Second-hand Chloroplasts: Evolution of Cryptomonad Algae

https://doi.org/10.1016/S0065-2296(08)60205-0Get rights and content

Publisher Summary

This chapter presents an overview of endosymbiosis, particularly the evolution of cryptomonad and the endosymbiosis between cryptomonad and red algae. The cryptomonad engulfs red algae and acquires photosynthetic capacity along with morphological and biochemical evidence. The endosymbiosis between cryptomonad and red algae developed from a predator-prey relationship is described. The studies to validate that cryptomonads and red algae are endosymbiont have been examined. The chapter discusses the close relationship between the nuclear and nucleomorph sequences of red algae and cryptomonad respectively. The conversion of phagotrophic protists to an autotrophic life-style by engulfing and retaining photosynthetic eukaryotes during evolution is also presented. The structures of cryptomonad and nucleomorph are described. Cryptomonads have small organelle called nucleomorph which is the vestigial nucleus of the eukaryotic endosymbiont. Nucleus–like status of nucleomorph is confirmed by the presence of DNA in it. Studies also indicate transcriptionally active ribosomal RNAs present in the nucleomorph. Techniques to isolate the nucleomorph are explained. Details regarding the structure of cryptomonad chloroplast, the periplastidal space for storage and the photosynthetic pigments—phycoerythrin or phycocyanin are explained. The genome reveals circular chromosome with inverted repeats of gene sequences. Nucleomorph DNA encodes ribosomal proteins and housekeeping genes as well as proteins essential to the chloroplast. The pivotal role of nucleomorph in the endosymbiotic relationship is clearly explained.

References (182)

  • E.V. Ariztia et al.

    A new phylogeny for chromophyte algae using 16S-like rRNA sequences from Mallomonas papillosa (Synurophyceae) and Tribonema aequale (Xanthophyceae).

    Journal of Phycology

    (1991)
  • D. Bhattacharya et al.

    Phylogenetic comparisons of the small subunit ribosomal DNA sequence of Costaria costata (Phaeophyta) with those of other algae, vascular plants, and Öomycetes.

    Journal of Phycology

    (1988)
  • D. Bhattacharya et al.

    Molecular phylogenetic analysis of actin geneic regions from Achlya bisexualis (Oomycota) and Costaria costata (Chromophyta).

    Journal of Molecular Evolution

    (1991)
  • G.W. Beakes

    Oomycete fungi: their phylogeny and relationship to chromophyte algae

  • M. Bendayan

    Ultrastructural localization of nucleic acids by use of enzymegold complexes.

    Journal of Histochemistry and Cytochemistry

    (1981)
  • Boczar, B. A., Delaney, T. P. and Cattolico, R. A. (1989). Gene for the ribulose-1,5-bisphosphate carboxylase small...
  • L. Bogorad

    Evolution of organelles and eukaryotic genomes. Separation of genes for chloroplast ribosomes in two genomes suggest principles of organelle biology.

    Science

    (1975)
  • L. Bogorad

    Regulation of intracellular gene flow in the evolution of eukaryotic genomes.

  • R.A. Cattolico et al.

    Analysis of chloroplast evolution and phylogeny: a molecular approach

  • T. Cavalier-Smith

    The origin of plastids.

    Biological Journal of the Linnean Society

    (1982)
  • T. Cavalier-Smith

    The kingdom Chromista: origin and systematics.

  • T. Cavalier-Smith

    The simultaneous symbiotic origin of mitochondria, chloroplasts, and microbodies.

    Annals of the New York Academy of Sciences

    (1987)
  • T. Cavalier-Smith

    The kingdom Chromista

  • T. Cavalier-Smith et al.

    Protozoa as hosts for endosymbioses and the conversion of symbionts into organelles.

    Journal of Protozoology

    (1985)
  • D.D. Chang et al.

    A mammalian mitochondrial RNA processing activity contains nucleus-encoded RNA.

    Science

    (1987)
  • J. Coombs et al.

    Compartmentation of the photosynthetic apparatus

  • J.S. Craigie

    Storage products.

  • T.P. Delaney et al.

    Chloroplast ribosomal DNA organization in the chromophytic alga Olisthodiscus luteus

    Current Genetics

    (1989)
  • J.D. Dodge

    The ultrastructure of Chroomonas mesostigmatica Butcher (Cryptophyceae).

    Archiv für Mikrobiologie

    (1969)
  • S.E. Douglas

    Physical mapping of the plastid genome from the chlorophyll c-containing alga Cryptomonas Φ.

    Current Genetics

    (1988)
  • S.E. Douglas

    Unusual organization of a ribosomal protein operon in the plastid genome of Cryptomonas Φ: evolutionary considerations.

    Current Genetics

    (1991)
  • S.E. Douglas et al.

    The small subunit of ribulose-1,5-bisphosphate carboxylase is plastid-encoded in the chlorophyll c-containing alga Cryptomonas Φ

    Plant Molecular Biology

    (1989)
  • S.E. Douglas et al.

    Sequence analysis of the plastid rDNA spacer region of the chlorophyll c-containing alga Cryptomonas Φ

    DNA Sequence-Journal of DNA Sequencing and Mapping

    (1990)
  • S.E. Douglas et al.

