Genome assembly of Nannochloropsis oceanica provides evidence of host nucleus overthrow by the symbiont nucleus during speciation

Abstract

The species of the genus Nannochloropsis are unique in their maintenance of a nucleus-plastid continuum throughout their cell cycle, non-motility and asexual reproduction. These characteristics should have been endorsed in their gene assemblages (genomes). Here we show that N. oceanica has a genome of 29.3 Mb consisting of 32 pseudochromosomes and containing 7,330 protein-coding genes; and the host nucleus may have been overthrown by an ancient red alga symbiont nucleus during speciation through secondary endosymbiosis. In addition, N. oceanica has lost its flagella and abilities to undergo meiosis and sexual reproduction, and adopted a genome reduction strategy during speciation. We propose that N. oceanica emerged through the active fusion of a host protist and a photosynthesizing ancient red alga and the symbiont nucleus became dominant over the host nucleus while the chloroplast was wrapped by two layers of endoplasmic reticulum. Our findings evidenced an alternative speciation pathway of eukaryotes.

Keywords: Evolution; Genomics.

Fig. 1

Protein-encoding gene models on each pseudochromosomes of N. oceanica. Mitochondrial and chloroplast pseudochromosomes are presented linearly but they can be circulated as their two ends contain the repeat assemblies of sequences. a The pseudochromosomes with gene models marked with vertical bars. The green bars represent gene models in the sense strand, while the yellow ones in the anti-sense strand of DNA. b The heatmap showing the interaction between 30 nuclear pseudochromosomes. c The Venn diagram of functional genes annotated against NT, NR, BLASTX, and BLASTP databases. d The similarity between nuclear pseudochromosomes. Less homozygosity is found among these pseudochromosomes, which is one of the characteristics of N. oceanica, genome reduction

Fig. 2

Phylogeny of Nannochloropsis and their relatives in different taxa deduced from nuclear genome (a), chloroplast genome (b), 18S ribosomal RNA gene (18S rDNA, c) and ribulose bisphosphate carboxylase large chain gene (rbcL) (d). a The phylogenetic tree of species inferred from the OrthoFinder using the genome protein sequences each species from the whole genome. b The phylogenetic tree of species inferred from the OrthoFinder using the chloroplast genome sequences each species. c The phylogenetic trees for 18S rDNA. The tree shows the consensus tree topology inferred by Bayesian analysis using alignments of 18S genes from NCBI. The scale bar indicates the nucleotide substitutions per site. This consensus topology derived from 512 trees, lnL = 22033.73. d The phylogenetic trees for rbcL protein. The tree shows the consensus tree topologies inferred by Bayesian analysis using alignments of rbcL proteins from NCBI. Scale bars represent 0.1 amino acid substitutions per site. In total, 439 aligned amino acid sites were analyzed. This consensus topology derived from 726 trees, α = 0.47 (0.41 < α < 0.56), pI = 0.0019 (0.0000007 < pI < 0.0059) and lnL = 10364.8

Fig. 3

Homologous protein-coding genes of N. oceanica found among a few representative microalgal species. a The percentages of homologous genes of P. tricornutum, T. pseudonana, A. anophagefferens, N. oceanica, and N. gaditana found in the nuclear genomes of E. huxleyi, G. theta, C. merolae, and G. sulphuraria. b The homologous protein-coding genes of N. oceanica found in A. anophagefferens but not in P. tricornutum, in P. tricornutum but not in A. anophagefferens and in both of them. c The number and percentage of the homologous genes of N. oceanica found in both A. anophagefferens and P. tricornutum (2478 in total) can be further partitioned into three patterns (I through III) and multi-copy genes. The pattern I contains the genes phylogenetically near to those of A. anophagefferens, while patterns II and III contain the genes phylogenetically far from those of A. anophagefferens

Fig. 4

The hypothetical route of N. oceanica speciation through cellular fusion and nuclear haploidization. The symbiont nucleus may have overthrown the host nucleus during speciation of Nannochloropsis. The cell fusion mode of speciation needs no evolution of new structure and function, which should aid to fast speciation of Nannochloropsis. Instead of free floating, the plastid homing in the host cytoplasm may be enveloped by either one or two layers of cytoplasmic reticulum, forming a continuum with nucleus and dividing simultaneously with nucleus