Biology:Paulinella

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Short description: Genus of single-celled organisms

Paulinella
Paulinella chromatophora.jpg
Scientific classification e
Domain: Eukaryota
Clade: Diaphoretickes
Clade: SAR
Phylum: Cercozoa
Class: Imbricatea
Order: Euglyphida
Family: Paulinellidae
Genus: Paulinella
Lauterborn[1][2]
Type species
Paulinella chromatophora
Lauterborn 1895[1]
Species
  • P. agassizi, 2009[3]
  • P. bulloides[4]
  • P. carsoni, 2009[3]
  • P. chromatophora, 1895[1][5]
  • P. gigantica, 2009[3]
  • P. gracilis[6][7]
  • P. indentata, 1996[8]
  • P. intermedia, 1993[9]
  • P. lauterborni, 2009[3]
  • P. longichromatophora, 2016[10][11]
  • P. micropora, 2017[12][11]
  • P. multipora, 2009[3]
  • P. osloensis[4]
  • P. ovalis, 1919[13][14]
  • P. quinqueloba[4]
  • P. riveroi[4]
  • P. sphaeroides[4]
  • P. subcarinata[4]
  • P. subsphaerica[4]
  • P. suzukii, 2009[3]
  • P. trinitatensis[4]
Synonyms

Calycomonas[6]

Paulinella is a genus of at least eleven[15][1][6][3] species including both freshwater and marine amoeboids.[16] Like many members of euglyphids it is covered by rows of siliceous scales, and use filose pseudopods to crawl over the substrate of the benthic zone.[17]

Its most famous members are the three photosynthetic species P. chromatophora, P. micropora and P. longichromatophora, the first two being freshwater forms and the third a marine form,[18] which have recently (in evolutionary terms) taken on a cyanobacterium as an endosymbiont.[19][20] As a result they are no longer able to perform phagocytosis like their non-photosynthetic relatives.[21] P. chromatophora was discovered in sediments of the river Rhine on Christmas Eve 1894 by German biologist Robert Lauterborn, who named it Paulinella after his stepmother Pauline.[22][23] The event to permanent endosymbiosis probably occurred with a cyanobiont.[24] The resulting organelle is a photosynthetic plastid that is often referred to as a 'cyanelle' or chromatophore, and is the only other known primary endosymbiosis event of photosynthetic cyanobacteria,[18][16] although primary endosymbiosis with a non-photosynthetic cyanobacterial symbiont have occurred in the diatom family Rhopalodiaceae.[25] The endosymbiotic event happened about 90–140 million years ago when an α-cyanobacterium (rather than a β-cyanobacterium which the plastids in Archaeplastida originates from),[26] who diverged about 500 million years ago from the ancestors of its sister clade that consist of the living members of the cyanobacteria genera Prochlorococcus and Synechococcus,[27][28][5][16] was permanently established within the amoeba.[5][29]

This is striking because the chloroplasts of all other known photosynthetic eukaryotes derive ultimately from a single cyanobacterium endosymbiont, which was taken in about 1.6 billion years ago by an ancestral archaeplastidan (and subsequently adopted into other eukaryote groups through secondary endosymbiosis events, and later tertiary and quaternary endosymbiosis, etc). The only exception is the ciliate Pseudoblepharisma tenue, which in addition to a photosynthetic symbiont that is a captured green algae, also has a photosynthetic prokaryote as a symbiont; a purple bacteria with a reduced genome, instead of a cyanobacteria.[30]

The chromatophore genome has gone through a reduction, and is now just one third the size of the genome of its closest free living relatives, but still 10-fold larger than most plastid genomes. Some of the genes have been lost, others have migrated to the amoeba's nucleus through endosymbiotic gene transfer.[31] It is estimated that 0.3-0.8% of Paulinellas genes were derived from its endosymbiont, in addition to a small amount of genes from other organisms.[32] Other genes have degenerated due to Muller's ratchet – accumulations of harmful mutations due to genetic isolation, and have probably been replaced with genes from other microbes through horizontal gene transfer.[33][34] Some of the genes the nucleus received from the chromatophore were multiplied many times over through a "copy-paste" mechanism called retrotransposition, enabling them to function more efficiently and making them more tolerant against toxic compounds associated with photosynthesis. This changed the metabolism of the amoeba so much that it could no longer feed on microbes like its ancestors, and it became completely dependent on its endosymbiont, which in turn has lost so many genes it can no longer survive outside its host cell.[35][36]

