Skip to main content
SpringerLink
Log in

Reconstructing Dynamic Evolutionary Events in Diatom Nuclear and Organelle Genomes

  • Chapter
  • First Online:
The Molecular Life of Diatoms

  • 2003 Accesses

Abstract

The diatoms evolved within the stramenopiles, an ecologically important and diverse assemblage of eukaryotes that includes both photosynthetic macrophytes and microalgae, as well as non-photosynthetic heterotrophs and parasites. The evolutionary history of the stramenopiles, which stretches back to the Palaeozoic, has been marked by the acquisition of chloroplasts in a recent common ancestor of their photosynthetic members, the ochrophytes; and progressive gains of genes in the nuclear genome by horizontal and endosymbiotic gene transfer. Here, we place diatoms in their actual evolutionary context within the stramenopiles; identify gene transfers that have shaped the coding content of the diatom nucleus; and profile sources of differences in chloroplast and mitochondrial genome content between different stramenopiles including diatoms. We underline the importance of considering diatoms as evolutionary mosaics, supported by genes of bacterial, red, green and other eukaryotic algal origins, as illustrated by multiple phylogenomic studies realised over the last two decades; and the relatively limited changes to organelle genome content in diatoms compared to other stramenopile lineages. We further identify a previously undocumented transfer of a novel open reading frame of the chloroplasts of green algae into the ochrophytes, underlining the importance of changes in organelle and nuclear gene content, in defining the current biology of diatoms.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 299.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

ATP:

adenosine triphosphate

BLAST:

Basic Local Alignment Search Tool

DNA:

deoxyribonucleic acid

ER:

endoplasmic reticulum

GFP:

green fluorescent protein

GTR:

generalised time reversible substitution model

HGT:

horizontal gene transfer

ISIP:

iron-stress-induced protein

JTT:

Jones-Taylor-Thornton substitution model

Lhc:

light harvesting complex

ORF:

open reading frame

Pt:

Phaeodactylum tricornutum

rRNA:

ribosomal ribonucleic acid

SAR:

stramenopiles, alveolates and rhizaria

Tat:

twin arginine transporter

Tp:

Thalassiosira pseudonana

tRNA:

transfer ribonucleic acid

WAG:

Whelan and Goldman substitution model

References

  • Adl SM et al (2012) The revised classification of eukaryotes. J Euk Microbiol 59:429–493

    Article  PubMed  Google Scholar 

  • Allen AE et al (2008) Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. Proc Natl Acad Sci U S A 105:10438–10443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • An SM, Noh JH, Choi DH, Lee JH, Yang EC (2016) Repeat region absent in mitochondrial genome of tube-dwelling diatom Berkeleya fennica (Naviculales, Bacillariophyceae). Mitochondrial DNAl 27:2137–2138

    CAS  Google Scholar 

  • Andersen RA, Saunders GW, Paskind MP, Sexton JP (1993) Ultrastructure and 18S ribosomal RNA gene sequence for Pelagomonas calceolata gen. Et sp. nov. and the description of a new algal class, the pelagophyceae classis nov. J Phycol 29:701–715

    Article  CAS  Google Scholar 

  • Armbrust EV et al (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86

    Article  CAS  PubMed  Google Scholar 

  • Ashworth MP, Ruck EC, Lobban CS, Romanovicz DK, Theriot EC (2012) A revision of the genus Cyclophora and description of Astrosyne gen. Nov (Bacillariophyta), two genera with the pyrenoids contained within pseudosepta. Phycologia 51:684–699

    Article  Google Scholar 

  • Basu S et al (2017) Finding a partner in the ocean: molecular and evolutionary bases of the response to sexual cues in a planktonic diatom. New Phytol 215:140–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bečková M et al (2017) Association of Psb28 and Psb27 proteins with PSII-PSI supercomplexes upon exposure of Synechocystis sp. PCC 6803 to high light. Mol Plant 10:62–72

    Article  PubMed  CAS  Google Scholar 

  • Bhattacharya D et al (2013) Genome of the red alga Porphyridium purpureum. Nat Commun 4:1941

    Article  PubMed  CAS  Google Scholar 

  • Bowler C et al (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–244

    Article  CAS  PubMed  Google Scholar 

  • Brawley SH et al (2017) Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta). Proc Natl Acad Sci U S A 114:6361–6370

