Skip to main content

A genomic and phylogenetic perspective on endosymbiosis and algal origin

  • Conference paper
Eighteenth International Seaweed Symposium

Part of the book series: Developments in Applied Phycology ((DAPH,volume 1))

  • 2525 Accesses

Abstract

Accounting for the diversity of photosynthetic eukaryotes is an important challenge in microbial biology. It has now become clear that endosymbiosis explains the origin of the photosynthetic organelle (plastid) in different algal groups. The first plastid originated from a primary endosymbiosis, whereby a previously non-photosynthetic protist engulfed and enslaved a cyanobacterium. This alga then gave rise to the red, green, and glaucophyte lineages. Algae such as the chlorophyll c-containing chromists gained their plastid through secondary endosymbiosis, in which an existing eukaryotic alga (in this case, a rhodophyte) was engulfed. Another chlorophyll c-containing algal group, the dinoflagellates, is a member of the alveolates that is postulated to be sister to chromists. The plastid in these algae has followed a radically different path of evolution. The peridinin-containing dinoflagellates underwent an unprecedented level of plastid genome reduction with the ca. 16 remaining genes encoded on 1–3 gene minicircles. In this short review, we examine algal plastid diversity using phylogenetic and genomic methods and show endosymbiosis to be a major force in algal evolution. In particular, we focus on the evolution of targeting signals that facilitate the import of nuclear-encoded photosynthetic proteins into the plastid.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
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

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Abrahamsen MS, Templeton TJ, Enomoto S, Abrahante JE, Zhu G, Lancto CA, Deng M, Liu C, Widmer G, Tzipori S, Buck GA, Xu P, Bankier AT, Dear PH, Konfortov BA, Spriggs HF, Iyer L, Anantharaman V, Aravind L, Kapur V (2004) Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304: 441–445.

    Article  PubMed  CAS  Google Scholar 

  • Apt KE, Zaslavkaia L, Lippmeier JC, Lang M, Kilian O, Wetherbee R, Grossman AR, Kroth PG (2002) In vivo characterization of diatom multipartite plastid targeting signals. J. Cell Sci. 115:4061–4069.

    Article  PubMed  CAS  Google Scholar 

  • Archibald JM, Keeling PJ (2002) Recycled plastids: A ‘green movement’ in eukaryotic evolution. Trends in Genet. 18: 577–584.

    Article  CAS  Google Scholar 

  • Archibald JM, Rogers MB, Toop M, Ishida K, Keeling PJ (2003) Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. PNAS 100: 7678–7683.

    Article  PubMed  CAS  Google Scholar 

  • Bachvaroff TR, Concepcion GT, Rogers CR, Herman EM, Delwiche CF (2004) Dinoflagellate expressed sequence tag data indicate massive transfer of chloroplast genes to the nuclear genome. Protist 155: 65–78.

    Article  PubMed  CAS  Google Scholar 

  • Baldauf SL (2003) The deep roots of eukaryotes. Science 300: 1703–1706.

    Article  PubMed  CAS  Google Scholar 

  • Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF (2000) A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290: 972–977.

    Article  PubMed  CAS  Google Scholar 

  • Bhattacharya D, Medlin L (1995) The phylogeny of plastids: A review based on comparisons of small-subunit ribosomal RNA coding regions. J. Phycol. 31: 489–498.

    Article  CAS  Google Scholar 

  • Bhattacharya D, Yoon HS, Hackett JD (2004) Photosynthetic eukaryotes unite: Endosymbiosis connects the dots. BioEssays 26:50–60.

    Article  PubMed  Google Scholar 

  • Cavalier-Smith T (1986) The kingdon chromista: Origin and systematics. In: Round FE, Chapman DJ (eds.) Progress in Phycological Research No. 4, Biopress, Bristol, pp 309–347.

    Google Scholar 

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

    Article  PubMed  CAS  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. Eukaryot. Microbiol. 46: 347–366.

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (2000) Membrane heredity and early chloroplast evolution. Trends in Plant Sci. 5: 174–182.

