The evolution of algal chloroplasts
01 Jan 1992-pp 107-121
TL;DR: The present understanding of how chloroplasts evolved in the different groups of algae is summed up in this symposium presentation.
Abstract: The algae are not a natural assemblage of organisms Rather they are a diverse group of protists and fungi which have acquired chloroplasts in various ways, in some groups directly from symbiotic photosynthetic prokaryotes and in others from symbiotic eukaryotic algae The new techniques for rapidly sequencing ribosomal RNA, discussed by Adoutte in this volume, are producing evolutionary trees which are giving us a clearer understanding of the true relationships between different eukaryotes In Fig 1, I have drawn an evolutionary tree based on the sequences of the small subunit ribosomal RNA of a number of eukaryotes The most ancient eukaryotes whose ribosomal RNA has been sequenced to date are Giardia lamblia, a parasitic diplomonad, and Vairimorpha necatrix, a microsporidian Neither of these protists has mitochondria, and it is possible that these ancient eukaryotes evolved prior to the acquisition of mitochondria Also ancient are the trypanosomes and Euglena Somewhat later Dictyostelium evolved, but then came an explosive radiation of many protist groups, fungi, plants and animals In this tree, I have put in boldface lettering those groups which contain species with chloroplasts A glance at the tree shows that the algae are polyphyletic Euglenoids evolved very early and are related to trypanosomes The dinoflagellates, which many have assumed to be an ancient group because of the presence of a mesokaryotic nucleus (Loeblich, 1976), in fact evolved late and are related to ciliates The brown algae and Chrysophytes are related to each other and to the Oomycetes, a relationship long suspected due to the presence of heterokont flagella in each group Higher plants and green algae form a natural assemblage The fact that organisms with chloroplasts appear on different branches of the tree indicates that different groups have acquired chloroplasts independently of each other In this symposium presentation, I will summarize our present understanding of how chloroplasts evolved in the different groups of algae
Citations
More filters
TL;DR: The demarcation of protist kingdoms is reviewed, a complete revised classification down to the level of subclass is provided for the kingdoms Protozoa, ArchezoA, and Chromista, and the phylogenetic basis of the revised classification is outlined.
878 citations
TL;DR: The eukaryotic crown group Alveolata has a particularly complex history of plastid acquisition, and may or may not be descended from a single endosymbiotic event.
Abstract: Plastids (chloroplasts) are endosymbiotic organelles derived from previously free-living cyanobacteria. They are dependent on their host cell to the degree that the majority of the proteins expressed in the plastid are encoded in the nuclear genome of the host cell, and it is this genetic dependency that distinguishes organelles from obligate endosymbionts. Reduction in the size of the plastid genome has occurred via gene loss, substitution of nuclear genes, and gene transfer. The plastids of Chlorophyta and plants, Rhodophyta, and Glaucocystophyta are primary plastids (i.e., derived directly from a cyanobacterium). These three lineages may or may not be descended from a single endosymbiotic event. All other lineages of plastids have acquired their plastids by secondary (or tertiary) endosymbiosis, in which a eukaryote already equipped with plastids is preyed upon by a second eukaryote. Considerable gene transfer has occurred among genomes and, at times, between organisms. The eukaryotic crown group Alveolata has a particularly complex history of plastid acquisition.
374 citations
TL;DR: Algal diversity is examined and endosymbiosis is shown to be a major force in algal evolution, with long-standing issues such as the chromalveolate hypothesis and the extent of endOSymbiotic gene transfer clarified.
Abstract: The photosynthetic organelle of algae and plants (the plastid) traces its origin to a primary endosymbiotic event in which a previously non-photosynthetic protist engulfed and enslaved a cyanobacterium. This eukaryote then gave rise to the red, green and glaucophyte algae. However, many algal lineages, such as the chlorophyll c-containing chromists, have a more complicated evolutionary history involving a secondary endosymbiotic event, in which a protist engulfed an existing eukaryotic alga (in this case, a red alga). Chromists such as diatoms and kelps then rose to great importance in aquatic habitats. Another algal group, the dinoflagellates, has undergone tertiary (engulfment of a secondary plastid) and even quaternary endosymbioses. In this review, we examine algal diversity and show endosymbiosis to be a major force in algal evolution. This area of research has advanced rapidly and long-standing issues such as the chromalveolate hypothesis and the extent of endosymbiotic gene transfer have recently been clarified.
330 citations
TL;DR: In this paper, the authors identify the earliest morphological evidence for heterotrophic eukaryotic organisms by mid-Neoproterozoic times and, more significantly, provide the earliest morphology evidence for the testate amoebae in marine ecosystems.
Abstract: Vase-shaped microfossils (VSMs) occur globally in Neoproterozoic rocks, but until now their biological relationships have remained problematic. Exceptionally preserved new populations from the uppermost Chuar Group, Grand Canyon, Arizona, display details of morphology and taphonomy that collectively point to affinities with the testate amoebae. The fossils are tear-shaped tests, ∼20–300 μm long and ∼10–200 μm wide, that are circular in transverse section, expand aborally toward a rounded or slightly pointed pole, and taper orally toward a “neck” that ends in a single aperture. Apertures may be circular, hexagonal, triangular, or crenulate, and may be rimmed by a distinct collar. Approximately 25% of the Chuar VSMs are curved, such that the oral and aboral poles do not lie opposite each other. Tests are preserved as mineralized casts and molds, commonly coated with organic debris or iron minerals, but they were originally composed of nonresistant organic matter. Approximately 1% have a “honeycomb-patterned” wall attributable to the original presence of mineralized scales whose bases were arranged regularly in the test wall. Scale-bearing testate amoebae, such as members of the Euglyphidae, are essentially identical to the honeycomb VSMs, and a close relationship between other Grand Canyon VSMs and additional testate amoebae, both lobose and filose, is likely. The VSM population therefore most likely represents a multispecies assemblage whose spatial association reflects a common habitat and/or taphonomic circumstances that favor test preservation. The assignment of these fossils to the testate amoebae strengthens the case for a major diversification of eukaryotic organisms by mid-Neoproterozoic times and, more significantly, provides the earliest morphological evidence for heterotrophic eukaryotes in marine ecosystems.