    Article  CAS  Google Scholar 

  • Brown JW, Sorhannus U (2010) A molecular genetic timescale for the diversification of autotrophic stramenopiles (Ochrophyta): substantive underestimation of putative fossil ages. PLoS One 6:12759

    Article  CAS  Google Scholar 

  • Browning TJ et al (2017) Nutrient co-limitation at the boundary of an oceanic gyre. Nature 551:242–246

    Article  CAS  PubMed  Google Scholar 

  • Brunson JK et al (2018) Biosynthesis of the neurotoxin domoic acid in a bloom-forming diatom. Science 361:1356–1358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Büchel C (2015) Evolution and function of light harvesting proteins. J Plant Physiol 172:62–75

    Article  PubMed  CAS  Google Scholar 

  • Buck JM et al (2019) Lhcx proteins provide photoprotection via thermal dissipation of absorbed light in the diatom Phaeodactylum tricornutum. Nat Commun 10:4167

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Burki F et al (2007) Phylogenomics reshuffles the eukaryotic supergroups. PLoS One 2:000790

    Article  CAS  Google Scholar 

  • Burki F et al (2012) Re-evaluating the green versus red signal in eukaryotes with secondary plastid of red algal origin. Genom Biol Evol 4:626–635

    Article  CAS  Google Scholar 

  • Burki F et al (2014) Endosymbiotic gene transfer in tertiary plastid-containing dinoflagellates. Eukaryot Cell 13:00299–00213

    Article  CAS  Google Scholar 

  • Burki F et al (2016) Untangling the early diversification of eukaryotes: a phylogenomic study of the evolutionary origins of Centrohelida, Haptophyta and Cryptista. Proc Biol Sci 283:20152802

    PubMed  PubMed Central  Google Scholar 

  • Caputi L et al (2019) Community-level responses to iron availability in open ocean planktonic ecosystems. Glob Biogeochem Cycles 10:1029

    Google Scholar 

  • Carradec Q et al (2018) A global ocean atlas of eukaryotic genes. Nat Commun 9:373

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cattolico RA et al (2008) Chloroplast genome sequencing analysis of Heterosigma akashiwo CCMP452 (West Atlantic) and NIES293 (West Pacific) strains. BMC Genomics 9:211

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cavalier-Smith T (1998) A revised six-kingdom system of life. Biol Rev 73:203–266

    Article  CAS  PubMed  Google Scholar 

  • Cavalier-Smith T (1999) Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J Euk Microbiol 46:347–366

    Article  CAS  PubMed  Google Scholar 

  • Coesel S, Obornik M, Varela J, Falciatore A, Bowler C (2008) Evolutionary origins and functions of the carotenoid biosynthetic pathway in marine diatoms. PLoS One 3:2896

    Article  CAS  Google Scholar 

  • Collén J et al (2013) Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc Natl Acad Sci U S A 110:5247–5252

    Article  PubMed  PubMed Central  Google Scholar 

  • Crowell RM, Nienow JA, Cahoon AB (2019) The complete chloroplast and mitochondrial genomes of the diatom Nitzschia palea (Bacillariophyceae) demonstrate high sequence similarity to the endosymbiont organelles of the dinotom Durinskia baltica. J Phycol 55:352–364

    Article  CAS  PubMed  Google Scholar 

  • Dagan T, Martin W (2009) Seeing green and red in diatom genomes. Science 324:1651–1652

    Article  CAS  PubMed  Google Scholar 

  • Dautermann O, Lohr M (2017) A functional zeaxanthin epoxidase from red algae shedding light on the evolution of light-harvesting carotenoids and the xanthophyll cycle in photosynthetic eukaryotes. Plant J 92:879–891

    Article  CAS  PubMed  Google Scholar 

  • Derelle R, López-García P, Timpano H, Moreira D (2016) A phylogenomic framework to study the diversity and evolution of stramenopiles (heterokonts). Mol Biol Evol 33:2890–2898

    Article  CAS  PubMed  Google Scholar 

  • Deschamps P, Moreira D (2012) Re-evaluating the green contribution to diatom genomes. Genome Biol Evol 4:683–688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dorrell RG, Bowler C (2017) Secondary plastids of stramenopiles. In: Hirakawa Y (ed) Adv. Bot. Res.: secondary endosymbiosis, vol 84. Elsevier, pp 57–103

