An Early-Branching Freshwater Cyanobacterium at the Origin of Plastids

Published on Feb 1, 2017in Current Biology 9.25
· DOI :10.1016/j.cub.2016.11.056
Rafael I. Ponce-Toledo1
Estimated H-index: 1
(University of Paris-Sud),
Philippe Deschamps22
Estimated H-index: 22
(University of Paris-Sud)
+ 3 AuthorsDavid Moreira52
Estimated H-index: 52
(University of Paris-Sud)
Abstract
Summary Photosynthesis evolved in eukaryotes by the endosymbiosis of a cyanobacterium, the future plastid, within a heterotrophic host. This primary endosymbiosis occurred in the ancestor of Archaeplastida, a eukaryotic supergroup that includes glaucophytes, red algae, green algae, and land plants [1–4]. However, although the endosymbiotic origin of plastids from a single cyanobacterial ancestor is firmly established, the nature of that ancestor remains controversial: plastids have been proposed to derive from either early- or late-branching cyanobacterial lineages [5–11]. To solve this issue, we carried out phylogenomic and supernetwork analyses of the most comprehensive dataset analyzed so far including plastid-encoded proteins and nucleus-encoded proteins of plastid origin resulting from endosymbiotic gene transfer (EGT) of primary photosynthetic eukaryotes, as well as wide-ranging genome data from cyanobacteria, including novel lineages. Our analyses strongly support that plastids evolved from deep-branching cyanobacteria and that the present-day closest cultured relative of primary plastids is Gloeomargarita lithophora . This species belongs to a recently discovered cyanobacterial lineage widespread in freshwater microbialites and microbial mats [12, 13]. The ecological distribution of this lineage sheds new light on the environmental conditions where the emergence of photosynthetic eukaryotes occurred, most likely in a terrestrial-freshwater setting. The fact that glaucophytes, the first archaeplastid lineage to diverge, are exclusively found in freshwater ecosystems reinforces this hypothesis. Therefore, not only did plastids emerge early within cyanobacteria, but the first photosynthetic eukaryotes most likely evolved in terrestrial-freshwater settings, not in oceans as commonly thought.
  • References (39)
  • Citations (51)
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References39
Published on May 1, 1998in Nature 41.58
William Martin79
Estimated H-index: 79
(University of Düsseldorf),
Bettina Stoebe6
Estimated H-index: 6
(Braunschweig University of Technology)
+ 3 AuthorsKlaus V. Kowallik16
Estimated H-index: 16
(Braunschweig University of Technology)
Photosynthetic eukaryotes, particularly unicellular forms, possess a fossil record that is either wrought with gaps or difficult to interpret, or both. Attempts to reconstruct their evolution have focused on plastid phylogeny, but were limited by the amount and type of phylogenetic information contained within single genes1, 2, 3, 4, 5. Among the 210 different protein-coding genes contained in the completely sequenced chloroplast genomes from a glaucocystophyte, a rhodophyte, a diatom, a eugleno...
612 Citations Source Cite
Published on Jul 8, 2014in Frontiers in Microbiology 4.02
Marie Ragon6
Estimated H-index: 6
(University of Paris),
Karim Benzerara38
Estimated H-index: 38
(University of Paris)
+ 2 AuthorsPurificación López-García10
Estimated H-index: 10
(Centre national de la recherche scientifique)
Cyanobacteria are mainly thought to induce carbonate precipitation extracellularly via their photosynthetic activity combined with the nucleation potential of exopolymeric substances. The discovery in microbialites of the alkaline lake Alchichica (Mexico) of Candidatus Gloeomargarita lithophora, a cyanobacterium forming large amounts of intracellular Mg-Ca-Sr-Ba carbonate spherules, showed that intracellular biomineralization in cyanobacteria is also possible. A second cyanobacterium isolated fr...
