Nucleomorph

Last updated
Nucleomorph chloroplast.svg
Diagram of a four membraned chloroplast containing a nucleomorph. Such a layout results from secondary endosymbiosis.

Nucleomorphs are small, vestigial eukaryotic nuclei found between the inner and outer pairs of membranes in certain plastids. They are thought to be vestiges of red and green algal nuclei that were engulfed by a larger eukaryote. Because the nucleomorph lies between two sets of membranes, nucleomorphs support the endosymbiotic theory and are evidence that the plastids containing them are complex plastids. Having two sets of membranes indicate that the plastid, a prokaryote, was engulfed by a eukaryote, an alga, which was then engulfed by another eukaryote, the host cell, making the plastid an example of secondary endosymbiosis. [1] [2]

Contents

Organisms with known nucleomorphs

As of 2007, only two monophyletic groups of organisms are known to contain plastids with a vestigial nucleus or nucleomorph: the cryptomonads [3] of the supergroup Cryptista and the chlorarachniophytes [4] of the supergroup Rhizaria, both of which have examples of sequenced nucleomorph genomes. [3] [4] Studies of the genomic organization and of the molecular phylogeny have shown that the nucleomorph of the cryptomonads used to be the nucleus of a red alga, whereas the nucleomorph of the chlorarchniophytes was the nucleus of a green alga. In both groups of organisms the plastids originate from engulfed photoautotrophic eukaryotes.

Of the two known plastids that contain nucleomorphs, both have four membranes, the nucleomorph residing in the periplastidial compartment, evidence of being engulfed by a eukaryote through phagocytosis. [1]

In 2020, genetic work identified the plastid in Lepidodinium and two previously undescribed dinoflagellates ("MGD" and "TGD") as being most closely related to the green alga Pedinomonas . The observation of a nucleomorph in Lepidodinium is controversial, but MGD and TGD are proven to have DNA-containing nucleomorphs. [5] The transcriptomes of the nucleomorphs have been sequenced. [6] One slight issue in understanding the sequence of evolution is that although the phylogenetic tree built from Lepidodinium-MGD-TGD's plastid is monophyletic, the tree built from their host-nucleus DNA is not, implying that they might have acquired very similar algae independently. [5]

Structure

A cryptomonad nucleomorph is typically much smaller than the host nucleus. A relatively large portion of its size is devoted to the nucleolus, which contains its own ribosomes and rRNA. [7] There seems to be nuclear pores observable by imaging, but genetic work has failed to find any protein appropriate for forming the nuclear pore complex. [8] [9]

There is one nucleomorph per plastid. The nucleomorph divides before the accompanying plastid. The dividing nucleomorph lacks a mitotic spindle, and the nucleomorph envelope persists throughout division. [7]

Between the plastid and the cytoplasm of the host there are four membranes: the inner and outer membranes of the chloroplast, the periplastid membrane, and the epiplastid membrane. The epiplastid membrane is encrusted with ribosomes (in cryptomonads) and is in many ways similar to a endoplasmic reticulum, hence the name "chloroplast endoplasmic reticulum" (cER). Plastid-targeted proteins encoded in the host genome must cross all four membranes to reach the plastid. First they use classic secretory signal peptides to cross the epiplastid membrane. Then the symbiont-specific ERAD-like machinery (SELMA) – encoded in the nucleomorph as a repurposed ERAD – pulls the protein from the epiplastid space (or the lumen of the cER) into the periplastid space (the cytoplasm of the symbiote). The standard chloroplast transit peptide then acts to cross the remaining two layers via TIC/TOC complex. [7]

The chlorarachniophytes, on the other hand, has no such thing as a cER, hence the initial import into the epiplastid space must occur by some other mechanism. It's only known that their plastid-targeted proteins are prefixed by both a signal peptide and a chloroplast-targeting peptide much like cryptomonads. Based on research done on apicomplexa, which also has 4 membranes but no cER, it's possible that the protein is first sent into the ER, then sent to the epiplastid space by the endomembrane sorting system. [10] Some sort of a pore may then move the peptide into the periplastid space, but there seems to be no SELMA-like pore in this group. It's only known that the TIC/TOC complex exists for crossing the last two layers. [11]