    Chapter  Google Scholar 

  • Dorrell RG, Howe CJ (2012) What makes a chloroplast? Reconstructing the establishment of photosynthetic symbioses. J Cell Sci 125:1865–1875

    CAS  PubMed  Google Scholar 

  • Dorrell RG, Smith AG (2011) Do red and green make brown?: perspectives on plastid acquisitions within chromalveolates. Eukaryot Cell 10:856–868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dorrell RG et al (2017a) Chimeric origins of ochrophytes and haptophytes revealed through an ancient plastid proteome. elife 6:23717

    Article  Google Scholar 

  • Dorrell RG et al (2017b) Progressive and biased divergent evolution underpins the origin and diversification of peridinin dinoflagellate plastids. Mol Biol Evol 34:361–379

    CAS  PubMed  Google Scholar 

  • Dorrell RG et al (2019) Principles of plastid reductive evolution illuminated by nonphotosynthetic chrysophytes. Proc Natl Acad Sci U S A 116:6914–6923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dorrell RG et al (2021) Phylogenomic fingerprinting of tempo and functions of horizontal gene transfer within ochrophytes. Proc Natl Acad Sci U S A 118:2009974118

    Article  CAS  Google Scholar 

  • Ehara M, Inagaki Y, Watanabe KI, Ohama T (2000) Phylogenetic analysis of diatom coxI genes and implications of a fluctuating GC content on mitochondrial genetic code evolution. Curr Genet 37:29–33

    Article  CAS  PubMed  Google Scholar 

  • Elias M, Patron NJ, Keeling PJ (2009) The RAB family GTPase Rab1A from plasmodium falciparum defines a unique paralog shared by chromalveolates and Rhizaria. J Eukaryot Microbiol 56:348–356

    Article  CAS  PubMed  Google Scholar 

  • Eme L, Gentekaki E, Curtis B, Archibald JM, Roger AJ (2017) Lateral gene transfer in the adaptation of the anaerobic parasite Blastocystis to the gut. Curr Biol 27:807–820

    Article  CAS  PubMed  Google Scholar 

  • Fan X et al (2020) Phytoplankton pangenome reveals extensive prokaryotic horizontal gene transfer of diverse functions. Sci Adv 6:0011

    Google Scholar 

  • Fork DC, Herbert SK, Malkin S (1991) Light energy distribution in the brown alga Macrocystis pyrifera (giant kelp). Plant Physiol 95:731–739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frommolt R et al (2008) Ancient recruitment by chromists of green algal genes encoding enzymes for carotenoid biosynthesis. Mol Biol Evol 25:2653–2667

    Article  CAS  PubMed  Google Scholar 

  • Gao X, Bowler C, Kazamia E (2021) Iron metabolism strategies in diatoms. J Exp Bot 72:2165–2180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao L, Zhou Y, Wang ZW, Su YJ, Wang T (2011) Evolution of the rpoB-psbZ region in fern plastid genomes: notable structural rearrangements and highly variable intergenic spacers. BMC Plant Biol 11:64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gile GH, Moog D, Slamovits CH, Maier UG, Archibald JM (2015) Dual organellar targeting of aminoacyl-tRNA synthetases in diatoms and cryptophytes. Genome Biol Evol 7:1728–1742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graupner N et al (2018) Evolution of heterotrophy in chrysophytes as reflected by comparative transcriptomics. FEMS Microbiol Ecol 94:fiy039

    Article  PubMed Central  CAS  Google Scholar 

  • Guillory WX et al (2018) Recurrent loss, horizontal transfer, and the obscure origins of mitochondrial introns in diatoms (Bacillariophyta). Genom Biol Evol 10:1504–1515

    Article  CAS  Google Scholar 

  • Hadariová L, Vesteg M, Hampl V, Krajčovič J (2018) Reductive evolution of chloroplasts in non-photosynthetic plants, algae and protists. Curr Genet 64:365–387

    Article  PubMed  CAS  Google Scholar 

  • Hamsher SE et al (2019) Extensive chloroplast genome rearrangement amongst three closely related Halamphora spp. (Bacillariophyceae), and evidence for rapid evolution as compared to land plants. PLoS One 14:e0217824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han KY et al (2019) Dictyochophyceae plastid genomes reveal unusual variability in their organization. J Phycol 55:1166–1180

