Abstract

Phototrophic eukaryotes have evolved mainly by the primary or secondary uptake of photosynthetic organisms. A return to heterotrophy occurred multiple times in various protistan groups such as Chrysophyceae, despite the expected advantage of autotrophy. It is assumed that the evolutionary shift to mixotrophy and further to heterotrophy is triggered by a differential importance of nutrient and carbon limitation. We sequenced the genomes of 16 chrysophyte strains and compared them in terms of size, function, and sequence characteristics in relation to photo-, mixo- and heterotrophic nutrition. All strains were sequenced with Illumina and partly with PacBio. Heterotrophic taxa have reduced genomes and a higher GC content of up to 59% as compared to phototrophic taxa. Heterotrophs have a large pan genome, but a small core genome, indicating a differential specialization of the distinct lineages. The pan genome of mixotrophs and heterotrophs taken together but not the pan genome of the mixotrophs alone covers the complete functionality of the phototrophic strains indicating a random reduction of genes. The observed ploidy ranges from di- to tetraploidy and was found to be independent of taxonomy or trophic mode. Our results substantiate an evolution driven by nutrient and carbon limitation.

Highlights

  • Phototrophic eukaryotes have evolved mainly by the primary or secondary uptake of photosynthetic organisms

  • Recent hypotheses suggest that the shift from photo- to mixotrophy was one way to overcome nutrient limitations while the shift towards heterotrophy was caused by carbon limitations[4,5]

  • Findings from transcriptome sequencing of 18 chrysophyte strains provide first insights into molecular changes between trophic modes showing that heterotrophs possess a reduced repertoire of genes related to photosynthesis but an increased or upregulated repertoire of pathways associated with food uptake and motility[12]

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Summary

Introduction

Phototrophic eukaryotes have evolved mainly by the primary or secondary uptake of photosynthetic organisms. The presence of phototrophic, heterotrophic, and mixotrophic taxa and evidence for multiple gains and losses of photosynthesis across most major eukaryotic supergroups reflects the significance of nutritional constraints in the evolution of life[1,2,3]. The changing relevance of either nutrient or carbon limitation alters constraints in genome evolution which should be reflected by the incorporation of nucleotides with different costs, the loss of obsolete genes, and the evolution of new gene functions for a predatory lifestyle. Findings from transcriptome sequencing of 18 chrysophyte strains provide first insights into molecular changes between trophic modes showing that heterotrophs possess a reduced repertoire of genes related to photosynthesis but an increased or upregulated repertoire of pathways associated with food uptake and motility[12]. In this study, we examine genomes of 16 chrysophytes including phototrophic, mixotrophic, and heterotrophic lineages to investigate the impact of the nutritional shift and its drivers

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