Nucleomorph genome

Nucleomorphs represent some of the smallest genomes ever sequenced. After the red or green alga was engulfed by a cryptomonad or chlorarachniophyte, respectively, its genome was reduced. The nucleomorph genomes of both cryptomonads and chlorarachniophytes converged upon a similar size from larger genomes. They retained only three chromosomes and many genes were transferred to the nucleus of the host cell, while others were lost entirely. [1] Chlorarachniophytes contain a nucleomorph genome that is diploid and cryptomonads contain a nucleomorph genome that is tetraploid. [12] The unique combination of host cell and complex plastid results in cells with four genomes: two prokaryotic genomes (mitochondrion and plastid of the red or green algae) and two eukaryotic genomes (nucleus of host cell and nucleomorph).

The model cryptomonad Guillardia theta became an important focus for scientists studying nucleomorphs. Its complete nucleomorph sequence was published in 2001, coming in at 551 Kbp. The G. theta sequence gave insight as to what genes were retained in nucleomorphs. Most of the genes that moved to the host cell involved protein synthesis, leaving behind a compact genome with mostly single-copy “housekeeping” genes (affecting transcription, translation, protein folding and degradation and splicing) and no mobile elements. The genome contains 513 genes, 465 of which code for protein. Thirty genes are considered “plastid” genes, coding for plastid proteins. [1] [13] It has three chromosomes with eukaryotic telomeres subtended by rRNA. [7]

The genome sequence of another organism, the chlorarachniophyte Bigelowiella natans indicates that its nucleomorph is probably the vestigial nucleus of a green alga, whereas the nucleomorph in G. theta probably came from a red alga. The B. natans genome is smaller than that of G. theta, with about 373 Kbp and contains 293 protein-coding genes as compared to the 465 genes in G. theta. B. natans also only has 17 genes that code for plastid proteins, again fewer than G. theta. Comparisons between the two organisms have shown that B. natans contains significantly more introns (852) than G. theta (17). B. natans also had smaller introns, ranging from 18-21 bp, whereas G. theta’s introns ranged from 42-52 bp. [1]

Both the genomes of B. natans and G. theta display evidence of genome reduction besides elimination of genes and tiny size, including elevated composition of adenine (A) and thymine (T), and high substitution rates. [4] [13] [14]

Persistence of nucleomorphs

There are no recorded instances of vestigial nuclei in any other secondary plastid-containing organisms, yet they have been retained independently in the cryptomonads and chlorarachniophytes. Plastid gene transfer happens frequently in many organisms, and it is unusual that these nucleomorphs have not disappeared entirely. One theory as to why these nucleomorphs have not disappeared as they have in other groups is that introns present in nucleomorphs are not recognized by host spliceosomes because they are too small and therefore cannot be cut and later incorporated into host DNA.

Nucleomorphs also often code for many of their own critical functions, like transcription and translation. [15] Some say that as long as there exists a gene in the nucleomorph that codes for proteins necessary for the plastid’s functioning that are not produced by the host cell, the nucleomorph will persist. [1] The cryptomonad nucleomorph also codes for genes that function in plastid maintenance. [7]

In cryptophytes and chlorarachniophytes all DNA transfer between the nucleomorph and host genome seems to have ceased, but the process is still going on in a few dinoflagellates (MGD and TGD). [16]

Tertiary endosymbiosis

The standard nucleomorph is the result of secondary endosymbiosis: a cyanobacterium first became the chloroplast of ancestral plants, which diverged into green and red algae among other groups; the algal cell is then captured by another eukaryote. The chloroplast is surrounded by 4 membranes: 2 layers resulting from the primary, and 2 resulting from the secondary. When the nucleus of the algal endosymbiont remains, it's called a "nucleomorph". [1]