    Article  CAS  PubMed  Google Scholar 

  • Hehenberger E, Burki F, Kolisko M, Keeling PJ (2016) Functional relationship between a dinoflagellate host and its diatom endosymbiont. Mol Biol Evol 33:2376–2390

    Article  CAS  PubMed  Google Scholar 

  • Hendry KR et al (2018) Competition between silicifiers and non-silicifiers in the past and present ocean and its evolutionary impacts. Front Mar Sci 5:22

    Article  Google Scholar 

  • Hildebrand M et al (1991) Plasmids in diatom species. J Bacteriol 173:5924–5927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ichinomiya M, Lopes dos Santos A, Gourvil P, Yoshikawa S, Kamiya M, Ohki K, Audic S, de Vargas C, Noël MH, Vaulot D, Kuwata A (2016) Diversity and oceanic distribution of the Parmales (Bolidophyceae), a picoplanktonic group closely related to diatoms. ISME J 10:2419–2436

    Article  PubMed  PubMed Central  Google Scholar 

  • Imanian B, Pombert JF, Dorrell RG, Burki F, Keeling PJ (2012) Tertiary endosymbiosis in two dinotoms has generated little change in the mitochondrial genomes of their dinoflagellate hosts and diatom endosymbionts. PLoS One 7:e43763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Imanian B, Pombert JF, Keeling PJ (2010) The complete plastid genomes of the two 'dinotoms' Durinskia baltica and Kryptoperidinium foliaceum. PLoS One 5:107111

    Article  CAS  Google Scholar 

  • Ishida K, Cavalier-Smith T, Green BR (2000) Endomembrane structure and the chloroplast protein targeting pathway in Heterosigma akashiwo (Raphidophyceae, Chromista). J Phycol 36:1135–1144

    Article  CAS  Google Scholar 

  • Jacobs JD et al (1992) Characterization of two circular plasmids from the marine diatom Cylindrotheca fusiformis: plasmids hybridize to chloroplast and nuclear DNA. Mol Gen Genet 233:302–310

    Article  CAS  PubMed  Google Scholar 

  • Janouskovec J, Horák A, Oborník M, Lukes J, Keeling PJ (2010) A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci U S A 107:10949–10954

    Article  PubMed  PubMed Central  Google Scholar 

  • Janouškovec J et al (2017) A new lineage of eukaryotes illuminates early mitochondrial genome reduction. Curr Biol 27:3717–3724.e3715

    Article  PubMed  CAS  Google Scholar 

  • Jiroutova K, Koreny L, Bowler C, Obornik M (2010) A gene in the process of endosymbiotic transfer. PLoS One 5:013234

    Article  CAS  Google Scholar 

  • Jirsová D, Füssy Z, Richtová J, Gruber A, Oborník M (2019) Morphology, ultrastructure, and mitochondrial genome of the marine non-photosynthetic bicosoecid Cafileria marina gen. Et sp. nov. Microorganisms 7:240

    Article  PubMed Central  CAS  Google Scholar 

  • Kamikawa R, Azuma T, Ishii KI, Matsuno Y, Miyashita H (2018) Diversity of organellar genomes in non-photosynthetic diatoms. Protist 169:351–361

    Article  CAS  PubMed  Google Scholar 

  • Kamikawa R et al (2015a) Multiple losses of photosynthesis in Nitzschia (Bacillariophyceae). Phycol Res 63:19–28

    Article  CAS  Google Scholar 

  • Kamikawa R et al (2015b) Proposal of a twin arginine translocator system-mediated constraint against loss of ATP synthase genes from nonphotosynthetic plastid genomes. Mol Biol Evol 32:2598–2604

    Article  CAS  PubMed  Google Scholar 

  • Kamikawa R et al (2017) A non-photosynthetic diatom reveals early steps of reductive evolution in plastids. Mol Biol Evol 34:2355–2366

    Article  CAS  PubMed  Google Scholar 

  • Kayama M et al (2020) Highly reduced plastid genomes of the non-photosynthetic dictyochophyceans Pteridomonas spp. (Ochrophyta, SAR) are retained for tRNA-Glu-based organellar heme biosynthesis. Front Plant Sci 11:602455

