BACKGROUND: Organelle retention is a form of mixotrophy that allows organisms to reap metabolic benefits similar to those of photoautotrophs through capture of algal prey and sequestration of their plastids. Mesodinium rubrum is an abundant and broadly distributed photosynthetic marine ciliate that steals organelles from cryptophyte algae, such as Geminigera cryophila. M. rubrum is unique from most other acquired phototrophs because it also steals a functional nucleus that facilitates genetic control of sequestered plastids and other organelles. We analyzed changes in G. cryophila nuclear gene expression and transcript abundance after its incorporation into the cellular architecture of M. rubrum as an initial step towards understanding this complex system. METHODS: We compared Illumina-generated transcriptomes of the cryptophyte Geminigera cryophila as a free-living cell and as a sequestered nucleus in M. rubrum to identify changes in protein abundance and gene expression. After KEGG annotation, proteins were clustered by functional categories, which were evaluated for over- or under-representation in the sequestered nucleus. Similarly, coding sequences were grouped by KEGG categories/ pathways, which were then evaluated for over- or under-expression via read count strategies. RESULTS: At the time of sampling, the global transcriptome of M. rubrum was dominated (~58-62 %) by transcription from its stolen nucleus. A comparison of transcriptomes from free-living G. cryophila cells to those of the sequestered nucleus revealed a decrease in gene expression and transcript abundance for most functional protein categories within the ciliate. However, genes coding for proteins involved in photosynthesis, oxidative stress reduction, and several other metabolic pathways revealed striking exceptions to this general decline. CONCLUSIONS: Major changes in G. cryophila transcript expression after sequestration by M. rubrum and the ciliate's success as a photoautotroph imply some level of control or gene regulation by the ciliate and at the very least reflect a degree of coordination between host and foreign organelles. Intriguingly, cryptophyte genes involved in protein transport are significantly under-expressed in M. rubrum, implicating a role for the ciliate's endomembrane system in targeting cryptophyte proteins to plastid complexes. Collectively, this initial portrait of an acquired transcriptome within a dynamic and ecologically successful ciliate highlights the remarkable cellular and metabolic chimerism of this system.

Mixoplankton are protist plankton that are capable of phototrophy and phagotrophy. These organismsare increasingly recognised not just as freaks of nature, but as a substantial part of marineplankton. Most existing plankton models still assume a strict dichotomy between phototrophsand heterotrophs. Few models consider mixoplanktonic activity as a synergism of the two trophicmodes. Many different mixoplankton functional types exist on a gradient between heterotrophy andphototrophy. The cryptophyte (Teleaulax)-Mesodinium-Dinophysis (TMD) complex is a specificpredator-prey interaction of different types of mixoplankton and a good example of the complexityof mixoplankton interaction and trophodynamics. The specialist non-constitutive mixoplankton(SNCM) Mesodinium acquires its chloroplasts strictly from a specific constitutive mixoplankton(CM) cryptophyte, while the harmful algal bloom (HAB) species Dinophysis acquires its third-handchloroplasts exclusively from Mesodinium.The generic NPZ-style protist model developed here shows that mixoplankton displays dynamicsthat are distinctly different from strict heterotrophs and autotrophs in terms of growth and theway they shape their environment. In addition, there is a clear niche separation between differentmixoplankton types (general non-constitutive mixoplankton (GNCM), SNCM and CM) according tonutrient, prey and light resource availabilities indicating a niche separation of each type. Thus,considering the different mixoplankton functional types in specialised multi-organism relationshipsas they are found in the TMD-complex may be important for their understanding and accurateprediction of growth and biomass development. Currently, none of the many models of Dinophysiscapture the biological dependencies. Results from a nitrogen-based TMD model suggest thatthe timing and quantity of