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. 2024 Jul 25;27(8):110575.
doi: 10.1016/j.isci.2024.110575. eCollection 2024 Aug 16.

Chromosome-scale genome assembly reveals insights into the evolution and ecology of the harmful algal bloom species Phaeocystis globosa Scherffel

Nansheng Chen  1   2   3   4 , Qing Xu  1   2   3   5 , Jianan Zhu  1   2   3   6 , Huiyin Song  1   2   3 , Liyan He  1   2   3 , Shuya Liu  1   2   3 , Xiuxian Song  1   2   3   6 , Yongquan Yuan  1   2   3 , Yang Chen  1   2   3   6 , Xihua Cao  1   2   3 , Zhiming Yu  1   2   6
Affiliations

Chromosome-scale genome assembly reveals insights into the evolution and ecology of the harmful algal bloom species Phaeocystis globosa Scherffel

Nansheng Chen et al. iScience. .

Abstract

The phytoplankton Phaeocystis globosa plays an important role in sulfur cycling and climate control, and can develop harmful algal blooms (HABs). Here we report a chromosome-scale reference genome assembly of P. globosa, which enable in-depth analysis of molecular underpinnings of important ecological characteristics. Comparative genomic analyses detected two-rounds of genome duplications that may have fueled evolutionary innovations. The genome duplication may have resulted in the formation of dual HiDP and LoDP dimethylsulphoniopropionate (DMSP) biosynthesis pathways in P. globosa. Selective gene family expansions may have strengthened biological pathways critical for colonial formation that is often associated with the development of algal blooms. The copy numbers of rhodopsin genes are variable in different strains, suggesting that rhodopsin genes may play a role in strain-specific adaptation to ecological factors. The successful reconstruction of the P. globosa genome sets up an excellent platform that facilitates in-depth research on bloom development and DMSP metabolism.

Keywords: Aquatic biology; Ecology; Environmental science; Evolutionary ecology; Genomics; Microbial genomics; Microbiology.

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Conflict of interest statement

The authors declare no competing interests.

Figures

None
Graphical abstract
Figure 1
Figure 1
Genomic features of P. globosa and comparative analysis of P. globosa and other algal species (A) Genomic landscape of the 23 chromosomes of the P. globosa genome assembled in this project. Track a represents 23 P globosa chromosomes (Mb); Tracks b–d represent distribution of gene density, repeat element density, and GC content, respectively (bin size = 100k); Track e represents syntenic blocks in the P. globosa genome. (B) Distribution of nine copies of ribosomal operons in chromosomes PglChr23 (eight copies) and PglChr16 (one single copy). Each copy consisted of an 18S rDNA, an internal transcribed spacer (ITS, including 5.8S rDNA), a 28S rDNA, and an IGS. Two adjacent copies are separated by a genomic sequence of various lengths. (C) Divergence distribution of transposable elements. (D) Whole genome duplication (WGD) events are estimated from the 4-fold degenerate synonymous sites of the third codons (4DTv) distance of homologous pairs in syntenic regions of P. globosa. (E) Venn diagram for orthologous protein-coding gene clusters in P. globosa, C. tobin, G. theta, and C. merolae. (F) Evolutionary analysis of single copy genes in P. globosa and selected species.
Figure 2
Figure 2
Genes involved in DMSP biosynthesis and degradation in P. globosa (A) Key genes in DMSP biosynthesis and degradation in P. globosa; (B) Phylogenetic analysis of PgMT2 genes; (C) Phylogenetic analysis of DSYB genes; (D) Phylogenetic analysis Alma genes; (E) Important functional domains identified in PgDSYB, PgTM2, and PgAlma.
Figure 3
Figure 3
Illustration of P. globosa colony formation-associated biological pathways impacted by gene family expansion (A) Glycan precursors and glycan biosynthesis. (B) Nitrogen metabolism. (C) Differential gene expression during P. globosa bloom development. Araf, arabinofuranose; Asn, glutamine; Fuc, fructose; Gal, galactose; GlcN, glucosamine; GlcNAc, N-Acetyl-glucosamine; Hyp, hydroxyproline; Man, mannose; Ser, serine; Xyl, xylose.
Figure 4
Figure 4
Genetic diversity and population genetics of P. globosa (A) Geographical locations of sampling sites and morphology for P. globosa strains. (B) Phylogenetic tree of 39 strains inferred from whole-genome SNPs, basing whole-genome resequencing results. (C) Pairwise comparison of a scaffold of the CNS00080 with its corresponding genomic region of reference strain CNS00066. Yellow rectangles represent coding sequences (CDSs), while blue rectangles represent PCGs. Gray ribbons represent corresponding genomic regions between these two strains. (D) Population structure of 13 strains isolated from the Beibu Gulf, with reference to P. globsa population in other regions. Population structure of P. globosa population, and the Beibu Gulf strain is shown separately. (E) Pairwise genomic sequence similarity of P. globosa strains.
Figure 5
Figure 5
Rich and diverse proton pump-type rhodopsin genes in the P. globosa (A) Putative proton pump-type rhodopsin genes annotated in the reference P. globosa strain (CNS00066). (B) Putative proton pump-type rhodopsin genes annotated in different P. globosa strains. (C) Gene structures of proton pump-type rhodopsin genes annotated in P. globosa strains. (D) Transmembrane domains annotated in the proton pump-type rhodopsin genes in P. globosa strains. (E) Peptide sequence alignment of the putative ketocarotenoid-binding region of rhodopsin genes. Amino acids corresponding to Gly156 of Salinibacter ruber xanthorhodopsin are highlighted in red. (F) Peptide sequence alignment of rhodopsin genes with eBAC31A08. Amino acids corresponding to 105 of eBAC31A08 are highlighted in red.
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