    Article  PubMed  PubMed Central  Google Scholar 

  • Kazamia E et al (2018) Endocytosis-mediated siderophore uptake as a strategy for Fe acquisition in diatoms. Sci Adv 4:4536

    Article  CAS  Google Scholar 

  • Keeling PJ, Palmer JD (2008) Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 9:605–618

    Article  CAS  PubMed  Google Scholar 

  • Kim JI et al (2017) Evolutionary dynamics of cryptophyte plastid genomes. Genome Biol Evol 9:1859–1872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klinger CM et al (2018) Plastid transcript editing across dinoflagellate lineages shows lineage-specific application but conserved trends. Genom Biol Evol 10:1019–1038

    Article  CAS  Google Scholar 

  • Kowallik KV, Stoebe B, Schaffran I, Kroth-Pancic P, Freier U (1995) The chloroplast genome of a chlorophyll a+c-containing alga, Odontella sinensis. Plant Mol Biol Reporter 13:336–342

    Article  CAS  Google Scholar 

  • Krasovec M, Sanchez-Brosseau S, Piganeau G (2019) First estimation of the spontaneous mutation rate in diatoms. Genom Biol Evol 11:1829–1837

    Article  CAS  Google Scholar 

  • Kretschmann J, Žerdoner Čalasan A, Gottschling M (2018) Molecular phylogenetics of dinophytes harboring diatoms as endosymbionts (Kryptoperidiniaceae, Peridiniales), with evolutionary interpretations and a focus on the identity of Durinskia oculata from Prague. Mol Phylogenet Evol 118:392–402

    Article  PubMed  Google Scholar 

  • Kuczynska P, Jemiola-Rzeminska M, Strzalka K (2015) Photosynthetic pigments in diatoms. Mar Drugs 13:5847–5881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larkum AWD, Lockhart PJ, Howe CJ (2007) Shopping for plastids. Trends Plant Sci 12:189–195

    Article  CAS  PubMed  Google Scholar 

  • Lax G et al (2018) Hemimastigophora is a novel supra-kingdom-level lineage of eukaryotes. Nature 564:410–414

    Article  CAS  PubMed  Google Scholar 

  • Le Corguillé G et al (2009) Plastid genomes of two brown algae, Ectocarpus siliculosus and Fucus vesiculosus: further insights on the evolution of red-algal derived plastids. BMC Evol Biol 9:253

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leliaert F et al (2016) Chloroplast phylogenomic analyses reveal the deepest-branching lineage of the chlorophyta, Palmophyllophyceae class nov. Sci Rep 6:25367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leonard G et al (2018) Comparative genomic analysis of the 'pseudofungus' Hyphochytrium catenoides. Open Biol 8:170184

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Levesque CA et al (2010) Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol 11:73

    Article  CAS  Google Scholar 

  • Li L et al (2020) The genome of Prasinoderma coloniale unveils the existence of a third phylum within green plants. Nat Ecol Evol 4:1220–1231

    Article  PubMed  PubMed Central  Google Scholar 

  • Lommer M et al (2010) Recent transfer of an iron-regulated gene from the plastid to the nuclear genome in an oceanic diatom adapted to chronic iron limitation. BMC Genomics 11:718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Magee AM et al (2010) Localized hypermutation and associated gene losses in legume chloroplast genomes. Genome Res 20:1700–1710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsuzaki M et al (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657

    Article  CAS  PubMed  Google Scholar 

  • McQuaid JB et al (2018) Carbonate-sensitive phytotransferrin controls high-affinity iron uptake in diatoms. Nature 555:534–537

    Article  CAS  PubMed  Google Scholar 

  • Méheust R, Zelzion E, Bhattacharya D, Lopez P, Bapteste E (2016) Protein networks identify novel symbiogenetic genes resulting from plastid endosymbiosis. Proc Natl Acad Sci U S A 113:3579–3584

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mock T et al (2017) Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus. Nature 541:536–540

    Article  CAS  PubMed  Google Scholar 

  • Moll KM et al (2017) Strategies for optimizing BioNano and dovetail explored through a second reference quality assembly for the legume model, Medicago trunculata. BMC Genom 18:578