prey availability is crucial for the bloom dynamics of Mesodinium andDinophysis. Some CMs may only feed when phosphate is the limiting nutrient. The results ofthe variable stoichiometric “Perfect Beast” model that was configured as Teleaulax amphioxeia incombination with experimental data strongly suggest that the cryptophyte feeds on bacteria tocompensate for phosphate limitation.This work shows the importance of considering mixoplankton in ecosystem models alongsidestrict heterotrophs and autotrophs and that distinction between different mixoplankton functionaltypes matters. Mixoplankton distinctly differ in their nutrient utilisation and growth dynamics.Predator-prey interactions have different implications for mixoplankton than for heterotrophs andtheir inclusion in models could improve our understanding of the formation of harmful mixoplanktonblooms. The unique physiology of mixoplankton and their nutrient utilisation and trophic levelsneed consideration in species specific models. / Le mixoplancton inclut les protistes planctoniques capables de phototrophie et de phagotrophie.Ces organismes sont de plus en plus reconnus comme une partie importante du plancton marin.Toutefois, la plupart des modèles mathématiques planctoniques existants supposent encoreune stricte dichotomie entre les organismes phototrophes et hétérotrophes et peu de modèlesconsidèrent l’activité mixoplanctonique comme une synergie entre les deux modes trophiques.De nombreux types fonctionnels mixoplanctoniques différents existent dans un gradient entrel’hétérotrophie et la phototrophie. Le complexe cryptophyte (Teleaulax)-Mesodinium-Dinophysis(TMD) est une interaction prédateur-proie spécifique entre différents types de mixoplancton et unbon exemple de la complexité des interactions et des relations trophodynamiques du mixoplancton.Mesodinium, mixoplancton spécialiste non constitutif (SNCM), ne peut acquérir ses chloroplastesque de cryptophytes (mixoplancton constitutif (CM)) spécifiques (tel que Teleaulax), tandis quel’espèce Dinophysis, responsable d’efflorescences algales nuisibles, acquiert ses chloroplastesexclusivement de Mesodinium. Le modèle générique de protistes, de type NPZ, développé dansce travail montre que le mixoplancton présente une dynamique nettement différente de celle deshétérotrophes et autotrophes strictes en termes de croissance et de la façon dont ils façonnentleur environnement. En outre, il existe une séparation de niches claire entre les différents typesde mixoplancton (mixoplancton généraliste non-constitutif (GNCM), SNCM et CM) en fonction dela disponibilité en lumière, en nutriments et en proies. En conséquence, la prise en compte desdifférents types fonctionnels du mixoplancton dans des relations multi-organismes spécialisées,telles qu’on les trouve dans le complexe TMD, peut être importante pour leur compréhension et laprédiction précise de leur croissance et biomasse. Actuellement, aucun des modèles existants deDinophysis ne rend compte de ces dépendances biologiques. Les résultats d’un modèle TMD basésur l’azote suggèrent que le moment et la quantité de proies disponibles sont des facteurs cruciauxpour la dynamique de Mesodinium et de Dinophysis. Certains CM peuvent se nourrir uniquementlorsque le phosphate est le nutriment limitant. Les résultats du modèle à stoechiométrie variable"Perfect Beast", qui a été configuré pour représenter Teleaulax amphioxeia sur base de donnéesexpérimentales, suggèrent fortement que le cryptophyte se nourrit de bactéries pour compenserla limitation en phosphate. Ce travail montre l’importance de prendre en compte le mixoplanctondans les modèles d’écosystème en plus des hétérotrophes et des autotrophes stricts et que ladistinction entre les différents types fonctionnels de mixoplancton est importante. Le mixoplanctonse distingue par son utilisation des nutriments et sa dynamique de croissance. Les interactionsprédateur-proie n’ont pas les mêmes implications pour le mixoplancton que pour les hétérotropheset leur prise en compte dans les modèles pourrait améliorer notre compréhension de la formationdes efflorescences nuisibles de mixoplancton. La physiologie unique du mixoplancton, sonutilisation des nutriments et ses niveaux trophiques doivent être pris en compte dans les modèlesspécifiques aux espèces. / Doctorat en Sciences agronomiques et ingénierie biologique / info:eu-repo/semantics/nonPublished