15 Citations Source Cite
Published on Dec 1, 2009in Molecular Biology and Evolution 10.22
Philippe Deschamps22
Estimated H-index: 22
(University of Paris-Sud),
David Moreira52
Estimated H-index: 52
(University of Paris-Sud)
It is widely accepted that the first photosynthetic eukaryotes arose from a single primary endosymbiosis of a cyanobacterium in a phagotrophic eukaryotic host, which led to the emergence of three major lineages: Chloroplastida (green algae and land plants), Rhodophyta, and Glaucophyta. For a long time, Glaucophyta have been thought to represent the earliest branch among them. However, recent massive phylogenomic analyses of nuclear genes have challenged this view, because most of them suggested ...
36 Citations Source Cite
Published on Feb 1, 2014in Nature 41.58
Timothy W. Lyons64
Estimated H-index: 64
,
Christopher T. Reinhard24
Estimated H-index: 24
,
Noah J. Planavsky36
Estimated H-index: 36
The rapid increase of carbon dioxide concentration in Earth’s modern atmosphere is a matter of major concern. But for the atmosphere of roughly two-and-half billion years ago, interest centres on a different gas: free oxygen (O2) spawned by early biological production. The initial increase of O2 in the atmosphere, its delayed build-up in the ocean, its increase to near-modern levels in the sea and air two billion years later, and its cause-and-effect relationship with life are among the most com...
639 Citations Source Cite
Published on Dec 1, 2008in BMC Bioinformatics 2.21
Martin Kostka9
Estimated H-index: 9
(Charles University in Prague),
Magdalena Uzlíková3
Estimated H-index: 3
(Charles University in Prague)
+ 1 AuthorsJaroslav Flegr41
Estimated H-index: 41
(Charles University in Prague)
Background Slow-fast analysis is a simple and effective method to reduce the influence of substitution saturation, one of the causes of phylogenetic noise and long branch attraction (LBA) artifacts. In several steps of increasing stringency, the slow-fast analysis omits the fastest substituting alignment positions from the analysed dataset and thus increases its signal/noise ratio.
29 Citations Source Cite
Published on Jun 1, 2001in Journal of Molecular Evolution 1.96
Liisa B. Koski2
Estimated H-index: 2
(McMaster University),
G. Brian Golding30
Estimated H-index: 30
(McMaster University)
It is well known that basing phylogenetic reconstructions on uncorrected genetic distances can lead to errors in their reconstruction. Nevertheless, it is often common practice to report simply the most similar BLAST (Altschul et al. 1997) hit in genomic reports that discuss many genes (Ruepp et al. 2000; Freiberg et al. 1997). This is because BLAST hits can provide a rapid, efficient, and concise analysis of many genes at once. These hits are often interpreted to imply that the gene is most clo...
385 Citations Source Cite
Published on May 1, 2007in Computing in Science and Engineering 1.07
John D. Hunter2
Estimated H-index: 2
Matplotlib is a 2D graphics package used for Python for application development, interactive scripting,and publication-quality image generation across user interfaces and operating systems
3,670 Citations Source Cite
Published on Feb 14, 2008in Molecular Biology and Evolution 10.22
Oliver Deusch10
Estimated H-index: 10
(University of Düsseldorf),
Giddy Landan20
Estimated H-index: 20
(University of Houston)
+ 5 AuthorsTal Dagan29
Estimated H-index: 29
(University of Düsseldorf)
Plastids are descended from a cyanobacterial symbiosis which occurred over 1.2 billion years ago. During the course of endosymbiosis, most genes were lost from the cyanobacterium's genome and many were relocated to the host nucleus through endosymbiotic gene transfer (EGT). The issue of how many genes were acquired through EGT in different plant lineages is unresolved. Here, we report the genome-wide frequency of gene acquisitions from cyanobacteria in 4 photosynthetic eukaryotes-Arabidopsis, ri...
