Convergent evolution and horizontal gene transfer in Arctic Ocean microalgae

Author:

Dorrell Richard G12,Kuo Alan3,Füssy Zoltan4ORCID,Richardson Elisabeth H5,Salamov Asaf3,Zarevski Nikola12,Freyria Nastasia J6,Ibarbalz Federico M12,Jenkins Jerry37,Pierella Karlusich Juan Jose12,Stecca Steindorff Andrei3ORCID,Edgar Robyn E6,Handley Lori7,Lail Kathleen3,Lipzen Anna3,Lombard Vincent8,McFarlane John5,Nef Charlotte12,Novák Vanclová Anna MG12,Peng Yi3,Plott Chris7,Potvin Marianne6,Vieira Fabio Rocha Jimenez12,Barry Kerrie3,de Vargas Colomban29,Henrissat Bernard108,Pelletier Eric211ORCID,Schmutz Jeremy37,Wincker Patrick211,Dacks Joel B5,Bowler Chris12,Grigoriev Igor V312ORCID,Lovejoy Connie6ORCID

Affiliation:

1. Institut de Biologie de l’ENS, Département de Biologie, École Normale Supérieure, CNRS, INSERM, Université PSL, Paris, France

2. CNRS Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, Paris, France

3. US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA

4. Department of Parasitology, BIOCEV, Faculty of Science, Charles University, Prague, Czech Republic

5. Division of Infectious Diseases, Department of Medicine, University of Alberta and Department of Biological Sciences, and University of Alberta, Edmonton, Canada

6. Département de Biologie, Institut de Biologie Intégrative des Systèmes, Université Laval, Quebec, Canada

7. HudsonAlpha Institute for Biotechnology, Huntsville, AL, USA

8. Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia

9. Sorbonne Université, CNRS, Station Biologique de Roscoff, AD2M, UMR 7144, Roscoff, France

10. Architecture et Fonction des Macromolécules Biologiques, CNRS, Aix-Marseille Université, Marseille, France

11. Génomique Métabolique, Genoscope, Institut de Biologie François Jacob, Commissariat à l'Énergie Atomique, CNRS, Université Évry, Université Paris-Saclay, Évry, France

12. Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA, USA

Abstract

Microbial communities in the world ocean are affected strongly by oceanic circulation, creating characteristic marine biomes. The high connectivity of most of the ocean makes it difficult to disentangle selective retention of colonizing genotypes (with traits suited to biome specific conditions) from evolutionary selection, which would act on founder genotypes over time. The Arctic Ocean is exceptional with limited exchange with other oceans and ice covered since the last ice age. To test whether Arctic microalgal lineages evolved apart from algae in the global ocean, we sequenced four lineages of microalgae isolated from Arctic waters and sea ice. Here we show convergent evolution and highlight geographically limited HGT as an ecological adaptive force in the form of PFAM complements and horizontal acquisition of key adaptive genes. Notably, ice-binding proteins were acquired and horizontally transferred among Arctic strains. A comparison withTaraOceans metagenomes and metatranscriptomes confirmed mostly Arctic distributions of these IBPs. The phylogeny of Arctic-specific genes indicated that these events were independent of bacterial-sourced HGTs in Antarctic Southern Ocean microalgae.

Funder

U.S. Department of Energy

ECOS Sud-Argentine Program

JW Fulbright Commission of the Slovak Republic

Natural Science and Engineering Council, Genome Québec

CNRS Momentum Fellowship

Agence Nationale de la Recherche

European Research Council

MEMO LIFE

PSL* Research University

France Génomique

OCEANOMICS

BrownCut project

Human Frontier Science Program

Publisher

Life Science Alliance, LLC

Subject

Health, Toxicology and Mutagenesis,Plant Science,Biochemistry, Genetics and Molecular Biology (miscellaneous),Ecology

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