    Article  CAS  Google Scholar 

  • Morozov AA, Galachyants YP (2019) Diatom genes originating from red and green algae: implications for the secondary endosymbiosis models. Mar Genomics 45:72–78

    Article  CAS  PubMed  Google Scholar 

  • Moustafa A et al (2009) Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324:1724–1726

    Article  CAS  PubMed  Google Scholar 

  • Muñoz-Gómez SAM-F, Durnin FG, Colp K, Grisdale M, Archibald CJ, Slamovits JM (2017) The new red algal subphylum proteorhodophytina comprises the largest and most divergent plastid genomes known. Curr Biol 27:1677–1684

    Article  PubMed  CAS  Google Scholar 

  • Nash EA et al (2007) Organization of the mitochondrial genome in the dinoflagellate Amphidinium carterae. Mol Biol Evol 24:1528–1536

    Article  CAS  PubMed  Google Scholar 

  • Nonoyama T et al (2019) Metabolic innovations underpinning the origin and diversification of the diatom chloroplast. Biomol Ther 9:322

    CAS  Google Scholar 

  • Noordally ZB et al (2013) Circadian control of chloroplast transcription by a nuclear-encoded timing signal. Science 339:1316–1319

    Article  CAS  PubMed  Google Scholar 

  • Novák Vanclová AMG et al (2020) Metabolic quirks and the colourful history of the Euglena gracilis secondary plastid. New Phytol 225:1578–1592

    Article  PubMed  CAS  Google Scholar 

  • Ong HC et al (2010) Analyses of the commplete chloroplast genome sequences of two members of the Pelagophyceae: Aureococcus anophageferrens CCMP1984 and Aureooumbra lagunensis CCMP 1507. J Phycol 46:602–615

    Article  CAS  Google Scholar 

  • Onyshchenko A, Ruck EC, Nakov T, Alverson AJ (2019) A single loss of photosynthesis in the diatom order Bacillariales (Bacillariophyta). Am J Bot 106:560–572

    Article  PubMed  Google Scholar 

  • Oudot-Le Secq MP, Green BR (2011) Complex repeat structures and novel features in the mitochondrial genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana. Gene 476:20–26

    Article  CAS  PubMed  Google Scholar 

  • Parfrey LW, Lahr DJ, Knoll AH, Katz LA (2011) Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci U S A 108:13624–13629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parks MB, Wickett NJ, Alverson AJ (2018) Signal, uncertainty, and conflict in phylogenomic data for a diverse lineage of microbial eukaryotes (diatoms, Bacillariophyta). Mol Biol Evol 35:80–93

    Article  CAS  PubMed  Google Scholar 

  • Pendergrass A, Roberts WR, Ruck EC, Lewis JA, Alverson AJ (2020) The genome of the nonphotosynthetic diatom, Nitzschia sp.: insights into the metabolic shift to heterotrophy and the rarity of loss of photosynthesis in diatoms. bioRXiv 05.28.115543

    Google Scholar 

  • Ponce-Toledo RI, López-García P, Moreira D (2019) Horizontal and endosymbiotic gene transfer in early plastid evolution. New Phytol 224:618–624

    Article  PubMed  PubMed Central  Google Scholar 

  • Prasetiya F et al (2019) Haslea nusantara (Bacillariophyceae), a new blue diatom from the Java Sea, Indonesia: morphology, biometry and molecular characterization. Plant Ecol Evol 152(15)

    Google Scholar 

  • Qiu H, Lee JM, Yoon HS, Bhattacharya D (2017) Hypothesis: gene-rich plastid genomes in red algae may be an outcome of nuclear genome reduction. J Phycol 53:715–719

    Article  CAS  PubMed  Google Scholar 

  • Rastogi A et al (2018) Integrative analysis of large scale transcriptome data draws a comprehensive landscape of Phaeodactylum tricornutum genome and evolutionary origin of diatoms. Sci Rep 8:4834

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ravin NV et al (2010) Complete sequence of the mitochondrial genome of a diatom alga Synedra acus and comparative analysis of diatom mitochondrial genomes. Curr Genet 56:215–223

    Article  CAS  PubMed  Google Scholar 

  • Raymond JA, Kim HJ (2012) Possible role of horizontal gene transfer in the colonization of sea ice by algae. PLoS One 7:e35968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren Y et al (2020) Nucleotide substitution rates of diatom plastid encoded protein genes are correlated with genome architecture. Sci Rep 10:14358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rhoads A, Au KF (2015) PacBio sequencing and its applications. Genom Proteom Bioinformat 13:278–289