163 Citations Source Cite
Published on Apr 27, 2012in Science 41.06
Estelle Couradeau7
Estimated H-index: 7
(Pierre-and-Marie-Curie University),
Karim Benzerara38
Estimated H-index: 38
(Pierre-and-Marie-Curie University)
+ 4 AuthorsPurificación López-García37
Estimated H-index: 37
(University of Paris-Sud)
Cyanobacteria have affected major geochemical cycles (carbon, nitrogen, and oxygen) on Earth for billions of years. In particular, they have played a major role in the formation of calcium carbonates (i.e., calcification), which has been considered to be an extracellular process. We identified a cyanobacterium in modern microbialites in Lake Alchichica (Mexico) that forms intracellular amorphous calcium-magnesium-strontium-barium carbonate inclusions about 270 nanometers in average diameter, rev...
103 Citations Source Cite
Published on Dec 1, 2013in Journal of Phycology 3.00
Carrine E. Blank9
Estimated H-index: 9
(University of Montana)
Phylogenetic analyses were performed on concatenated data sets of 31 genes and 11,789 unambiguously alignable characters from 37 cyanobacterial and 35 chloroplast genomes. The plastid lineage emerged somewhat early in the cyanobacterial tree, at a time when Cyanobacteria were likely unicellular and restricted to freshwater ecosystems. Using relaxed molecular clocks and 22 age constraints spanning cyanobacterial and eukaryote nodes, the common ancestor to the photosynthetic eukaryotes was predict...
32 Citations Source Cite
  • References (39)
  • Citations (51)
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Cited By51
Published on Feb 1, 2017in Current Biology 9.25
Jan de Vries11
Estimated H-index: 11
(Dalhousie University),
John M. Archibald36
Estimated H-index: 36
(Canadian Institute for Advanced Research)
Summary Photosynthetic eukaryotes are the product of an endosymbiotic event between a eukaryotic host and a cyanobacterium that became today's plastid. A new phylogenomic study suggests that the closest relative of plastids among extant cyanobacteria is the recently discovered freshwater-dwelling Gloeomargarita lithophora.
8 Citations Source Cite
Published on Feb 1, 2017in Genome Biology and Evolution 3.94
Jan de Vries11
Estimated H-index: 11
(Dalhousie University),
John M. Archibald36
Estimated H-index: 36
(Canadian Institute for Advanced Research),
Sven B. Gould23
Estimated H-index: 23
(University of Düsseldorf)
5 Citations Source Cite
Published on Dec 1, 2017in Journal of Theoretical Biology 1.83
Purificación López-García21
Estimated H-index: 21
(Université Paris-Saclay),
Laura Eme15
Estimated H-index: 15
(Dalhousie University),
David Moreira52
Estimated H-index: 52
(Université Paris-Saclay)
Abstract Fifty years ago, Lynn Margulis, inspiring in early twentieth-century ideas that put forward a symbiotic origin for some eukaryotic organelles, proposed a unified theory for the origin of the eukaryotic cell based on symbiosis as evolutionary mechanism. Margulis was profoundly aware of the importance of symbiosis in the natural microbial world and anticipated the evolutionary significance that integrated cooperative interactions might have as mechanism to increase cellular complexity. To...
22 Citations Source Cite
Published on Jan 15, 2018in Journal of Cell Science 4.40
Jan de Vries11
Estimated H-index: 11
(Dalhousie University),
Sven B. Gould23
Estimated H-index: 23
(University of Düsseldorf)
ABSTRACT Plastids in plants and algae evolved from the endosymbiotic integration of a cyanobacterium by a heterotrophic eukaryote. New plastids can only emerge through fission; thus, the synchronization of bacterial division with the cell cycle of the eukaryotic host was vital to the origin of phototrophic eukaryotes. Most of the sampled algae house a single plastid per cell and basal-branching relatives of polyplastidic lineages are all monoplastidic, as are some non-vascular plants during cert...
