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A Streamlined and Predominantly Diploid Genome in the Tiny Marine Green Alga Chloropicon Primus

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A Streamlined and Predominantly Diploid Genome in the Tiny Marine Green Alga Chloropicon Primus ARTICLE https://doi.org/10.1038/s41467-019-12014-x OPEN A streamlined and predominantly diploid genome in the tiny marine green alga Chloropicon primus Claude Lemieux 1,3, Monique Turmel 1,3, Christian Otis 1 & Jean-François Pombert 2 Tiny marine green algae issued from two deep branches of the Chlorophyta, the Mamiello- phyceae and Chloropicophyceae, dominate different regions of the oceans and play key roles in planktonic communities. Considering that the Mamiellophyceae is the sole lineage of 1234567890():,; prasinophyte algae that has been intensively investigated, the extent to which these two algal groups differ in their metabolic capacities and cellular processes is currently unknown. To address this gap of knowledge, we investigate here the nuclear genome sequence of a member of the Chloropicophyceae, Chloropicon primus. Among the main biological insights that emerge from this 17.4 Mb genome, we find an unexpected diploid structure for most chromosomes and a propionate detoxification pathway in green algae. Our results support the notion that separate events of genome minimization, which entailed differential losses of genes/pathways, have occurred in the Chloropicophyceae and Mamiellophyceae, suggesting different strategies of adaptation to oceanic environments. 1 Département de biochimie, de microbiologie et de bio-informatique, Institut de Biologie Intégrative et des Systèmes, Université Laval, Québec, QC G1V 0A6, Canada. 2 Department of Biology, Illinois Institute of Technology, Chicago, IL 60616, USA. 3These authors contributed equally: Claude Lemieux, Monique Turmel. Correspondence and requests for materials should be addressed to C.L. (email: [email protected]) NATURE COMMUNICATIONS | (2019) 10:4061 | https://doi.org/10.1038/s41467-019-12014-x | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-019-12014-x reen algae are morphologically, ecologically, and phylo- insights into the nature of the first green algae and their patterns genetically diverse, and represent one of the most suc- of diversification. It has been suggested that the earliest-diverging G 1 fl cessful groups of photosynthetic eukaryotes ; yet our green algae were scaly agellates that were able to capture bac- knowledge about the genetic factors determining their ecological teria, although only a few extant prasinophytes such as Cymbo- success is still limited. Soon after their emergence about 1000 monas (Pyramimonadophyceae) exhibit a phagotrophic lifestyle1. Mya, early green algae split into two phyla: Chlorophyta, com- Among the independent prasinophyte lineages that have been prising the vast majority of extant species, and Streptophyta, identified so far, at least five (Prasinococcales, Mamiellophyceae, comprising charophyte algae and all land plants1–3. In recent Pycnococcaceae, Picocystophyceae, and Chloropicophyceae) years, the genomes of a number of photosynthetic green algae, comprise coccoid (no flagella, no scales) species of small size (≤5 mainly from the Chlorophyta, have been sequenced to unravel μm in diameter). A highly reduced, coccoid growth form is the evolutionary trajectories followed by ancestral green algae4–7, thought to confer a distinct advantage to planktonic algae because decipher cellular mechanisms such as the basis of multi- the resulting higher surface area to volume ratio enhances the cellularity8–11, pinpoint genes linked to adaptations to ecological efficiency of nutrient uptake, thus increasing competitiveness in niches12–15, and investigate metabolic networks, including routes an environment poor in nutrients; furthermore, a reduced size for the biosynthesis of highly valuable compounds for the helps to escape predators and promotes buoyancy21–23. industry16–19. The Mamiellophyceae comprises the smallest known free- Known for their important role in the global carbon cycle, the living eukaryote, the coccoid Ostreococcus tauri, and is the only green algae traditionally considered as prasinophytes constitute a prasinophyte lineage for which complete nuclear genomes are paraphyletic assemblage of unicellular, predominantly marine currently available (Fig. 1b). The tiny algae belonging to the three organisms at the base of the Chlorophyta2,20,21 (Fig. 1a). genera from the order Mamiellales—Ostreococcus, Micromonas Decoding their genomes is thus expected to yield important (no scales and one flagellum), and Bathycoccus (scales but no a b Genome Chromosome Gene Chlorophyceae size (Mb) no. no. Ulvophyceae 0.1 Volvox 131.2 19 15,494 Trebouxiophyceae Gonium 148.8 n/a 16,526 Chlorodendrophyceae Chlamydomonas Core Chlorophyta 111.1 17 18,115 Pedinophyceae