    Article  CAS  Google Scholar 

  • Chesnick JM, Kooistra WH, Wellbrock U, Medlin LK (1997) Ribosomal RNA analysis indicates a benthic pennate diatom ancestry for the endosymbionts of the dinoflagellates Peridinium foliaceum and Peridinium balticum (Pyrrhophyta). J. Eukaryot. Microbiol. 44: 314–320.

    Article  PubMed  CAS  Google Scholar 

  • Ciniglia C, Yoon HS, Pollio A, Pinto G, Bhattacharya D (2004) Hidden biodiodiversity of the extremophilic Cyanidiales red algae. Mol. Ecol. 13: 1827–1838.

    Article  PubMed  CAS  Google Scholar 

  • Delwiche CF, Kuhsel M, Palmer J.D (1995) Phylogenetic analysis of tufA sequences indicates a cyanobacterial origin of all plastids. Mol. Phylogenet. Evol. 4: 110–128.

    Article  PubMed  CAS  Google Scholar 

  • Douglas SE (1998) Plastid evolution: Origins, diversity, trends. Curr. Opin. Genet. Dev. 8: 655–661.

    Article  PubMed  CAS  Google Scholar 

  • Douglas SE, Murphy CA, Spencer DF, Gray MW (1991) Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature 350: 148–151.

    Article  PubMed  CAS  Google Scholar 

  • Eckart K, Eichacker L, Sohrt K, Schleiff E, Heins L, Soll J (2002) A toc75-like protein import channel is abundant in chloroplasts. EMBO Reports 3: 557–562.

    Article  PubMed  CAS  Google Scholar 

  • Fast NM, Kissinger JC, Roos DS, Keeling PJ (2001) Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol. Biol. Evol. 18: 418–426.

    PubMed  CAS  Google Scholar 

  • Funes S, Davidson E, Reyes-Prieto A, Magallon S, Herion P, King MP, Gonzalez-Halphen D (2002) A green algal apicoplast ancestor. Science 298: 2155.

    Article  PubMed  CAS  Google Scholar 

  • Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan MS, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DM, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498–511.

    Article  PubMed  CAS  Google Scholar 

  • Gibbs SP (1978) The chloroplasts of Euglena may have evolved from symbiotic green algae. Can. J. Bot. 56: 2883–2889.

    Google Scholar 

  • Gibbs SP (1981) The chloroplasts of some algal groups may have evolved from endosymbiotic eukaryotic algae. Annal. NY Acad. Sci. 361: 193–208.

    Article  CAS  Google Scholar 

  • Gray MW (1992) The endosymbiont hypothesis revisited. Int. Rev. Cytol. 141: 233–357.

    Article  PubMed  CAS  Google Scholar 

  • Hackett JD, Maranda L, Yoon HS, Bhattacharya D (2003) Phylogenetic evidence for the cryptophyte origin of the plastid of Dinophysis (dinophysiales, dinophyceae). J. Phycol. 39: 440–448.

    CAS  Google Scholar 

  • Hackett JD, Yoon HS, Butterfield NJ, Sanderson MJ, Bhattacharya D (2006) Plastid endosymbiosis: Origins and timing of events. In: Falkowski P, Knoll A (eds.) Evolution of Aquatic Photoautotrophs, Academic Press, in press.

    Google Scholar 

  • Hackett JD, Yoon HS, Soares MB, Bonaldo MF, Casavant TL, Scheetz TE, Nosenko T, Bhattacharya D (2004) Migration of the plastid genome to the nucleus in a peridinin dinoflagellate. Curr. Biol. 14: 213–218.

    PubMed  CAS  Google Scholar 

  • Harper JT, Keeling PJ (2003) Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids. Mol. Biol. Evol. 20:1730–1735.

    Article  PubMed  CAS  Google Scholar 

  • Hedges SB, Blair JE, Venturi ML, Shoe JL (2004) A molecular timescale of eukaryote evolution and the rise of complex multicellular life. BMC Evol. Biol. 4: 2.