Most tertiary endosymbiosis events end up with only the plastid retained. However, in the case of dinotoms (i.e. those having diatom endosymbionts), the symbiont's nucleus appears to be of normal size with a large amount of DNA, surrounded by plenty of cytoplasm. The symbiont even has its own DNA-containing mitochondria. As a result, the organism has two eukaryotic genomes and three prokaryotic-derived organelle genomes. [17]

See also

Related Research Articles

<span class="mw-page-title-main">Chloroplast</span> Plant organelle that conducts photosynthesis

A chloroplast is a type of organelle known as a plastid that conducts photosynthesis mostly in plant and algal cells. Chloroplasts have a high concentration of chlorophyll pigments which capture the energy from sunlight and convert it to chemical energy and release oxygen. The chemical energy created is then used to make sugar and other organic molecules from carbon dioxide in a process called the Calvin cycle. Chloroplasts carry out a number of other functions, including fatty acid synthesis, amino acid synthesis, and the immune response in plants. The number of chloroplasts per cell varies from one, in some unicellular algae, up to 100 in plants like Arabidopsis and wheat.

<span class="mw-page-title-main">Symbiogenesis</span> Evolutionary theory holding that eukaryotic organelles evolved through symbiosis with prokaryotes

Symbiogenesis is the leading evolutionary theory of the origin of eukaryotic cells from prokaryotic organisms. The theory holds that mitochondria, plastids such as chloroplasts, and possibly other organelles of eukaryotic cells are descended from formerly free-living prokaryotes taken one inside the other in endosymbiosis. Mitochondria appear to be phylogenetically related to Rickettsiales bacteria, while chloroplasts are thought to be related to cyanobacteria.

<span class="mw-page-title-main">Cryptomonad</span> Group of algae and colorless flagellates

The cryptomonads are a group of algae, most of which have plastids. They are traditionally considered a division of algae among phycologists, under the name of Cryptophyta. They are common in freshwater, and also occur in marine and brackish habitats. Each cell is around 10–50 μm in size and flattened in shape, with an anterior groove or pocket. At the edge of the pocket there are typically two slightly unequal flagella. Some may exhibit mixotrophy. They are classified as clade Cryptomonada, which is divided into two classes: heterotrophic Goniomonadea and phototrophic Cryptophyceae. The two groups are united under three shared morphological characteristics: presence of a periplast, ejectisomes with secondary scroll, and mitochondrial cristae with flat tubules. Genetic studies as early as 1994 also supported the hypothesis that Goniomonas was sister to Cryptophyceae. A study in 2018 found strong evidence that the common ancestor of Cryptomonada was an autotrophic protist.

<span class="mw-page-title-main">Plastid</span> Plant cell organelles that perform photosynthesis and store starch

A plastid is a membrane-bound organelle found in the cells of plants, algae, and some other eukaryotic organisms. Plastids are considered to be intracellular endosymbiotic cyanobacteria.

<span class="mw-page-title-main">Chlorarachniophyte</span> Group of algae

The chlorarachniophytes are a small group of exclusively marine algae widely distributed in tropical and temperate waters. They are typically mixotrophic, ingesting bacteria and smaller protists as well as conducting photosynthesis. Normally they have the form of small amoebae, with branching cytoplasmic extensions that capture prey and connect the cells together, forming a net. These extensions are dependent on the presence of light and polymerization of the actin cytoskeleton. They may also form flagellate zoospores, which characteristically have a single subapical flagellum that spirals backwards around the cell body, and walled coccoid cells.

<span class="mw-page-title-main">Chromista</span> Eukaryotic biological kingdom

Chromista is a proposed but polyphyletic biological kingdom, refined from the Chromalveolata, consisting of single-celled and multicellular eukaryotic species that share similar features in their photosynthetic organelles (plastids). It includes all eukaryotes whose plastids contain chlorophyll c and are surrounded by four membranes. If the ancestor already possessed chloroplasts derived by endosymbiosis from red algae, all non-photosynthetic Chromista have secondarily lost the ability to photosynthesise. Its members might have arisen independently as separate evolutionary groups from the last eukaryotic common ancestor.