316 citations
Cites background from "The evolution of algal chloroplasts..."
...Moreover, all algal protists acquired their chloroplasts via endosymbiosis (Gibbs 1992), so even the eukaryotic capacity for photosynthesis depends on the preexisting ability to swallow particles....
[...]
TL;DR: A previously unrecognized branch of Rubisco's evolution is confirmed: a eukaryotic form II enzyme that participates in oxygenic photosynthesis and is encoded by a diverse, nuclear multigene family.
Abstract: Genes encoding ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) were cloned from dinoflagellate symbionts (Symbiodinium spp) of the giant clam Tridacna gigas and characterized. Strikingly, Symbiodinium Rubisco is completely different from other eukaryotic (form I) Rubiscos: it is a form II enzyme that is approximately 65% identical to Rubisco from Rhodospirillum rubrum (Rubisco forms I and II are approximately 25 to 30% identical); it is nuclear encoded by a multigene family; and the predominantly expressed Rubisco is encoded as a precursor polyprotein. One clone appears to contain a predominantly expressed Rubisco locus (rbcA), as determined by RNA gel blot analysis of Symbiodinium RNA and sequencing of purified Rubisco protein. Another contains an enigmatic locus (rbcG) that exhibits an unprecedented pattern of amino acid replacement but does not appear to be a pseudogene. The expression of rbcG has not been analyzed; it was detected only in the minor of two taxa of Symbiodinium that occur together in T. gigas. This study confirms and describes a previously unrecognized branch of Rubisco's evolution: a eukaryotic form II enzyme that participates in oxygenic photosynthesis and is encoded by a diverse, nuclear multigene family.
209 citations
Cites background from "The evolution of algal chloroplasts..."
...There are no sequence data from chloroplasts of peridinincontaining dinoflagellates, and any discussion of their origin is speculative (Gibbs, 1990; Cavalier-Smith, 1992; Whatley, 1993)....
[...]
...Because this arrangement also exists in most dinoflagellates (Gibbs, 1990), including Symbiodinium (Blank, 1987), a long transit peptide is not unanticipated....
[...]
...…given; apparent deletions were scored as nonidentities for the number of positions missing. flagellates represent a reduced eukaryotic endosymbiont (Gibbs, 1990; Whatley, 1993), this might have occurred elsewhere , followed by the further translocation from endosymbiont nucleus to host…...
[...]
References
More filters
TL;DR: Investigation of the small subunit ribosomal RNA (16S-like rRNA) from the protozoan Giardia lamblia provided a new perspective on the evolution of nucleated cells and challenged the phylogenetic significance of multiple eukaryotic kingdoms.
Abstract: An analysis of the small subunit ribosomal RNA (16S-like rRNA) from the protozoan Giardia lamblia provided a new perspective on the evolution of nucleated cells. Evolutionary distances estimated from sequence comparisons between the 16S-like rRNAs of Giardia lamblia and other eukaryotes exceed similar estimates of evolutionary diversity between archaebacteria and eubacteria and challenge the phylogenetic significance of multiple eukaryotic kingdoms. The Giardia lamblia 16S-like rRNA has retained many of the features that may have been present in the common ancestor of eukaryotes and prokaryotes.
702 citations
TL;DR: The small-subunit rRNA gene sequences of the flagellated protists Euglena gracilis and Trypanosoma brucei were determined and compared and the genetic diversity in this collection of eukaryotes is seen to exceed that displayed within either the eubacterial or the archaebacterial lines of descent.
Abstract: The small-subunit rRNA gene sequences of the flagellated protists Euglena gracilis and Trypanosoma brucei were determined and compared to those of other eukaryotes. A phylogenetic tree was constructed in which the earliest branching among the eukaryotes is represented by E. gracilis. The E. gracilis divergence far antedates a period of massive evolutionary radiation that gave rise to the plants, animals, fungi, and certain groups of protists such as ciliates and the acanthamoebae. The genetic diversity in this collection of eukaryotes is seen to exceed that displayed within either the eubacterial or the archaebacterial lines of descent.
432 citations
432 citations
TL;DR: Comparisons of similarity values or inspection of phylogenetic trees constructed by distance matrix methods reveal a very close relationship between oomycetes and chrysophytes.
Abstract: The phylogenetic relationships among the chlorophyte Chlamydomonas reinhardtii, the chrysophyte Ochromonas danica, and the oomycete Achyla bisexualis were explored by comparing the sequences of their small-subunit ribosomal RNA coding regions. Comparisons of similarity values or inspection of phylogenetic trees constructed by distance matrix methods reveal a very close relationship between oomycetes and chrysophytes. The separation of chrysophytes from chlorophytes is comparable to that of plants from animals, and both separations are far antedated by the divergence of a number of other protist groups.
361 citations