Paulinella show both a very slow growth rate and sensitivity to light, and prefer low light conditions, probably as a protection against oxidative stress and other light related stress as it doesn't have the same degree of photoprotection mechanisms found in organisms with a photosynthetic apparatus of Archaeplastid origin, which has a much longer evolutionary history.[37]

The nuclear genes of P. chromatophora (those regions not affected by endosymbiotic gene transfer) are most closely related to the heterotrophic P. ovalis.[38] P. ovalis is a marine heterotrophic species of Paulinella that has been shown to eat cyanobacteria and bacteria.[39] P. ovalis also have at least two cyanobacterial-like genes, which were probably integrated into their genome through horizontal gene transfer from its cyanobacterial prey. Similar genes could have made the photosynthetic species pre-equipped to accept the chromatophore.[40] The presence of extant heterotrophic lineages makes Paulinella a perfect model for unravelling early stages of primary endosymbiosis event and studying the post symbiotic genome evolution of both the plastid and the host.[41]

References

  1. ↑ 1.0 1.1 1.2 1.3 Lauterborn, R. (1895). "Protozoenstudien. II. Paulinella chromatophora nov. gen. nov. spec., ein beschalter Rhizopode des Süßwassers mit blaugrünen chromatophorenartigen Einschlüssen". Zeitschrift für Wissenschaftliche Zoologie 59: 537–544. 
  2. ↑ M.D. Guiry in Guiry, M.D. & Guiry, G.M. 2013. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org; searched on 4 March 2013.
  3. ↑ 3.0 3.1 3.2 3.3 3.4 3.5 3.6 Nicholls, Kenneth H. (November 2009). "Six new marine species of the genus Paulinella (Rhizopoda: Filosea, or Rhizaria: Cercozoa)". Journal of the Marine Biological Association of the United Kingdom 89 (7): 1415–1425. doi:10.1017/S0025315409000514. Bibcode: 2009JMBUK..89.1415N. https://www.cambridge.org/core/journals/journal-of-the-marine-biological-association-of-the-united-kingdom/article/abs/six-new-marine-species-of-the-genus-paulinella-rhizopoda-filosea-or-rhizaria-cercozoa/F47539984556457F29A76B264C0A5B55. Retrieved 18 August 2022. 
  4. ↑ 4.0 4.1 4.2 4.3 4.4 4.5 4.6 4.7 "Paulinella". http://itis.gov/servlet/SingleRpt/SingleRpt?search_topic=TSN&search_value=44014. 
  5. ↑ 5.0 5.1 5.2 Marin, B; Nowack, EC; Glöckner, G; Melkonian, M (5 June 2007). "The ancestor of the Paulinella chromatophore obtained a carboxysomal operon by horizontal gene transfer from a Nitrococcus-like gamma-proteobacterium.". BMC Evolutionary Biology 7 (1): 85. doi:10.1186/1471-2148-7-85. PMID 17550603. Bibcode: 2007BMCEE...7...85M. 
  6. ↑ 6.0 6.1 6.2 Lohmann, H. (1908). "Untersuchungen zur Feststellung des vollständigen Gehaltes des Meeres an Plankton". Komm. Z. Wissensch. Untersuch. D. Deutschen Meere in Kiel und D. Biologischen Anstalt Auf Helgoland. Wissensch. Meeresuntersuch., N.F., Abt. Kiel, Bd. 10: 131–137. 
  7. ↑ Vørs, Naja (1 September 1992). "Heterotrophic Amoebae, Flagellates and Heliozoa from the Tvärminne Area, Gulf of Finland, in 1988–1990". Ophelia 36 (1): 1–109. doi:10.1080/00785326.1992.10429930. ISSN 0078-5326. https://www.tandfonline.com/doi/abs/10.1080/00785326.1992.10429930. Retrieved 19 August 2022. 