<span class="mw-page-title-main">Kleptoplasty</span> Form of algae symbiosis

Kleptoplasty or kleptoplastidy is a process in symbiotic relationships whereby plastids, notably chloroplasts from algae, are sequestered by the host. The word is derived from Kleptes (κλέπτης) which is Greek for thief. The alga is eaten normally and partially digested, leaving the plastid intact. The plastids are maintained within the host, temporarily continuing photosynthesis and benefiting the host.

<span class="mw-page-title-main">Archaeplastida</span> Clade of eukaryotes containing land plants and some algae

The Archaeplastida are a major group of eukaryotes, comprising the photoautotrophic red algae (Rhodophyta), green algae, land plants, and the minor group glaucophytes. It also includes the non-photosynthetic lineage Rhodelphidia, a predatorial (eukaryotrophic) flagellate that is sister to the Rhodophyta, and probably the microscopic picozoans. The Archaeplastida have chloroplasts that are surrounded by two membranes, suggesting that they were acquired directly through a single endosymbiosis event by phagocytosis of a cyanobacterium. All other groups which have chloroplasts, besides the amoeboid genus Paulinella, have chloroplasts surrounded by three or four membranes, suggesting they were acquired secondarily from red or green algae. Unlike red and green algae, glaucophytes have never been involved in secondary endosymbiosis events.

An apicoplast is a derived non-photosynthetic plastid found in most Apicomplexa, including Toxoplasma gondii, and Plasmodium falciparum and other Plasmodium spp., but not in others such as Cryptosporidium. It originated from algae through secondary endosymbiosis; there is debate as to whether this was a green or red alga. The apicoplast is surrounded by four membranes within the outermost part of the endomembrane system. The apicoplast hosts important metabolic pathways like fatty acid synthesis, isoprenoid precursor synthesis and parts of the heme biosynthetic pathway.

<span class="mw-page-title-main">Ochrophyte</span> Phylum of algae

Ochrophytes, also known as heterokontophytes or stramenochromes, are a group of algae. They are the photosynthetic stramenopiles, a group of eukaryotes, organisms with a cell nucleus, characterized by the presence of two unequal flagella, one of which has tripartite hairs called mastigonemes. In particular, they are characterized by photosynthetic organelles or plastids enclosed by four membranes, with membrane-bound compartments called thylakoids organized in piles of three, chlorophyll a and c as their photosynthetic pigments, and additional pigments such as β-carotene and xanthophylls. Ochrophytes are one of the most diverse lineages of eukaryotes, containing ecologically important algae such as brown algae and diatoms. They are classified either as phylum Ochrophyta or Heterokontophyta, or as subphylum Ochrophytina within phylum Gyrista. Their plastids are of red algal origin.

<i>Guillardia</i> Genus of single-celled organisms

Guillardia is a genus of marine biflagellate cryptomonad algae with a plastid obtained through secondary endosymbiosis of a red alga.

<i>Hemiselmis</i> Genus of single-celled organisms

Hemiselmis is a genus of cryptomonads.

<i>Dinophysis</i> Genus of single-celled organisms

Dinophysis is a genus of dinoflagellates common in tropical, temperate, coastal and oceanic waters. It was first described in 1839 by Christian Gottfried Ehrenberg.

<span class="mw-page-title-main">Chloroplast DNA</span> DNA located in cellular organelles called chloroplasts

Chloroplast DNA (cpDNA), also known as plastid DNA (ptDNA) is the DNA located in chloroplasts, which are photosynthetic organelles located within the cells of some eukaryotic organisms. Chloroplasts, like other types of plastid, contain a genome separate from that in the cell nucleus. The existence of chloroplast DNA was identified biochemically in 1959, and confirmed by electron microscopy in 1962. The discoveries that the chloroplast contains ribosomes and performs protein synthesis revealed that the chloroplast is genetically semi-autonomous. The first complete chloroplast genome sequences were published in 1986, Nicotiana tabacum (tobacco) by Sugiura and colleagues and Marchantia polymorpha (liverwort) by Ozeki et al. Since then, tens of thousands of chloroplast genomes from various species have been sequenced.

Bigelowiella natans is a species of Chlorarachniophyte alga that is a model organism for the Rhizaria.

