DE LA MACROEVOLUTION A LA MICROEVOLUTION CHEZ LE PHYTOPLANCTON : LE CAS DES ISOCHRYSIDALES

The haptophyte order Isochrysidales contains several ecologically and/or economically key taxa, including the bloom forming coccolithophore Gephyrocapsa (=Emiliania) huxleyi. Having originated less than 300,000 years ago, G. huxleyi is a relatively very young coccolithophore morphospecies that displays remarkable adaptive potential, having colonized most of the world's oceans to become the most abundant extant coccolithophore. This thesis focusses on investigating the biocomplexity and adaptability of G. huxleyi, with approaches ranging from definition of its macro-evolutionary phylogenetic context to finer scale study of intraspecific morpho-genetic variability and biogeographic structuring. A phylogenetic analysis including most described isochrysidalean morpho-species led to reevaluation of the major phenotypic characters and evolutionary trajectories within the order, and confirmation of the very tight evolutionary links between G. huxleyi and a sister species, G. oceanica, hence the proposal that this organism should be classified within Gephyrocapsa rather than the seperate genus Emiliania. Of the multiple nuclear and organellar genetic markers tested, only mitochondrial genes provided both sufficient resolution and suitable phylogenetic signal for reconstructing the micro-evolutionary history within the G. huxleyi morphospecies. Phylogenetic analyses of multiple mitochondrial genes from a large set of clonal culture strains of G.huxleyi isolated from diverse locations allowed distinction of two major haplotypes, termed α and β, displaying distinct biogeographic distributions. Further combined morpho-genetic analyses within the α and β genotypes, including analysis of ultrastructural characters of the coccoliths and genetic variations within the GPA marker, a gene known to be involved in biomineralization, allowed proposition of an evolutionary scenario that reconciles biological and morphological diversity and highlights cryptic morphological entities within the morphospecies. Furthermore, a molecular clock analysis of the mitochondrial phylogeny allowed correlation of diversification events to past environmental conditions. Automated microscopy analyses of gephyrocapsid coccolith mass in the world oceans over the last 40 ky indicate a global calcification decrease with increasing ocean acidification. However, the presence of hypercalcified forms in the most corrosive modern waters offshore Chile suggests that certain G. huxleyi genotypes are able to adapt to low pH conditions. Exploring intraspecific evolution at the genomic level, significant variations in gene content related to both ploidy level and environmentalconditions were detected. G. huxleyi strains from relatively stable, oligotrophic water-masses appear to have a tendency to have lost genes specifically expressed in the haploid phase of the haplo-diplontic life cycle. Seen as a dynamic process, the suggested loss of sex in open oceanic waters implies reduced long-term adaptability to environmental changes.L‘ordre phytoplanctonique des Isochrysidales comporte plusieurs taxa ayant une importance écologique et/ou économiqueremarquable, tel que le coccolithophore Gephyrocapsa (=Emiliania) huxleyi, connu pour ses larges efflorescences. Apparu ily a environ 300 000 ans, G. huxleyi est la plus jeune morpho-espèce de coccolithophore. G. huxleyi démontre un potentieladaptatif remarquable et a colonisé tous les océans tout en étant aujourd‘hui le plus abondant des coccolithophores. Au cours de ce travail de thèse, nous nous sommes interrogés sur la biocomplexité et l‘adaptabilité de G. huxleyi, en partant de son contexte phylogénétique macroévolutif vers les échelles plus fines de sa variabilité morphogénétique intraspécifique et de sa structuration biogéographique. L‘analyse phylogénétique de sept espèces d‘Isochrysidales a permis de revisiter les caractères phénotypiques majeurs et les trajectoires évolutives au sein de l‘ordre et de confirmer la relation étroite entre G. huxleyi et son espèce soeur Gephyrocapsa oceanica. Parmi les différents marqueurs nucléaires et cytoplasmiques testés, les gènes mitochondriaux sont les seuls qui ont un pouvoir de résolution suffisant pour reconstruire l‘histoire évolutive récente au sein des lignées de G. huxleyi. Les analyses phylogénétiques des gènes cox1, cox2, cox3, rpl16 et dam sur 150 souches isolées des océans mondiaux ont permis de distinguer deux haplotypes majeurs, et , qui présentent une distribution biogéographique bipolaire. En complément, des analyses morpho-génétiques combinant les caractères morphométriques des coccolithes et les variations génétiques du gène gpa, impliqué dans la biominéralisation, ont mené a une nouvelle définition des morphotypesde G. huxleyi au sein des deux haplotypes et . En particulier, des analyses en microscopie automatisée de la masse des coccolithes de gephyrocapsids dans les océans mondiaux sur les derniers 40 000 ans indiquent une baisse générale de la calcification avec l‘augmentation de l‘acidification de l‘océan. Cependant, la présence de formes hypercalcifiées dans les eaux les plus corrosives au large du Chili suggère que certains génotypes de G. huxleyi seraient adaptés à ces conditions de faible pH. En explorant l‘évolution des génomes au niveau intraspécifique, nous avons pu détecter de fortes variations du contenu génique liées au niveau de ploïdie et aux conditions environnementales. En effet, les souches de G. huxleyi provenant des masses d‘eau oligotrophes relativement stables ont manifestement perdu des gènes exprimés spécifiquement durant la phase haploïde du cycle de vie. Perçue comme un processus dynamique, cette perte putative de la sexualité dans le domaine océanique implique une réduction de la capacité de G. huxleyi à s‘adapter sur le long terme aux changements environnementaux