10 Citations Source Cite
Published on Aug 1, 2017in Journal of Phycology 3.00
Simon M. Dittami17
Estimated H-index: 17
(Centre national de la recherche scientifique),
Svenja Heesch10
Estimated H-index: 10
(Centre national de la recherche scientifique)
+ 1 AuthorsJonas Collén9
Estimated H-index: 9
(Centre national de la recherche scientifique)
Marine-freshwater and freshwater-marine transitions have been key events in the evolution of life, and most major groups of organisms have independently undergone such events at least once in their history. Here we first compile an inventory of bidirectional freshwater and marine transitions in multicellular photosynthetic eukaryotes. While green and red algae have mastered multiple transitions in both directions, brown algae have colonized fresh water on a maximum of six known occasions, and an...
5 Citations Source Cite
Published on Jun 2, 2017in bioRxiv
A. Del Cortona2
Estimated H-index: 2
(Ghent University),
Frederik Leliaert27
Estimated H-index: 27
(Botanic Garden Meise)
+ 7 AuthorsOlivier De Clerck29
Estimated H-index: 29
(Ghent University)
Chloroplast genomes, relics of an endosymbiotic cyanobacterial genome, are circular double-stranded DNA molecules. They typically range between 100-200 kb and code for circa 80-250 genes. While fragmented mitochondrial genomes evolved several times independently during the evolution of eukaryotes, fragmented plastid genomes are only known in dinoflagellates, where genes are present on several minicircles. Here we show that the chloroplast genome of the green alga Boodlea composita (Cladophorales...
2 Citations Source Cite
Published on Nov 1, 2017in Journal of Plant Research 2.00
Takashi Shiratori7
Estimated H-index: 7
(University of Tsukuba),
Sakuya Fujita (University of Tsukuba)+ 2 AuthorsKen-ichiro Ishida24
Estimated H-index: 24
(University of Tsukuba)
A new chlorarachniophyte, Viridiuvalis adhaerens gen. et sp. nov. was isolated from the mucus on a coral reef from Zanpa Beach, Okinawa, Japan. The main vegetative stage of V. adhaerens consisted of unicellular coccoid cells with cell walls, although sarcinoid colonies and uniflagellate zoospores were also observed. V. adhaerens had chloroplasts with nucleomorphs and pyrenoids that were completely embedded in the chloroplast. A deep plate-like invagination of the periplastidal compartment (PPC) ...
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Published on Jul 15, 2017in Biochemical Journal 3.86
Anthony J. Michael33
Estimated H-index: 33
(University of Texas Southwestern Medical Center)
Since the emergence of the last common ancestor from which all extant life evolved, the metabolite repertoire of cells has increased and diversified. Not only has the metabolite cosmos expanded, but the ways in which the same metabolites are made have diversified. Enzymes catalyzing the same reaction have evolved independently from different protein folds; the same protein fold can produce enzymes recognizing different substrates, and enzymes performing different chemistries. Genes encoding usef...
8 Citations Source Cite
Published on Jul 1, 2017in Current Biology 9.25
Kai H. Edel7
Estimated H-index: 7
,
Elodie Marchadier3
Estimated H-index: 3
(University of Bristol)
+ 2 AuthorsAlistair M. Hetherington44
Estimated H-index: 44
(University of Bristol)
The calcium-based intracellular signalling system is used ubiquitously to couple extracellular stimuli to their characteristic intracellular responses. It is becoming clear from genomic and physiological investigations that while the basic elements in the toolkit are common between plants and animals, evolution has acted in such a way that, in plants, some components have diversified with respect to their animal counterparts, while others have either been lost or have never evolved in the plant ...
30 Citations Source Cite
Published on Jul 1, 2017in Current Biology 9.25
David Moreira52
Estimated H-index: 52
(Université Paris-Saclay),
Purificación López-García21
Estimated H-index: 21
(Université Paris-Saclay)
Summary Plastids, the photosynthetic organelles of eukaryotes, exhibit remarkably stable genome architecture. However, a recent study of microscopic red algae has found new record-sized plastid genomes with unusual architectures. These species form a new branch in the tree of red algae.
2 Citations Source Cite
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