Chlorella 46.2 12 9833 Chloropicophyceae Auxenochlorella 22.9 n/a 7114 Picocystophyceae Coccomyxa 48.8 20 9947 Pycnococcaceae Chlorophyta Chloropicon 17.4 20 8693 Nephroselmidophyceae O. lucimarinus 13.2 21 7839 Mamiellophyceae O. tauri 12.5 20 7942 Pyramimonadophyceae Bathycoccus 15.0 19 7847 Palmophyllophyceae M. commoda 21.0 17 10,163 M. pusilla 22.0 21 10,707 Streptophyta charophytes + land plants Klebsormidium 103.9 n/a 16,244 cd 1.4 Intergenic Klebsormidium Mamiellophyceae Intron (5645) (5882) 1.2 CDS 139 141 264 1 0.8 4975 0.6 390 504 0.4 317 0.2 Number of SNPs and indels/kb 0 I II V X III XI IV VI IX XII Core Chlorophyta VII XV XX XIII VIII XVI XIX XIV XVII (6186) XVIII Chromosome Fig. 1 Phylogenetic position and genome features of Chloropicon relative to the 12 green algae selected for comparative analyses. a Schematic diagram depicting the main lineages of the Chloroplastida. The algae of our study group belong to the highlighted lineages. b Nuclear phylogenomic tree inferred from 792 concatenated proteins encoded by single-copy genes and comparison of genome sizes, numbers of chromosomes/DNA assemblies, and sizes of protein-coding gene repertoires. c Venn diagram showing the numbers of protein-coding genes that Chloropicon shares with the Mamiellophyceae, core chlorophytes and Klebsormidium. d Density of SNPs and small indels in coding (blue bars) and non-coding (intron, orange bars; intergenic sequences, gray bars) regions of individual Chloropicon chromosomes. The source data of d are provided as a Source Data file 2 NATURE COMMUNICATIONS | (2019) 10:4061 | https://doi.org/10.1038/s41467-019-12014-x | www.nature.com/naturecommunications NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-019-12014-x ARTICLE flagella)—are typically found in coastal waters although they have 3723 further assigned to KEGG orthologs. Nearly 78% of the been observed in open oceanic waters21. For each of these genera, predicted Chloropicon proteins are shared with the 12 other green cryptic species derived from separate clades or strains repre- algae used in our genome comparisons (Fig. 1c). Of the 1909 senting different ecotypes were targeted for genome proteins unique to Chloropicon, only 163 featured putative analysis4–7,24,25. All examined mamiellophyceans possess reduced functions as inferred using our annotation pipeline and genomes (12–22 Mb with only ~8000–11,000 predicted genes, GhostKOALA, and 82, 3, and 145 yielded strongest hits to Fig. 1b) compared to freshwater/terrestrial green algae and the proteins of bacteria, archaea, and eukaryotes from non-green prasinophyte Cymbomonas tetramitiformis26, implying that gen- lineages, respectively, in BLASTP searches (cutoff E-value = 1.0E- ome minimization occurred along cell reduction and simplifica- 10) against the nr database of the National Center for tion in the course of prasinophyte evolution22. The Ostreococcus Biotechnology Information (NCBI). genus exhibits the smallest genomes among sequenced green As an independent method to assess the quality and algae and as in other unicellular green algae, each chromosome is completeness of our genome assembly and annotation, we present in one copy. Within each genus of the Mamiellophyceae, queried using BUSCO32 the annotated proteins of Chloropicon species divergence or adaptation to ecological niches was linked and 13 other green algae against the OrthoDB v10 database, to dynamic genome evolution, with dispensable and fast-evolving which contains the collection of 2168 near-universal single-copy genes predominantly located in the smallest of the two outlier orthologs found in the Chlorophyta (Supplementary Fig. 1). The chromosomes displaying lower GC content. The small outlier Chloropicon proteins accounted for 82.5% of this collection, a chromosome is thought to be specialized in defense against value slightly lower than those obtained for Ostreococcus tauri viruses27, while the larger appears to contain the sex-determining (88.9%), Bathycoccus (86.9%), and Gonium (86.9%). region (SDR)4,6,28. As observed for the Mamiellales, there is a limited number of Recently, a late-diverging lineage of pico/nano-prasinophytes, gene families in Chloropicon, with copies of identical or very named Chloropicophyceae, has emerged as playing a key role in similar sequences often occurring as tandem repeats. The largest marine phytoplankton communities, especially in moderately families include genes that are dispersed throughout the genome oligotrophic waters29,30. This genetically diversified lineage, and these encode polyketide synthases (12 members, Supple- which includes two genera (Chloropicon and Chloroparvula), mentary Data 3), sialyltransferases (59 members, Supplementary occupies a sister position relative to the core Chlorophyta2,20,30,31 Data 4), guanylyl cyclases (30 members, Supplementary Data 5), (Fig. 1a) and although
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