  8. ↑ Hannah, Fiona; Rogerson, Andrew; Anderson, O. Roger (January 1996). "A Description of Paulinella indentata N. Sp. (Filosea: Euglyphina) from Subtidal Coastal Benthic Sediments" (in en). The Journal of Eukaryotic Microbiology 43 (1): 1–4. doi:10.1111/j.1550-7408.1996.tb02464.x. ISSN 1066-5234. https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1550-7408.1996.tb02464.x. 
  9. ↑ Vørs, Naja (May 1993). "Marine Heterotrophic Amoebae, Flagellates and Heliozoa From Belize (Central America) and Tenerife (Canary Islands), With Descriptions of New Species, Luffisphaera Bulbochaete N. Sp., L. Longihastis N. Sp., L. Turriformis N. Sp. and Paulinella Intermedia N. Sp." (in en). The Journal of Eukaryotic Microbiology 40 (3): 272–287. doi:10.1111/j.1550-7408.1993.tb04917.x. ISSN 1066-5234. https://onlinelibrary.wiley.com/doi/10.1111/j.1550-7408.1993.tb04917.x. Retrieved 19 August 2022. 
  10. ↑ Kim, Sunju; Park, Myung Gil (1 February 2016). "Paulinella longichromatophora sp. nov., a New Marine Photosynthetic Testate Amoeba Containing a Chromatophore" (in en). Protist 167 (1): 1–12. doi:10.1016/j.protis.2015.11.003. ISSN 1434-4610. PMID 26709891. https://www.sciencedirect.com/science/article/abs/pii/S1434461015001157. Retrieved 19 August 2022. 
  11. ↑ 11.0 11.1 "Paulinella" (in English). Bethesda, MD: National Center for Biotechnology Information. https://www.ncbi.nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi?mode=Tree&id=39716&lvl=3&keep=1&srchmode=1&unlock. "Lineage(full) cellular organisms; Eukaryota; Rhizaria; Cercozoa; Imbricatea; Silicofilosea; Euglyphida; Paulinellidae" 
  12. ↑ Lhee, Duckhyun; Yang, Eun Chan; Kim, Jong Im; Nakayama, Takuro; Zuccarello, Giuseppe; Andersen, Robert A.; Yoon, Hwan Su (April 2017). "Diversity of the Photosynthetic Paulinella Species, with the Description of Paulinella micropora sp. nov. and the Chromatophore Genome Sequence for strain KR01". Protist 168 (2): 155–170. doi:10.1016/j.protis.2017.01.003. ISSN 1618-0941. PMID 28262587. https://pubmed.ncbi.nlm.nih.gov/28262587/. 
  13. ↑ Wulff, A. (1919). "Ueber das Kleinplankton der Barentssee". Wissenschaftliche Meeresunterschungen. Neue Folge Abteilung Helgoland 13: 95–125. 
  14. ↑ Johnson, Paul W.; Hargraves, Paul E.; Sieburth, JOHN McN. (November 1988). "Ultrastructure and Ecology of Calycomonas ovalis Wulff, 1919, (Chrysophyceae) and Its Redescription as a Testate Rhizopod, Paulinella ovalis N. Comb. (Filosea: Euglyphina) 1" (in en). The Journal of Protozoology 35 (4): 618–626. doi:10.1111/j.1550-7408.1988.tb04160.x. https://doi.org/10.1111/j.1550-7408.1988.tb04160.x. 
  15. ↑ "Species Search :: AlgaeBase". https://www.algaebase.org/search/species/?name=paulinella. 
  16. ↑ 16.0 16.1 16.2 Gabr, Arwa; Grossman, Arthur R.; Bhattacharya, Debashish (2020-05-05). Palenik, B.. ed. "Paulinella, a model for understanding plastid primary endosymbiosis". Journal of Phycology (Wiley) 56 (4): 837–843. doi:10.1111/jpy.13003. ISSN 0022-3646. PMID 32289879. Bibcode: 2020JPcgy..56..837G. 
  17. ↑ Nakayama, Takuro; Archibald, John M. (2012). "Evolving a photosynthetic organelle". BMC Biology 10: 35. doi:10.1186/1741-7007-10-35. PMID 22531210. 