    Article  Google Scholar 

  • Rodolfi L et al (2009) Microalgae for oil: strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol Bioeng 102:100–112

    Article  CAS  PubMed  Google Scholar 

  • Ruck EC, Linard SR, Nakov T, Theriot EC, Alverson AJ (2017) Hoarding and horizontal transfer led to an expanded gene and intron repertoire in the plastid genome of the diatom, Toxarium undulatum (Bacillariophyta). Curr Genet 63:499–507

    Article  CAS  PubMed  Google Scholar 

  • Sabir JSM et al (2014) Conserved gene order and expanded inverted repeats characterize plastid genomes of Thalassiosirales. PLoS One 9:107854

    Article  CAS  Google Scholar 

  • Sato S et al (2020) Genome-enabled phylogenetic and functional reconstruction of an araphid pennate diatom Plagiostriata sp. CCMP470, previously assigned as a radial centric diatom, and its bacterial commensal. Sci Rep 10:9449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sekiguchi H, Moriya M, Nakayama T, Inouye I (2002) Vestigial chloroplasts in heterotrophic stramenopiles Pteridomonas danica and Ciliophrys infusionum (Dictyochophyceae). Protist 153:157–167

    Article  CAS  PubMed  Google Scholar 

  • Ševčíková T et al (2015) Updating algal evolutionary relationships through plastid genome sequencing: did alveolate plastids emerge through endosymbiosis of an ochrophyte? Sci Rep 5:10134

    Article  PubMed  PubMed Central  Google Scholar 

  • Ševčíková T et al (2016) A comparative analysis of mitochondrial genomes in eustigmatophyte algae. Genom Biol Evol 8:705–722

    Article  Google Scholar 

  • Ševcíková T et al (2019) Plastid genomes and proteins illuminate the evolution of eustigmatophyte algae and their bacterial endosymbionts. Genom Biol Evol 11:362–379

    Article  CAS  Google Scholar 

  • Sharma AK, Nymark M, Sparstad T, Bones AM, Winge P (2018) Transgene-free genome editing in marine algae by bacterial conjugation - comparison with biolistic CRISPR/Cas9 transformation. Sci Rep 8:14401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sorhannus U (2011) Evolution of antifreeze protein genes in the diatom genus fragilariopsis: evidence for horizontal gene transfer, gene duplication and episodic diversifying selection. Evol Bioinformatics Online 7:279–289

    Google Scholar 

  • Stiller JW, Huang JL, Ding Q, Tian J, Goodwillie C (2009) Are algal genes in nonphotosynthetic protists evidence of historical plastid endosymbioses? BMC Genomics 10:484

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stiller JW et al (2014) The evolution of photosynthesis in chromist algae through serial endosymbioses. Nat Commun 5:5764

    Article  CAS  PubMed  Google Scholar 

  • Stoebe B, Martin W, Kowallik K (1998) Distribution and nomenclature of protein-coding genes in 12 sequenced chloroplast genomes. Plant Mol Biol Rep 16:13

    Article  Google Scholar 

  • Sturm S et al (2013) A novel type of light-harvesting antenna protein of red algal origin in algae with secondary plastids. BMC Evol Biol 13:159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swenson NG (2009) Phylogenetic resolution and quantifying the phylogenetic diversity and dispersion of communities. PLoS One 4:e4390

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tabita FR, Satagopan S, Hanson TE, Kreel NE, Scott SS (2008) Distinct form I, II, III, and IV rubisco proteins from the three kingdoms of life provide clues about rubisco evolution and structure/function relationships. J Exp Bot 59:1515–1524

    Article  CAS  PubMed  Google Scholar 

  • Tajima N et al (2016) Sequencing and analysis of the complete organellar genomes of Parmales, a closely related group to Bacillariophyta (diatoms). Curr Genet 62:887–896

    Article  CAS  PubMed  Google Scholar 

  • Tsui CKM et al (2009) Labyrinthulomycetes phylogeny and its implications for the evolutionary loss of chloroplasts and gain of ectoplasmic gliding. Mol Phylogenet Evol 50:129–140