Declining metal availability in the Mesozoic seawater reflected in phytoplankton succession

Variable trace metal concentrations in the Precambrian ocean were closely linked to oxygen availability, although less is known about the drivers of seawater trace metal chemistry after the spread of complex life into the Phanerozoic eon. A major phytoplankton succession took place at the transition from the Palaeozoic to the Mesozoic era (~250 Myr ago), from an ocean dominated by the green Archaeplastida to secondary endosymbiotic algae with red-algal-derived plastids. Here, our comparative genomic analysis of 26 complete proteomes and metal domain analysis of additional 608 partially complete sequences of phytoplankton reveal that groups with different evolutionary history have distinct metal-binding proteins and contrasting metal acquisition strategies, adapted to differing availability of trace metals. The secondary-endosymbiont-bearing lineages are better adapted to well-oxygenated, nutrient-poor environments. This is supported by an enhanced thiol-based binding affinity of their transporters, coupled with minimized proteomic requirement for trace elements such as iron, copper and zinc at both protein and domain levels. Such different metal requirements across these lineages suggest a drastic decline in open-ocean trace metal concentrations at the inception of the Mesozoic, contributing to the shifts in phytoplankton communities that drove major changes in ocean chemical buffering.info:eu-repo/semantics/publishedVersio

Over-calcified forms of the coccolithophore Emiliania huxleyi in high-CO2 waters are not preadapted to ocean acidification

Marine multicellular organisms inhabiting waters with natural high fluctuations in pH appear more tolerant to acidification than conspecifics occurring in nearby stable waters, suggesting that environments of fluctuating pH hold genetic reservoirs for adaptation of key groups to ocean acidification (OA). The abundant and cosmopolitan calcifying phytoplankton Emiliania huxleyi exhibits a range of morphotypes with varying degrees of coccolith mineralization. We show that E. huxleyi populations in the naturally acidified upwelling waters of the eastern South Pacific, where pH drops below 7.8 as is predicted for the global surface ocean by the year 2100, are dominated by exceptionally over-calcified morphotypes whose distal coccolith shield can be almost solid calcite. Shifts in morphotype composition of E. huxleyi populations correlate with changes in carbonate system parameters. We tested if these correlations indicate that the hyper-calcified morphotype is adapted to OA. In experimental exposures to present-day vs. future pCO2 (400 vs. 1200 µatm), the over-calcified morphotypes showed the same growth inhibition (−29.1±6.3 %) as moderately calcified morphotypes isolated from non-acidified water (−30.7±8.8 %). Under the high-CO2–low-pH condition, production rates of particulate organic carbon (POC) increased, while production rates of particulate inorganic carbon (PIC) were maintained or decreased slightly (but not significantly), leading to lowered PIC ∕ POC ratios in all strains. There were no consistent correlations of response intensity with strain origin. The high-CO2–low-pH condition affected coccolith morphology equally or more strongly in over-calcified strains compared to moderately calcified strains. High-CO2–low-pH conditions appear not to directly select for exceptionally over-calcified morphotypes over other morphotypes, but perhaps indirectly by ecologically correlated factors. More generally, these results suggest that oceanic planktonic microorganisms, despite their rapid turnover and large population sizes, do not necessarily exhibit adaptations to naturally high-CO2 upwellings, and this ubiquitous coccolithophore may be near the limit of its capacity to adapt to ongoing ocean acidification

De la macroévolution à la microévolution chez le phytoplancton (le cas des isochrysidales)

PARIS-BIUSJ-Biologie recherche (751052107) / SudocSudocFranceF

Rapid diversification underlying the global dominance of a cosmopolitan phytoplankton

