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Sci Adv. 2017 Jul 5;3(7):e1700239. doi: 10.1126/sciadv.1700239. eCollection 2017 Jul.

Population genomics of picophytoplankton unveils novel chromosome hypervariability.

Author information

1
Bioinformatics Center, Institute for Chemical Research, Kyoto University, Uji, Kyoto 611-0011, Japan.
2
CNRS, Biologie Intégrative des Organismes Marins (BIOM), Observatoire Océanologique, F-66650 Banyuls-sur-Mer, France.
3
Sorbonne Universités, Université Pierre et Marie Curie, UMR7232, BIOM, Observatoire Océanologique, F-66650 Banyuls-sur-Mer, France.
4
Laboratoire d'Informatique, de Robotique et de Microélectronique de Montpellier, CNRS, and Université de Montpellier, 161 rue Ada, 34095 Montpellier Cedex 5, France.
5
Institut de Biologie Computationnelle, CNRS, and Université de Montpellier, 860 rue Saint Priest, 34095 Montpellier Cedex 5, France.
6
U.S. Department of Energy Joint Genome Institute, Walnut Creek, CA 94598, USA.
7
INRA, plateforme Génome et Transcriptome (GeT-PlaGe), GenoToul, Castanet-Tolosan, France.
8
Department of Plant and Microbial Biology, University of California, Berkeley, 111 Koshland Hall, Berkeley, CA 94720, USA.
9
School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK.

Abstract

Tiny photosynthetic microorganisms that form the picoplankton (between 0.3 and 3 μm in diameter) are at the base of the food web in many marine ecosystems, and their adaptability to environmental change hinges on standing genetic variation. Although the genomic and phenotypic diversity of the bacterial component of the oceans has been intensively studied, little is known about the genomic and phenotypic diversity within each of the diverse eukaryotic species present. We report the level of genomic diversity in a natural population of Ostreococcus tauri (Chlorophyta, Mamiellophyceae), the smallest photosynthetic eukaryote. Contrary to the expectations of clonal evolution or cryptic species, the spectrum of genomic polymorphism observed suggests a large panmictic population (an effective population size of 1.2 × 107) with pervasive evidence of sexual reproduction. De novo assemblies of low-coverage chromosomes reveal two large candidate mating-type loci with suppressed recombination, whose origin may pre-date the speciation events in the class Mamiellophyceae. This high genetic diversity is associated with large phenotypic differences between strains. Strikingly, resistance of isolates to large double-stranded DNA viruses, which abound in their natural environment, is positively correlated with the size of a single hypervariable chromosome, which contains 44 to 156 kb of strain-specific sequences. Our findings highlight the role of viruses in shaping genome diversity in marine picoeukaryotes.

KEYWORDS:

GC content evolution; chromothripsis; evolutionary genomics; linkage disequilbrium; mating type locus; multiple nucleotide mutation events; picophytoplankton; population genomics; prasinovirus; sex evolution

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