    Article  PubMed  Google Scholar 

  • Heins L, Soll J, Collinson I (1998) The protein translocation apparatus of chloroplast envelopes. Trends in Plant Sci. 3: 56–61.

    Article  Google Scholar 

  • Ishida K, Green BR (2002) Second-and third-hand chloroplasts in dinoflagellates: Phylogeny of oxygen-evolving enhancer 1 (psbO) protein reveals replacement of a nuclear-encoded plastid gene by that of a haptophyte tertiary endosymbiont. PNAS 99: 9294–9299.

    Article  PubMed  CAS  Google Scholar 

  • Kilian O, Kroth PG (2003) Evolution of protein targeting into “complex” plastids: The “secretory transport hypothesis”. Plant Biol. 5: 350–358.

    Article  CAS  Google Scholar 

  • Lopez-Garcia P, Rodriguez-Valera F, Pedros-Alio C, Moreira D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409: 603–607.

    Article  PubMed  CAS  Google Scholar 

  • Margulis L (1970) Origin of eukaryotic cells. Yale University Press, New Haven, CT.

    Google Scholar 

  • Martin W, Herrmann RG (1998) Gene transfer from organelles to the nucleus: How much, what happens, and why? Plant Physiol. 118: 9–17.

    Article  PubMed  CAS  Google Scholar 

  • Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D (2002) Evolutionary analysis of Aarabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. PNAS 99: 12246–12251.

    Article  PubMed  CAS  Google Scholar 

  • Matsuzaki M, Misumi O, Shin-i T, Maruyama S, Takahara M, Miyagishima S, Mori T, Nishida K, Yagisawa F, Nishida K, Yoshida Y, Nishimura Y, Nakao S, Kobayashi T, Momoyama Y, Higashiyama T, Minoda A, Sano M, Nomoto H, Oishi K, Hayashi H, Ohta F, Nishizaka S, Haga S, Miura S, Morishita T, Kabeya Y, Terasawa K, Suzuki Y, Ishii Y, Asakawa S, Takano H, Ohta N, Kuroiwa H, Tanaka K, Shimizu N, Sugano S, Sato N, Nozaki H, Ogasawara N, Kohara Y, Kuroiwa T (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428: 653–657.

    Article  PubMed  CAS  Google Scholar 

  • McFadden GI (1999). Plastids and protein targeting. J. Eukaryot. Microbiol. 46: 339–346.

    Article  PubMed  CAS  Google Scholar 

  • McFadden GI (2001) Primary and secondary endosymbiosis and the origin of plastids. J. Phycol. 37: 951–959.

    Article  Google Scholar 

  • McFadden GI, van Dooren GG (2004) Evolution: Red algal genome affirms a common origin of all plastids. Curr. Biol. 14: R514–R516.

    Article  PubMed  CAS  Google Scholar 

  • McFadden GI, Gilson PR, Hofmann CJ, Adcock GJ, Maier UG (1994) Evidence that an amoeba acquired a chloroplast by retaining part of an engulfed eukaryotic alga. PNAS 91: 3690–3694.

    Article  PubMed  CAS  Google Scholar 

  • Mereschkowsky C (1905) Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol. Centralbl. 25: 593–604.

    Google Scholar 

  • Moon-van der Staay SY, Wachter RDe, Vaulot D (2001) Oceanic 18s rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409: 607–610.

    Article  PubMed  CAS  Google Scholar 

  • Moreira D, Le Guyader H, Phillippe H (2000) The origin of red algae and the evolution of chloroplasts. Nature 405: 69–72.

    Article  PubMed  CAS  Google Scholar 

  • Nassoury N, Cappadocia M, Morse D (2003) Plastid ultrastructure defines the protein import pathway in dinoflagellates. J. Cell Sci. 116: 2867–2874.

    Article  PubMed  CAS  Google Scholar 

  • Palmer JD (2003) The symbiotic birth and spread of plastids: How many times and whodunit. J. Phycol. 39: 4–12.