  18. ↑ 18.0 18.1 Lhee, Duckhyun; Ha, Ji-San; Kim, Sunju; Park, Myung Gil; Bhattacharya, Debashish; Yoon, Hwan Su (2019-02-22). "Evolutionary dynamics of the chromatophore genome in three photosynthetic Paulinella species". Scientific Reports (Nature) 9 (1): 2560. doi:10.1038/s41598-019-38621-8. PMID 30796245. Bibcode: 2019NatSR...9.2560L. 
  19. ↑  , Wikidata Q21090155
  20. ↑ McCutcheon, John P. (6 October 2021). "The Genomics and Cell Biology of Host-Beneficial Intracellular Infections" (in en). Annual Review of Cell and Developmental Biology 37 (1): 115–142. doi:10.1146/annurev-cellbio-120219-024122. ISSN 1081-0706. PMID 34242059. https://www.annualreviews.org/doi/10.1146/annurev-cellbio-120219-024122. Retrieved 19 August 2022. 
  21. ↑ Gagat, Przemysław; Mackiewicz, Paweł (January 2017). "Cymbomonas tetramitiformis - a peculiar prasinophyte with a taste for bacteria sheds light on plastid evolution". Symbiosis 71 (1): 1–7. doi:10.1007/s13199-016-0464-1. PMID 28066124. PMC 5167767. Bibcode: 2017Symbi..71....1G. https://d-nb.info/1120829321/34. Retrieved 18 August 2022. 
  22. ↑ Archibald, John M. (2017). "Evolution: Protein Import in a Nascent Photosynthetic Organelle". Current Biology 27 (18): R1004–R1006. doi:10.1016/j.cub.2017.08.013. PMID 28950079. 
  23. ↑ One Plus One Equals One: Symbiosis and the evolution of complex life
  24. ↑ Vries, Jan de; Gould, Sven B. (2018-01-15). "The monoplastidic bottleneck in algae and plant evolution" (in en). Journal of Cell Science 131 (2): jcs203414. doi:10.1242/jcs.203414. ISSN 0021-9533. PMID 28893840. https://www.biorxiv.org/content/biorxiv/early/2017/02/22/109975.full.pdf. 
  25. ↑ Nakayama, Takuro; Inagaki, Yuji (12 October 2017). "Genomic divergence within non-photosynthetic cyanobacterial endosymbionts in rhopalodiacean diatoms" (in en). Scientific Reports (Nature) 7 (1): 13075. doi:10.1038/s41598-017-13578-8. ISSN 2045-2322. PMID 29026213. Bibcode: 2017NatSR...713075N. 
  26. ↑ Nowack, Eva C. M.; Price, Dana C.; Bhattacharya, Debashish; Singer, Anna; Melkonian, Michael; Grossman, Arthur R. (2016). "Gene transfers from diverse bacteria compensate for reductive genome evolution in the chromatophore of Paulinella chromatophora". Proceedings of the National Academy of Sciences 113 (43): 12214–12219. doi:10.1073/pnas.1608016113. PMID 27791007. Bibcode: 2016PNAS..11312214N. 
  27. ↑ Sánchez-Baracaldo, Patricia; Raven, John A.; Pisani, Davide; Knoll, Andrew H. (2017-09-12). "Early photosynthetic eukaryotes inhabited low-salinity habitats" (in en). Proceedings of the National Academy of Sciences 114 (37): E7737–E7745. doi:10.1073/pnas.1620089114. ISSN 0027-8424. PMID 28808007. Bibcode: 2017PNAS..114E7737S. 
  28. ↑  , Wikidata Q36374426
  29. ↑ Lewis, Louise A. (12 September 2017). "Hold the salt: Freshwater origin of primary plastids" (in en). Proceedings of the National Academy of Sciences 114 (37): 9759–9760. doi:10.1073/pnas.1712956114. ISSN 0027-8424. PMID 28860199. Bibcode: 2017PNAS..114.9759L. 
  30. ↑ Muñoz-Gómez, Sergio A.; Kreutz, Martin; Hess, Sebastian (11 June 2021). "A microbial eukaryote with a unique combination of purple bacteria and green algae as endosymbionts" (in en). Science Advances 7 (24): eabg4102. doi:10.1126/sciadv.abg4102. ISSN 2375-2548. PMID 34117067. Bibcode: 2021SciA....7.4102M. 