    Nucleotide sequence of the genes for ribosomal protein S4 and tRNAArg from the chlorophyll c-containing alga Cryptomonas Φ.

    Nucleic Acids Research

    (1990)
  • S.E. Douglas et al.

    Molecular evidence for the origin of plastids from a cyanobacterium-like ancestor.

    Journal of Molecular Evolution

    (1991)
  • S.E. Douglas et al.

    Nucleotide sequence of the gene for the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase from Cryptomonas Φ.: Evidence supporting the polyphyletic origin of plastids.

    Journal of Phycology

    (1991)
  • S.E. Douglas et al.

    Molecular evidence that cryptomonad algae are evolutionary chimeras of two phylogenetically distinct unicellular eukaryotes.

    Nature

    (1991)
  • D. Dwarte et al.

    A freeze-fracture study of cryptomonad thylakoids.

    Protoplasma

    (1982)
  • Egelhoff, T. and Grossman, A. R. (1983). Cytoplasmic and chloroplast synthesis of phycobilisome polypeptides....
  • C.G. Ehrenberg

    Über dei Entwicklung und Lebensdauer der Infusionthiere; nebst fernen Beitragen zu einer Vergleichung ihrer organischen System.

    Abhandlungen der Königlichen Akademie der Wissenschaften in Berlin

    (1832)
  • V. Enea et al.

    The evolution of plasmodial stage-specific rRNA genes is dominated by gene conversion.

    Journal of Molecular Evolution

    (1991)
  • S. Eschbach et al.

    A eukaryotic genome of 660 kb: electrophoretic karyotype of nucleomorph and cell nucleus of the cryptomonad alga.

    Pyrenomonas salina. Nucleic Acids Research

    (1991)
  • S. Eschbach et al.

    Primary and secondary structure of the nuclear small subunit ribosomal RNA of the cryptomonad Pyrenomonas salina as inferred from the gene sequence: evolutionary implications.

    Journal of Molecular Evolution

    (1991)
  • H. Ettl

    Über einen intrazellulären Parasiten bei Cryptomonas (Cryptophyceae), II.

    Plant Systematics and Evolution

    (1984)
  • H. Ettl et al.

    Über einen intrazellulären Parasiten bei Cryptomonas (Cryptophyceae)

    Plant Systematics and Evolution

    (1980)
  • L.V. Evans

    Electron microscopical observation on a new Med unicell, Rhodella maculata gen. nov., sp. nov.

    British Phyological Journal

    (1970)
  • M.A. Farmer et al.

    Organelle loss in the endosymbiont of Gymnodinium acidotum (Dinophyceae).

    Protoplasma

    (1990)
  • S.D. Fields et al.

    Ingestion and retention of Chroomonas spp. (Cryptophyceae) by Gymnodinium acidotum (Dinophyceae).

    Journal of Phycology

    (1991)
  • E. Gantt

    Photosynthetic cryptophytes.

  • E. Gantt et al.

    Chloroplast structure of the Cryptophyceae. Evidence for phycobiliproteins within the intrathylakoidal spaces.

    Journal of Cell Biology

    (1971)
  • Cited by (41)

    • Feeding and grazing impact by the bloom-forming euglenophyte Eutreptiella eupharyngea on marine eubacteria and cyanobacteria

      2018, Harmful Algae
      Citation Excerpt :

      Thus, mixotrophic capabilities of the euglenophyte, cryptophytes, and raphidophytes may be weaker than those of mixotrophic dinoflagellates. Euglenophyte and raphidophytes possibly have acquired photosynthetic capabilities via secondary endosymbiosis, whereas the phototrophic dinoflagellates via tertiary endosymbiosis (Gibbs, 1978, 1981; McFadden, 1993; Delwiche, 1999; Yoon et al., 2005; Milanowski et al., 2006; Petersen et al., 2006; Kořenỷ and Oborník, 2011). Endosymbiosis occurs through feeding (Delwiche, 1999; Archibald, 2009; Keeling, 2010); thus, weaker mixotrophic ability of the euglenophyte, cryptophytes, and raphidophytes compared to mixotrophic dinoflagellates could partially be attributed to them being less evolved.

    • Cryptomonads

      2015, Freshwater Algae of North America: Ecology and Classification
    • Cell cycle and nucleomorph division in pyrenomonas helgolandii (cryptophyta)

      2014, Protist
      Citation Excerpt :

      Moreover, McFadden (1990) reported that eukaryotic ribosomal RNAs are certainly present in the nucleomorph and the periplastidal space. These ultrastructural observations show four characteristics of a eukaryotic nucleus in the nucleomorph; a double membrane envelope with pores, DNA, eukaryotic rRNAs and self-replication (McFadden 1993). In this study, we examined whether a distinct S phase (DNA synthetic phase) occurs in the nucleomorph using immunofluorescence and electron microscopy.

    • Nucleomorph Genomes

      2013, Brenner's Encyclopedia of Genetics: Second Edition
    • Cryptomonads

      2003, Freshwater Algae of North America: Ecology and Classification
    View all citing articles on Scopus
    View full text