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Paulinella

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Paulinella
Scientific classification Edit this classification
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
Synonyms

Calycomonas[6]

Paulinella is a genus of at least eleven[15][1][6][3] species including both freshwater and marine amoeboids.[16]

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,[17] which have recently (in evolutionary terms) taken on a cyanobacterium as an endosymbiont.[18][19] As a result they are no longer able to perform phagocytosis like their non-photosynthetic relatives.[20] The event to permanent endosymbiosis probably occurred with a cyanobiont.[21] 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,[17][16] although primary endosymbiosis with a non-photosynthetic cyanobacterial symbiont have occurred in the diatom family Rhopalodiaceae.[22] The endosymbiotic event happened about 90–140 million years ago in a cyanobacterial species which diverged about 500 million years ago[23][24] from the ancestors of its sister clade that consist of the living members of the Prochlorococcus and Synechococcus cyanobacteria genera,[5][16] which is a different clade to the plastids belonging to the Archaeplastida.[5][25]

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.[26]

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.[27] 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.[28][29] 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.[30][31]

The nuclear genes of P. chromatophora (those regions not modified by the symbiont) are most closely related to the heterotrophic P. ovalis.[32] 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.[33]

References

  1. ^ a b c d 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. ^ a b c d e f g 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. S2CID 86359271. Retrieved 18 August 2022.
  4. ^ a b c d e f g h "Paulinella". Integrated Taxonomic Information System. Retrieved 28 January 2008.
  5. ^ a b c 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: 85. doi:10.1186/1471-2148-7-85. PMC 1904183. PMID 17550603.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  6. ^ a b c 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. 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". The Journal of Eukaryotic Microbiology. 43 (1): 1–4. doi:10.1111/j.1550-7408.1996.tb02464.x. ISSN 1066-5234. S2CID 84358420.
  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". The Journal of Eukaryotic Microbiology. 40 (3): 272–287. doi:10.1111/j.1550-7408.1993.tb04917.x. ISSN 1066-5234. S2CID 221852241. 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". Protist. 167 (1): 1–12. doi:10.1016/j.protis.2015.11.003. ISSN 1434-4610. PMID 26709891. Retrieved 19 August 2022.
  11. ^ a b "Paulinella". NCBI taxonomy. Bethesda, MD: National Center for Biotechnology Information. Retrieved 4 January 2019. 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.
  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". The Journal of Protozoology. 35 (4): 618–626. doi:10.1111/j.1550-7408.1988.tb04160.x.
  15. ^ "Species Search :: AlgaeBase". www.algaebase.org. Retrieved 19 August 2022.
  16. ^ a b c Gabr, Arwa; Grossman, Arthur R.; Bhattacharya, Debashish (5 May 2020). Palenik, B. (ed.). "Paulinella, a model for understanding plastid primary endosymbiosis". Journal of Phycology. 56 (4). Wiley: 837–843. doi:10.1111/jpy.13003. ISSN 0022-3646. PMC 7734844. PMID 32289879.
  17. ^ a b Lhee, Duckhyun; Ha, Ji-San; Kim, Sunju; Park, Myung Gil; Bhattacharya, Debashish; Yoon, Hwan Su (22 February 2019). "Evolutionary dynamics of the chromatophore genome in three photosynthetic Paulinella species". Scientific Reports. 9 (1). Nature: 2560. Bibcode:2019NatSR...9.2560L. doi:10.1038/s41598-019-38621-8. PMC 6384880. PMID 30796245.
  18. ^ Laura Wegener Parfrey; Erika Barbero; Elyse Lasser; Micah Dunthorn; Debashish Bhattacharya; David J Patterson; Laura A Katz (December 2006). "Evaluating support for the current classification of eukaryotic diversity". PLOS Genetics. 2 (12): e220. doi:10.1371/JOURNAL.PGEN.0020220. ISSN 1553-7390. PMC 1713255. PMID 17194223. Wikidata Q21090155.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  19. ^ McCutcheon, John P. (6 October 2021). "The Genomics and Cell Biology of Host-Beneficial Intracellular Infections". Annual Review of Cell and Developmental Biology. 37 (1): 115–142. doi:10.1146/annurev-cellbio-120219-024122. ISSN 1081-0706. PMID 34242059. S2CID 235786110. Archived from the original on 7 July 2022. Retrieved 19 August 2022.
  20. ^ 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. PMC 5167767. PMID 28066124. Retrieved 18 August 2022.
  21. ^ Vries, Jan de; Gould, Sven B. (15 January 2018). "The monoplastidic bottleneck in algae and plant evolution". Journal of Cell Science. 131 (2): jcs203414. doi:10.1242/jcs.203414. ISSN 0021-9533. PMID 28893840.
  22. ^ Nakayama, Takuro; Inagaki, Yuji (12 October 2017). "Genomic divergence within non-photosynthetic cyanobacterial endosymbionts in rhopalodiacean diatoms". Scientific Reports. 7 (1). Nature: 13075. Bibcode:2017NatSR...713075N. doi:10.1038/s41598-017-13578-8. ISSN 2045-2322. PMC 5638926. PMID 29026213.
  23. ^ Sánchez-Baracaldo, Patricia; Raven, John A.; Pisani, Davide; Knoll, Andrew H. (12 September 2017). "Early photosynthetic eukaryotes inhabited low-salinity habitats". Proceedings of the National Academy of Sciences. 114 (37): E7737–E7745. doi:10.1073/pnas.1620089114. ISSN 0027-8424. PMC 5603991. PMID 28808007.
  24. ^ Luis Delaye; Cecilio Valadez-Cano; Bernardo Pérez-Zamorano (15 March 2016). "How Really Ancient Is Paulinella Chromatophora?". PLOS Currents. 8. doi:10.1371/CURRENTS.TOL.E68A099364BB1A1E129A17B4E06B0C6B. ISSN 2157-3999. PMC 4866557. PMID 28515968. Wikidata Q36374426.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  25. ^ Lewis, Louise A. (12 September 2017). "Hold the salt: Freshwater origin of primary plastids". Proceedings of the National Academy of Sciences. 114 (37): 9759–9760. doi:10.1073/pnas.1712956114. ISSN 0027-8424. PMC 5604047. PMID 28860199.
  26. ^ 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". Science Advances. 7 (24): eabg4102. Bibcode:2021SciA....7.4102M. doi:10.1126/sciadv.abg4102. ISSN 2375-2548. PMC 8195481. PMID 34117067.
  27. ^ 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.
  28. ^ 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". Proceedings of the National Academy of Sciences. 113 (43): 12214–12219. doi:10.1073/pnas.1608016113. PMC 5087059. PMID 27791007.
  29. ^ Callier, Viviane (8 June 2022). "Mitochondria and the origin of eukaryotes". Knowable Magazine. doi:10.1146/knowable-060822-2. Retrieved 18 August 2022.
  30. ^ Microbe study sheds light on a critical step in the evolution of life on Earth
  31. ^ Uncovering An Evolutionary Process That Enabled Diversity Of Plant Life On Earth
  32. ^ 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.
  33. ^ Smith, David (1 January 2013). "Steal My Sunshine". The Scientist Magazine®. Retrieved 18 August 2022.
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