU metagenomic database maintained by his research group at the Department of Biology at ETH Zürich. We thank A. Roger, H. Baños, and C. McCarthey for discussions, and for kindly providing custom scripts for running the phylogenetic models MEOW and GF-MIX. We thank J.E. Dharamshi for discussions about phylogenetic analyses. Our survey was made possible by the sampling and sequencing efforts of the Tara Oceans Project. Tara Oceans (which includes the Tara Oceans and Tara Oceans Polar Circle expeditions) would not exist without the leadership of the Tara Oceans Foundation and the continuous support of 23 institutes (https://oceans.taraexpeditions.org/). This article is contribution number 164 of Tara Oceans. Phylogenetic analyses were enabled by resources provided by the National Academic Infrastructure for Supercomputing in Sweden (NAISS 2024/5-197), partially funded by the Swedish Research Council through grant agreement no. 2022-06725. M.J. was supported by the Swedish Research Council (International Postdoc grant 2022-00351). FB’s research is supported by grants from the European Research Council (ERC consolidator grant 101044505), the Swedish Research Council VR (2021-04055), and Science for Life Laboratory. TD’s research is supported by a grant from the l’Agence Nationale de la Recherche (ANR-23-CE02-0022). We also thank the commitment of the CNRS and Genoscope/CEA. Some of the computations were performed using the platine, titane and curie HPC machine provided through GENCI grants (t2011076389, t2012076389, t2013036389, t2014036389, t2015036389 and t2016036389).

Funding

Open access funding provided by Uppsala University.

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Author notes

  1. Eric Pelletier & Tom O. Delmont

    Present address: Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara GOsee, Paris, France

Authors and Affiliations

  1. Department of Aquatic Sciences and Assessment, Swedish University of Agricultural Sciences, Uppsala, Sweden

    Mahwash Jamy

  2. Department of Organismal Biology, Program in Systematic Biology, Uppsala University, Uppsala, Sweden

    Thomas Huber & Fabien Burki

  3. Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, Evry, France

    Thibault Antoine, Eric Pelletier & Tom O. Delmont

  4. Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara GOsee, Paris, France

    Thibault Antoine

  5. Department of Biology, Institute of Microbiology and Swiss Institute of Bioinformatics, ETH Zürich, Zürich, Switzerland

    Hans-Joachim Ruscheweyh

  6. Global Health Institute, School of Life Sciences, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland

    Lucas Paoli

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Contributions

F.B. and T.O.D. conceived the project. T.O.D. characterised the ptMAGs. M.J., F.B. and T.H., performed phylogenetic analyses. T.A., E.P. and T.O.D. created the plastid genomic database and performed surveys for nucleomorphs. H.J.R. and L.P. retrieved relevant data from mOTUs. M.J. and T.H. annotated the ptMAGs, and E.P. performed mapping analyses. F.B., M.J., and T.O.D. wrote the manuscript with input from all the authors.

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Jamy, M., Huber, T., Antoine, T. et al. Identification of a deep-branching lineage of algae using environmental plastid genomes.
Nat Commun (2025). https://doi.org/10.1038/s41467-025-67401-4

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