Durinskia is a genus of dinoflagellates that can be found in freshwater and marine environments. This genus was created to accommodate its type species, Durinskia baltica, after major classification discrepancies were found. While Durinskia species appear to be typical dinoflagellates that are armored with cellulose plates called theca, the presence of a pennate diatom-derived tertiary endosymbiont is their most defining characteristic. This genus is significant to the study of endosymbiotic events and organelle integration since structures and organelle genomes in the tertiary plastids are not reduced. Like some dinoflagellates, species in Durinskia may cause blooms.

<span class="mw-page-title-main">Plastid evolution</span> Evolution

A plastid is a membrane-bound organelle found in plants, algae and other eukaryotic organisms that contribute to the production of pigment molecules. Most plastids are photosynthetic, thus leading to color production and energy storage or production. There are many types of plastids in plants alone, but all plastids can be separated based on the number of times they have undergone endosymbiotic events. Currently there are three types of plastids; primary, secondary and tertiary. Endosymbiosis is reputed to have led to the evolution of eukaryotic organisms today, although the timeline is highly debated.

Lepidodinium is a genus of dinoflagellates belonging to the family Gymnodiniaceae. Lepidodinium is a genus of green dinoflagellates in the family Gymnodiniales. It contains two different species, Lepidodiniumchlorophorum and Lepidodinium viride. They are characterised by their green colour caused by a plastid derived from Pedinophyceae, a green algae group. This plastid has retained chlorophyll a and b, which is significant because it differs from the chlorophyll a and c usually observed in dinoflagellate peridinin plastids. They are the only known dinoflagellate genus to possess plastids derived from green algae. Lepidodinium chlorophorum is known to cause sea blooms, partially off the coast of France, which has dramatic ecological and economic consequences. Lepidodinium produces some of the highest volumes of Transparent Exopolymer Particles of any phytoplankton, which can contribute to bivalve death and the creation of anoxic conditions in blooms, as well as playing an important role in carbon cycling in the ocean.

<i>Rapaza</i> Monospecific genus of predatory algae

Rapaza viridis is a species of single-celled flagellate within the Euglenophyceae, a group of algae. It is the only species within the genus Rapaza, family Rapazidae and order Rapazida. It was discovered in a tide pool in British Columbia and described in 2012.