    Article  CAS  Google Scholar 

  • Rodriguez-Ezpeleta N, Brinkmann H, Burey SC, Roure B, Burger G, Loffelhardt W, Bohert HJ, Philippe H, Lang BF (2005) Mono-phyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr. Biol. 15: 1325–1330.

    Article  PubMed  CAS  Google Scholar 

  • Sulli C, Fang Z, Muchhal U, Schwartzbach SD (1999) Topology of Euglena chloroplast protein precursors within endoplasmic reticulum to Golgi to chloroplast transport vesicles. J. Biol. Chem. 274: 457–463.

    Article  PubMed  CAS  Google Scholar 

  • Tengs T, Dahlberg OJ, Shalchian-Tabrizi K, Klaveness D, Rudi K, Delwiche CF, Jakobsen KS (2000) Phylogenetic analyses indicate that the 19′hexanoyloxy-fucoxanthin-containing dinoflagellates have tertiary plastids of haptophyte origin. Mol. Biol. Evol. 17: 718–729.

    PubMed  CAS  Google Scholar 

  • Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu D, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers Y-H, Smith HO (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304: 66–74.

    Article  PubMed  CAS  Google Scholar 

  • Waller RF, Keeling PJ, Donald RG, Striepen B, Handman E, Lang-Unnasch N, Cowman AF, Besra GS, Roos DS, McFadden GI (1998) Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. PNAS 95: 12352–12357.

    Article  PubMed  CAS  Google Scholar 

  • Waller RF, Keeling PJ, van Dooren GG, McFadden GI (2003) Comment on “a green algal apicoplast ancestor”. Science 301: 49.

    Article  PubMed  Google Scholar 

  • Waller RF, Reed MB, Cowman AF, McFadden GI (2000) Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J. 19: 1794–1802.

    Article  PubMed  CAS  Google Scholar 

  • Watanabe MM, Suda S, Inouye I, Sawaguchi T, Chihara M (1990) Lepidodinium viride gen. et sp. nov. (Gymnodiniales, Dinophyta), a green dinoflagellate with chlorophyll a-and bcontaining endosymbiont. J. Phycol. 26: 741–751.

    Article  Google Scholar 

  • Williamson DH, Gardner MJ, Preiser P, Moore DJ, Rangachari K, Wilson RJ (1994) The evolutionary origin of the 35 kb circular DNA of Plasmodium falciparum: New evidence supports a possible rhodophyte ancestry. Mol. Gen. Genet. 243: 249–252.

    PubMed  CAS  Google Scholar 

  • Yoon HS, Hackett JD, Bhattacharya D (2002a) A single origin of the peridinin-and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. PNAS 99: 11724–11729.

    Article  PubMed  CAS  Google Scholar 

  • Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol. Biol. Evol. 21: 809–818.

    Article  PubMed  CAS  Google Scholar 

  • Yoon HS, Hackett JD, Pinto G, Bhattacharya D (2002b) The single, ancient origin of chromist plastids. PNAS 99: 15507–15512.

    Article  PubMed  CAS  Google Scholar 

  • Yoon HS, Hackett JD, Van Dolah FM, Nosenko T, Lidie KL, Bhattacharya D (2005) Tertiary endosymbiosis driven genome evolution in dinoflagellate algae. Mol. Biol. Evol. 22: 1299–1308.

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Green BR, Cavalier-Smith T (1999) Single gene circles in dinoflagellate chloroplast genomes. Nature 400: 155–159.

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Green BR, Cavalier-Smith T (2000) Phylogeny of ultra-rapidly evolving dinoflagellate chloroplast genes: A possible common origin for sporozoan and dinoflagellate plastids. J. Mol. Evol. 51: 26–40.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Springer

About this paper

Cite this paper

Yoon, H.S., Hackett, J.D., Bhattacharya, D. (2006). A genomic and phylogenetic perspective on endosymbiosis and algal origin. In: Anderson, R., Brodie, J., Onsøyen, E., Critchley, A.T. (eds) Eighteenth International Seaweed Symposium. Developments in Applied Phycology, vol 1. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-5670-3_31

Download citation

Publish with us

Policies and ethics