International audienceAbstract Marine phytoplankton play important roles in the global ecosystem, with a limited number of cosmopolitan keystone species driving their biomass. Recent studies have revealed that many of these phytoplankton are complexes composed of sibling species, but little is known about the evolutionary processes underlying their formation. Gephyrocapsa huxleyi , a widely distributed and abundant unicellular marine planktonic algae, produces calcified scales (coccoliths), thereby significantly affects global biogeochemical cycles via sequestration of inorganic carbon. This species is composed of morphotypes defined by differing degrees of coccolith calcification, the evolutionary ecology of which remains unclear. Here, we report an integrated morphological, ecological and genomic survey across globally distributed G. huxleyi strains to reconstruct evolutionary relationships between morphotypes in relation to their habitats. While G. huxleyi has been considered a single cosmopolitan species, our analyses demonstrate that it has evolved to comprise at least three distinct species, which led us to formally revise the taxonomy of the G. huxleyi complex. Moreover, the first speciation event occurred before the onset of the last interglacial period (~140 ka), while the second followed during this interglacial. Then, further rapid diversifications occurred during the most recent ice-sheet expansion of the last glacial period and established morphotypes as dominant populations across environmental clines. These results suggest that glacial-cycle dynamics contributed to the isolation of ocean basins and the segregations of oceans fronts as extrinsic drivers of micro-evolutionary radiations in extant marine phytoplankton

Rapid diversification underlying the global dominance of a cosmopolitan phytoplankton

International audienceAbstract Marine phytoplankton play important roles in the global ecosystem, with a limited number of cosmopolitan keystone species driving their biomass. Recent studies have revealed that many of these phytoplankton are complexes composed of sibling species, but little is known about the evolutionary processes underlying their formation. Gephyrocapsa huxleyi , a widely distributed and abundant unicellular marine planktonic algae, produces calcified scales (coccoliths), thereby significantly affects global biogeochemical cycles via sequestration of inorganic carbon. This species is composed of morphotypes defined by differing degrees of coccolith calcification, the evolutionary ecology of which remains unclear. Here, we report an integrated morphological, ecological and genomic survey across globally distributed G. huxleyi strains to reconstruct evolutionary relationships between morphotypes in relation to their habitats. While G. huxleyi has been considered a single cosmopolitan species, our analyses demonstrate that it has evolved to comprise at least three distinct species, which led us to formally revise the taxonomy of the G. huxleyi complex. Moreover, the first speciation event occurred before the onset of the last interglacial period (~140 ka), while the second followed during this interglacial. Then, further rapid diversifications occurred during the most recent ice-sheet expansion of the last glacial period and established morphotypes as dominant populations across environmental clines. These results suggest that glacial-cycle dynamics contributed to the isolation of ocean basins and the segregations of oceans fronts as extrinsic drivers of micro-evolutionary radiations in extant marine phytoplankton

Global compilation of the first occurrence of Gephyrocapsa huxleyi and other Gephyrocapsa species from sediment core samples

The data compilation includes the first occurrence of G. huxleyi and other species of Gephyrocapsa as revealed by Quaternary sediment samples from the world oceans. This new synthesis includes previously published data, all with rigorous relationships of their emergence events with marine isotope stages based on good quality oxygen isotope stratigraphy and/or astronomical tuning from each sediment core

ORIGINAL PAPER Integrative Taxonomy of the Pavlovophyceae (Haptophyta): A Reassessment

Rebecca) and only thirteen characterised species, several of which are important in ecological and economic contexts. We have constructed molecular phylogenies inferred from sequencing of ribosomal gene markers with comprehensive coverage of the described diversity, using type strains when available, together with additional cultured strains. The morphology and ultrastructure of 12 of the described species was also re-examined and the pigment signatures of many culture strains were determined. The molecular analysis revealed that sequences of all described species differed, although those of Pavlova gyrans and P. pinguis were nearly identical, these potentially forming a single cryptic species complex. Four well-delineated genetic clades were identified, one of which included species of both Pavlova and Diacronema. Unique combinations of morphological/ultrastructural characters were identified for each of these clades. The ancestral pigment signature of the Pavlovophyceae consisted of a basic set of pigments plus MV chl cPAV, the latter being entirely absent in the Pavlova + Diacronema clade and supplemented by DV chl cPAV in part of the Exanthemachrysis clade. Based on this combination of characters, we propose a taxonomic revision of the class, with transfer of several Pavlova species to an emended Diacronema genus. The evolution of the class is discussed in the context o

Repeated species radiations in the recent evolution of the key marine phytoplankton lineage Gephyrocapsa

International audiencePhytoplankton account for nearly half of global primary productivity and strongly affect the global carbon cycle, yet little is known about the forces that drive the evolution of these keystone microscopic organisms. Here we combine morphometric data from the fossil record of the ubiquitous coccolithophore genus Gephyrocapsa with genomic analyses of extant species to assess the genetic processes underlying Pleistocene palaeontological patterns. We demonstrate that all modern diversity in Gephyrocapsa (including Emiliania huxleyi) originated in a rapid species radiation during the last 0.6 Ma, coincident with the latest of the three pulses of Gephyrocapsa diversification and extinction documented in the fossil record. Our evolutionary genetic analyses indicate that new species in this genus have formed in sym-patry or parapatry, with occasional hybridisation between species. This sheds light on the mode of speciation during evolutionary radiation of marine phytoplankton and provides a model of how new plankton species form