Genome analyses provide insights into the evolution and adaptation of the eukaryotic Picophytoplankton Mychonastes homosphaera

Abstract

Background: Picophytoplankton are abundant and can contribute greatly to primary production in eutrophic lakes. Mychonastes species are among the common eukaryotic picophytoplankton in eutrophic lakes. We used third-generation sequencing technology to sequence the whole genome of Mychonastes homosphaera isolated from Lake Chaohu, a eutrophic freshwater lake in China.

Result: The 24.23 Mbp nuclear genome of M.homosphaera, harboring 6649 protein-coding genes, is more compact than the genomes of the closely related Sphaeropleales species. This genome streamlining may be caused by a reduction in gene family number, intergenic size and introns. The genome sequence of M.homosphaera reveals the strategies adopted by this organism for environmental adaptation in the eutrophic lake. Analysis of cultures and the protein complement highlight the metabolic flexibility of M.homosphaera, the genome of which encodes genes involved in light harvesting, carbohydrate metabolism, and nitrogen and microelement metabolism, many of which form functional gene clusters. Reconstruction of the bioenergetic metabolic pathways of M.homosphaera, such as the lipid, starch and isoprenoid pathways, reveals characteristics that make this species suitable for biofuel production.

Conclusion: The analysis of the whole genome of M. homosphaera provides insights into the genome streamlining, the high lipid yield, the environmental adaptation and phytoplankton evolution.

Keywords: Adaptation; Genome; Mychonastes; Picophytoplankton.

Fig. 1

Phylogenetic tree of 18S rDNA sequences using the maximum likelihood method

Fig. 2

Size distributions of nuclear and organellar genomes of M.homosphaera, two Sphaeropleales species (M.neglectum and R.subcapitata) and two picophytoplankton species (O.tauri and M.commoda)

Fig. 3

Chloroplast genome of M.homosphaera

Fig. 4

Mitochondrial genome of M.homosphaera

Fig. 5

Venn diagram of the gene families of M.homosphaera and other Viridiplantae

Fig. 6

Venn diagram of the gene families of M.homosphaera, two Sphaeropleales species (M.neglectum and R.subcapitata) and a chlorophyte species (C.reinhardtii)

Fig. 7

Top BLASTp hits of M.homosphaera compared with the nonredundant protein database

Fig. 8

Gene Ontology (GO) assignments for M.homosphaera The 31 most extensive GO terms of the three GO supercategories “molecular function” (blue), “cellular component” (green) and “biological process” (red) are shown

Fig. 9

Functional comparison of M.homosphaera and other phytoplankton according to KEGG classification. (a), (b), (c) and (d) represent cellular processes, environmental information processing, genetic information processing and metabolism, respectively

Fig. 10

Carbohydrate metabolism, nutrient transport and photoreceptors in Mychonastes homosphaera. The metabolites are shown in black, and the enzymes are shown in yellow. G3P: glyceraldehyde 3-phosphate, MA: malic acid, OAA: oxaloacetate, PEP: phosphoenolpyruvate, 3-PGA: 3-phosphoglycerate, Pyr: pyruvate, RuBP: ribulose-1,5-bisphosphate, BCT: bicarbonate transporter, CA: carbonic anhydrase, MDH: malate dehydrogenase, ME: malic enzyme, PC: pyruvate carboxylase, PEPC: phosphoenolpyruvate carboxylase, PPDK: pyruvate, phosphate dikinase, RuBisCO: ribulose-1,5-bisphosphate carboxylase oxygenase, PHO: phototropins, CRY: cryptochromes, PHY: phytochrome. In nutrient transport, a solid line or circle indicates that the gene has been identified, and a dashed circle indicates that the gene may be present. Metabolic pathway reconstruction was performed based on the KEGG database

Fig. 11

Fatty acid biosynthesis pathways (a) and the TCA (glycerolipid) metabolism pathways (b) of Mychonastes homosphaera. ACC: acetyl-CoA carboxylase, MAT: malonyl-CoA:ACP transacylase, KAS3: the beta-ketoacyl-acyl-carrier protein synthase 3, KAS1/2: the beta-ketoacyl-acyl-carrier-protein synthase, KAR: the 3-oxoacyl-ACP reductase, HAD: the beta-hydroxyacyl-ACP dehydrase, EAR: enoyl-ACP reductase, OAH: oleoyl-acyl-carrier-protein hydrolase, PAH: palmitoyl-protein thioesterase, GK: glycerol kinase, GPAT: glycerol-3phosphate O-acyltransferase, AGPAT: 1-acylglycerol-3phosphate O-acyltransferase, PP: phosphatidate phosphatase, DGAT: acyl-CoA:diacylglycerol acyltransferase, PDAT: phospholipid:diacylglycerol acyltransferase. Each coloured square represents a homologous gene, and different color represent different species. Pathway reconstruction was performed for fatty acid biosynthesis and TCA synthesis based on the KEGG database

Fig. 12

Starch synthesis (a) and degradation (b) in Mychonastes homosphaera. glgC: glucose-1-phosphate adenylyltransferase, WAXY: granule-bound starch synthase, glgA: starch synthase, glgB: glucan branching enzyme, ISA: isoamylase, R1: alpha-glucan, water dikinase, PWD: phosphoglucan, water dikinase, amyA: alpha-amylase, amyB: beta-amylase, malQ: 4-alpha-glucanotransferase, glgP: starch phosphorylase. Pathway reconstruction was performed for starch synthesis and starch degradation based on the KEGG database

Fig. 13

Histogram with raw read length vs. number of raw reads