Abstract
The single-celled ciliate Paramecium bursaria is an indispensable model for investigating endosymbiosis between protists and green-algal symbionts. To elucidate the mechanism of this type of endosymbiosis, we combined PacBio and Illumina sequencing to assemble a high-quality and near-complete macronuclear genome of P. bursaria. The genomic characteristics and phylogenetic analyses indicate that P. bursaria is the basal clade of the Paramecium genus. Through comparative genomic analyses with its close relatives, we found that P. bursaria encodes more genes related to nitrogen metabolism and mineral absorption, but encodes fewer genes involved in oxygen binding and N-glycan biosynthesis. A comparison of the transcriptomic profiles between P. bursaria with and without endosymbiotic Chlorella showed differential expression of a wide range of metabolic genes. We selected 32 most differentially expressed genes to perform RNA interference experiment in P. bursaria, and found that P. bursaria can regulate the abundance of their symbionts through glutamine supply. This study provides novel insights into Paramecium evolution and will extend our knowledge of the molecular mechanism for the induction of endosymbiosis between P. bursaria and green algae.
Highlights
Endosymbiosis is a widely accepted theory that explains the origin of eukaryotic organelles, such as chloroplasts and mitochondria
By comparing P. tetraurelia, P. biaurelia and P. sexaurelia to P. caudatum, we found that the average globin gene number in the three Paramecium species was twice that in P. caudatum, which can be attributed to multiple whole-genome duplication events that occurred in these species
The transient receptor potential cation channel subfamily M member 6 (TRPM6) gene of hosts encodes a protein including an ion channel domain and a protein kinase domain, which can transport the Mg2+ that plays a key role in harvesting solar energy during photosynthesis [29, 30]. This finding indicates that P. bursaria may supply its endosymbiotic algae with Mg2+ to ensure the symbionts’ ability to photosynthesize, which may explain the ability of P. bursaria to manipulate symbionts load according to light intensity [9]
Summary
Endosymbiosis is a widely accepted theory that explains the origin of eukaryotic organelles, such as chloroplasts and mitochondria. The transient receptor potential cation channel subfamily M member 6 (TRPM6) gene of hosts encodes a protein including an ion channel domain and a protein kinase domain, which can transport the Mg2+ that plays a key role in harvesting solar energy during photosynthesis [29, 30] This finding indicates that P. bursaria may supply its endosymbiotic algae with Mg2+ to ensure the symbionts’ ability to photosynthesize, which may explain the ability of P. bursaria to manipulate symbionts load according to light intensity [9]. Macronucleus glnA RNAi group was significantly lower than that of the control group (t-test, P < 0.001) (Fig. 2h, i and Supplementary Figure S6) These findings indicated that P. bursaria may supply glutamine for C. variabilis as a nitrogen source, and the host cells can regulate the abundance of endosymbiotic algae through the expression of their glnA gene. We believe that this study offers a unique opportunity to research ‘in progress’ genetic changes that are caused by endosymbiosis
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