    Article  CAS  PubMed  Google Scholar 

  • Vancaester E, Depuydt T, Osuna-Cruz CM, Vandepoele K (2020) Comprehensive and functional analysis of horizontal gene transfer events in diatoms. Mol Biol Evol 37:3243–3257

    Article  CAS  PubMed  Google Scholar 

  • Villanova V et al (2017) Investigating mixotrophic metabolism in the model diatom Phaeodactylum tricornutum. Philos Trans R Soc B 372:20160404

    Article  CAS  Google Scholar 

  • Walker G, Dorrell RG, Schlacht A, Dacks JB (2011) Eukaryotic systematics: a user's guide for cell biologists and parasitologists. Parasitology 138:1638–1663

    Article  PubMed  Google Scholar 

  • Wang Q, Sun H, Huang J (2017) Re-analyses of “algal” genes suggest a complex evolutionary history of oomycetes. Front Plant Sci 8:1540

    Article  PubMed  PubMed Central  Google Scholar 

  • Wetherbee R et al (2019) The golden paradox - a new heterokont lineage with chloroplasts surrounded by two membranes. J Phycol 55:257–278

    Article  CAS  PubMed  Google Scholar 

  • Yamada N, Sakai H, Onuma R, Kroth PG, Horiguchi T (2020) Five non-motile dinotom dinoflagellates of the genus Dinothrix. Front Plant Sci 11:591050

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamada N, Sym SD, Horiguchi T (2017) Identification of highly divergent diatom-derived chloroplasts in dinoflagellates, including a description of Durinskia kwazulunatalensis sp. nov. (Peridiniales, Dinophyceae). Mol Biol Evol 34:1335–1351

    Article  CAS  PubMed  Google Scholar 

  • Yamada N et al (2019) Discovery of a kleptoplastic 'dinotom' dinoflagellate and the unique nuclear dynamics of converting kleptoplastids to permanent plastids. Sci Rep 9:10474

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang M, Lin X, Liu X, Zhang J, Ge F (2018) Genome annotation of a model diatom Phaeodactylum tricornutum using an integrated proteogenomic pipeline. Mol Plant 11:1292–1307

    Article  CAS  PubMed  Google Scholar 

  • Yu M et al (2018) Evolution of the plastid genomes in diatoms. In: Chaw S, Jansen R (eds) Adv. Bot. Res. Plastid genome evolution, vol 85. Elsevier, pp 129–155

    Chapter  Google Scholar 

Download references

Acknowledgements

RGD acknowledges a CNRS Momentum Fellowship (awarded 2019-2021) and an ANR JCJC (“PanArctica”, grant number ANR-21-CE02-0014-01, awarded 2022-2025).

Author information

Authors and Affiliations

  1. Institut de Biologie de l’ENS (IBENS), Département de Biologie, École Normale Supérieure, CNRS, INSERM, Université PSL, Paris, France

    Richard G. Dorrell, Fuhai Liu & Chris Bowler

  2. Centre de Recherches Interdisciplinaires, Université de Paris, INSERM U1284, Paris, France

    Fuhai Liu

  3. Tsinghua-UC Berkeley Shenzhen Institute (TBSI), Tsinghua University, University of California, Berkeley, Berkeley, CA, USA

    Fuhai Liu

Authors
  1. Richard G. Dorrell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fuhai Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chris Bowler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Richard G. Dorrell .

Editor information

Editors and Affiliations

  1. Laboratoire de Biologie du chloroplaste et perception de la lumière chez les microalgues, UMR7141, Centre national de la recherche scientifique, Sorbonne Université Institut de Biologie Physico-Chimique, Paris, France

    Angela Falciatore

  2. School of Environmental Sciences, University of East Anglia Norwich Research Park, Norwich, UK

    Thomas Mock

Rights and permissions

Reprints and permissions

Copyright information

© 2022 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Dorrell, R.G., Liu, F., Bowler, C. (2022). Reconstructing Dynamic Evolutionary Events in Diatom Nuclear and Organelle Genomes. In: Falciatore, A., Mock, T. (eds) The Molecular Life of Diatoms. Springer, Cham. https://doi.org/10.1007/978-3-030-92499-7_6

Download citation

Publish with us

Policies and ethics

Search

Navigation