1. Evolutionary Mechanisms of Long-Term Genome Diversification Associated With Niche Partitioning in Marine Picocyanobacteria
- Author
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Doré, Hugo, Farrant, Gregory K., Guyet, Ulysse, Haguait, Julie, Humily, Florian, Ratin, Morgane, Pitt, Frances Diana, Ostrowski, Martin, Six, Christophe, Brillet-Guéguen, Loraine, Hoebeke, Mark, Bisch, Antoine, Le Corguillé, Gildas, Corre, Erwan, Labadie, Karine, Aury, Jean-Marc, Wincker, Patrick, Choi, Dong Han, Noh, Jae Hoon, Eveillard, Damien, Scanlan, David J., Partensky, Frédéric, Garczarek, Laurence, Adaptation et diversité en milieu marin (AD2M), Station biologique de Roscoff (SBR), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Laboratoire des Sciences du Numérique de Nantes (LS2N), Université de Nantes - UFR des Sciences et des Techniques (UN UFR ST), Université de Nantes (UN)-Université de Nantes (UN)-École Centrale de Nantes (ECN)-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique Bretagne-Pays de la Loire (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT), ABiMS - Informatique et bioinformatique = Analysis and Bioinformatics for Marine Science (FR2424), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Laboratoire de Biologie Intégrative des Modèles Marins (LBI2M), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Station biologique de Roscoff (SBR), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Institut de Biologie François JACOB (JACOB), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Combinatoire et Bioinformatique (COMBI), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Université de Nantes - UFR des Sciences et des Techniques (UN UFR ST), Adaptation et diversité en milieu marin (ADMM), Institut national des sciences de l'Univers (INSU - CNRS)-Station biologique de Roscoff (SBR), Université de Nantes (UN)-Université de Nantes (UN)-École Centrale de Nantes (ECN)-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique (IMT Atlantique), ABiMS - Informatique et bioinformatique = Analysis and Bioinformatics for Marine Science (ABIMS), Fédération de recherche de Roscoff (FR2424), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Station biologique de Roscoff (SBR), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Combinatoire et Bioinformatique (LS2N - équipe COMBI), ANR-13-ADAP-0010,SAMOSA,Synechococcus as a model genus for studying adaptation of marine phytoplankton to environmental changes(2013), ANR-17-CE02-0014,CINNAMON,Analyse multi-échelle de l'adaptation à la carence en Fer chez un organisme clé du phytoplancton marin, dans un contexte de changement global(2017), IMT Atlantique Bretagne-Pays de la Loire (IMT Atlantique), and Université de Nantes (UN)-Université de Nantes (UN)-École Centrale de Nantes (ECN)-Centre National de la Recherche Scientifique (CNRS)
- Subjects
Marine cyanobacteria 1 ,amino-acid substitutions 6 ,amino-acid substitutions ,[INFO.INFO-OH]Computer Science [cs]/Other [cs.OH] ,comparative genomics ,Microbiology ,genomic islands ,QH301 ,comparative genomics 4 ,evolution ,QH426 ,0502 Environmental Science and Management, 0503 Soil Sciences, 0605 Microbiology ,ComputingMilieux_MISCELLANEOUS ,Synechococcus 3 ,Original Research ,Prochlorococcus ,niche adaptation ,Synechococcus ,marine cyanobacteria ,[SDV.BIBS]Life Sciences [q-bio]/Quantitative Methods [q-bio.QM] ,QR ,niche adaptation 5 ,evolution 8 ,Prochlorococcus2 ,[INFO.INFO-BI]Computer Science [cs]/Bioinformatics [q-bio.QM] ,genomic islands 7 ,[SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis - Abstract
Marine picocyanobacteria of the genera Prochlorococcus and Synechococcus are the most abundant photosynthetic organisms on Earth, an ecological success thought to be linked to the differential partitioning of distinct ecotypes into specific ecological niches. However, the underlying processes that governed the diversification of these microorganisms and the appearance of niche-related phenotypic traits are just starting to be elucidated. Here, by comparing 81 genomes, including 34 new Synechococcus, we explored the evolutionary processes that shaped the genomic diversity of picocyanobacteria. Time-calibration of a core-protein tree showed that gene gain/loss occurred at an unexpectedly low rate between the different lineages, with for instance 5.6 genes gained per million years (My) for the major Synechococcus lineage (sub-cluster 5.1), among which only 0.71/My have been fixed in the long term. Gene content comparisons revealed a number of candidates involved in nutrient adaptation, a large proportion of which are located in genomic islands shared between either closely or more distantly related strains, as identified using an original network construction approach. Interestingly, strains representative of the different ecotypes co-occurring in phosphorus-depleted waters (Synechococcus clades III, WPC1, and sub-cluster 5.3) were shown to display different adaptation strategies to this limitation. In contrast, we found few genes potentially involved in adaptation to temperature when comparing cold and warm thermotypes. Indeed, comparison of core protein sequences highlighted variants specific to cold thermotypes, notably involved in carotenoid biosynthesis and the oxidative stress response, revealing that long-term adaptation to thermal niches relies on amino acid substitutions rather than on gene content variation. Altogether, this study not only deciphers the respective roles of gene gains/losses and sequence variation but also uncovers numerous gene candidates likely involved in niche partitioning of two key members of the marine phytoplankton.
- Published
- 2020
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