References

  1. 1 2 3 4 5 6 7 Archibald, J.M.; Lane, C.E. (2009). "Going, Going, Not Quite Gone: Nucleomorphs as a Case Study in Nuclear Genome Reduction". Journal of Heredity. 100 (5): 582–90. doi: 10.1093/jhered/esp055 . PMID   19617523.
  2. ↑ Reyes-Prieto, Adrian; Weber, Andreas P.M.; Bhattacharya, Debashish (2007). "The Origin and Establishment of the Plastid in Algae and Plants". Annual Review of Genetics. 41 (1): 147–68. doi:10.1146/annurev.genet.41.110306.130134. PMID   17600460. S2CID   8966320.
  3. 1 2 Lane, C. E.; Van Den Heuvel, K.; Kozera, C.; Curtis, B. A.; Parsons, B. J.; Bowman, S.; Archibald, J. M. (2007). "Nucleomorph genome of Hemiselmis andersenii reveals complete intron loss and compaction as a driver of protein structure and function". Proceedings of the National Academy of Sciences. 104 (50): 19908–19913. Bibcode:2007PNAS..10419908L. doi: 10.1073/pnas.0707419104 . PMC   2148396 . PMID   18077423.
  4. 1 2 3 Gilson, P. R.; Su, V.; Slamovits, C. H.; Reith, M. E.; Keeling, P. J.; McFadden, G. I. (2006). "Complete nucleotide sequence of the chlorarachniophyte nucleomorph: Nature's smallest nucleus". Proceedings of the National Academy of Sciences. 103 (25): 9566–9571. Bibcode:2006PNAS..103.9566G. doi: 10.1073/pnas.0600707103 . PMC   1480447 . PMID   16760254.
  5. 1 2 Sarai, C; Tanifuji, G; Nakayama, T; Kamikawa, R; Takahashi, K; Yazaki, E; Matsuo, E; Miyashita, H; Ishida, KI; Iwataki, M; Inagaki, Y (10 March 2020). "Dinoflagellates with relic endosymbiont nuclei as models for elucidating organellogenesis". Proceedings of the National Academy of Sciences of the United States of America. 117 (10): 5364–5375. Bibcode:2020PNAS..117.5364S. doi: 10.1073/pnas.1911884117 . PMC   7071878 . PMID   32094181.
  6. ↑ Putative genome features of relic green alga-derived nuclei in dinoflagellates and future perspectives as model organisms
  7. 1 2 3 4 5 McFadden, Geoffrey I. (September 2017). "The cryptomonad nucleomorph". Protoplasma. 254 (5): 1903–1907. doi:10.1007/s00709-017-1153-5. PMID   28828570.
  8. ↑ Irwin, NAT; Keeling, PJ (1 March 2019). "Extensive Reduction of the Nuclear Pore Complex in Nucleomorphs". Genome Biology and Evolution. 11 (3): 678–687. doi:10.1093/gbe/evz029. PMC   6411479 . PMID   30715330.
  9. ↑ Zauner, S; Heimerl, T; Moog, D; Maier, UG (1 June 2019). "The Known, the New, and a Possible Surprise: A Re-Evaluation of the Nucleomorph-Encoded Proteome of Cryptophytes". Genome Biology and Evolution. 11 (6): 1618–1629. doi:10.1093/gbe/evz109. PMC   6559170 . PMID   31124562.
  10. ↑ van Dooren, Giel G; Schwartzbach, Steven D; Osafune, Tetsuaki; McFadden, Geoffrey I (December 2001). "Translocation of proteins across the multiple membranes of complex plastids". Biochimica et Biophysica Acta (BBA) - Molecular Cell Research. 1541 (1–2): 34–53. doi:10.1016/S0167-4889(01)00154-9. PMID   11750661.
  11. ↑ Sheiner, L; Striepen, B (February 2013). "Protein sorting in complex plastids". Biochimica et Biophysica Acta (BBA) - Molecular Cell Research. 1833 (2): 352–9. doi:10.1016/j.bbamcr.2012.05.030. PMC   3494742 . PMID   22683761.
  12. ↑ Hirakawa, Yoshihisa; Ishida, Ken-Ichiro (2014-04-01). "Polyploidy of Endosymbiotically Derived Genomes in Complex Algae". Genome Biology and Evolution. 6 (4): 974–980. doi:10.1093/gbe/evu071. ISSN   1759-6653. PMC   4007541 . PMID   24709562.
  13. 1 2 Archibald, John M (2007). "Nucleomorph Genomes: Structure, Function, Origin and Evolution". BioEssays. 29 (4): 392–402. doi:10.1002/bies.20551. PMID   17373660.
  14. ↑ Douglas, SE; Zauner, S; Fraunholz, M; Beaton, M; Penny, S; et al. (2001). "The highly reduced genome of an enslaved algal nucleus". Nature . 410 (6832): 1091–1096. Bibcode:2001Natur.410.1091D. doi: 10.1038/35074092 . PMID   11323671.
  15. ↑ Curtis, Bruce et al. "Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs." Nature 492 :59-65
  16. ↑ Organellogenesis still a work in progress in novel dinoflagellates (2020)
  17. ↑ Tertiary Endosymbiosis in Two Dinotoms Has Generated Little Change in the Mitochondrial Genomes of Their Dinoflagellate Hosts and Diatom Endosymbionts - PLOS

According to GenBank release 164 (Feb 2008), there are 13 Cercozoa and 181 Cryptophyta entries (an entry is the submission of a sequence to the DDBJ/EMBL/GenBank public database of sequences). Most sequenced organisms were:

Guillardia theta: 54; Rhodomonas salina: 18; Cryptomonas sp.: 15; Chlorarachniophyceae sp.:10; Cryptomonas paramecium: 9; Cryptomonas erosa: 7.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.