  31. ↑ Zhang, Ru; Nowack, Eva C. M.; Price, Dana C.; Bhattacharya, Debashish; Grossman, Arthur R. (1 April 2017). "Impact of light intensity and quality on chromatophore and nuclear gene expression in Paulinella chromatophora, an amoeba with nascent photosynthetic organelles". The Plant Journal: For Cell and Molecular Biology 90 (2): 221–234. doi:10.1111/tpj.13488. PMID 28182317. 
  32. ↑ Nowack, E. C.; Vogel, H.; Groth, M.; Grossman, A. R.; Melkonian, M.; Glöckner, G. (2011). "Endosymbiotic gene transfer and transcriptional regulation of transferred genes in Paulinella chromatophora". Molecular Biology and Evolution 28 (1): 407–422. doi:10.1093/molbev/msq209. PMID 20702568. 
  33. ↑ Nowack, Eva C. M.; Price, Dana C.; Bhattacharya, Debashish; Singer, Anna; Melkonian, Michael; Grossman, Arthur R. (25 October 2016). "Gene transfers from diverse bacteria compensate for reductive genome evolution in the chromatophore of Paulinella chromatophora" (in en). Proceedings of the National Academy of Sciences 113 (43): 12214–12219. doi:10.1073/pnas.1608016113. PMID 27791007. Bibcode: 2016PNAS..11312214N. 
  34. ↑ Callier, Viviane (8 June 2022). "Mitochondria and the origin of eukaryotes". Knowable Magazine. doi:10.1146/knowable-060822-2. https://knowablemagazine.org/article/living-world/2022/mitochondria-origin-eukaryotes. Retrieved 18 August 2022. 
  35. ↑ "Microbe study sheds light on a critical step in the evolution of life on Earth". June 2022. https://english.elpais.com/science-tech/2022-06-01/microbe-study-sheds-light-on-a-critical-step-in-the-evolution-of-life-on-earth.html. 
  36. ↑ "Uncovering An Evolutionary Process That Enabled Diversity of Plant Life on Earth". https://carnegiescience.edu/news/uncovering-evolutionary-process-enabled-diversity-plant-life-earth. 
  37. ↑ Gabr, Arwa; Zournas, Apostolos; Stephens, Timothy G.; Dismukes, G. Charles; Bhattacharya, Debashish (2022). "Evidence for a robust photosystem II in the photosynthetic amoeba Paulinella". New Phytologist 234 (3): 934–945. doi:10.1111/nph.18052. PMID 35211975. https://nph.onlinelibrary.wiley.com/doi/full/10.1111/nph.18052. 
  38. ↑ Patrick J. Keeling (2004). "Diversity and evolutionary history of plastids and their hosts". American Journal of Botany 91 (10): 1481–1493. doi:10.3732/ajb.91.10.1481. PMID 21652304. 
  39. ↑ Johnson, Paul W.; Hargraves, Paul E.; Sieburth, JOHN McN. (November 1988). "Ultrastructure and Ecology of Calycomonas ovalis Wulff, 1919, (Chrysophyceae) and Its Redescription as a Testate Rhizopod, Paulinella ovalis N. Comb. (Filosea: Euglyphina) 1" (in en). The Journal of Protozoology 35 (4): 618–626. doi:10.1111/j.1550-7408.1988.tb04160.x. ISSN 0022-3921. https://onlinelibrary.wiley.com/doi/10.1111/j.1550-7408.1988.tb04160.x. 
  40. ↑ Smith, David (1 January 2013). "Steal My Sunshine" (in en). The Scientist Magazine®. https://www.the-scientist.com/features/steal-my-sunshine-39996. 
  41. ↑ Gabr, Arwa; Grossman, Arthur R.; Bhattacharya, Debashish (August 2020). Palenik, B.. ed. "Paulinella , a model for understanding plastid primary endosymbiosis" (in en). Journal of Phycology 56 (4): 837–843. doi:10.1111/jpy.13003. ISSN 0022-3646. PMID 32289879. Bibcode: 2020JPcgy..56..837G. 

Wikidata ☰ Q3815918 entry



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