What is another cell organelle that is thought to have originated through endosymbiosis

Understanding:

•  The origin of eukaryotic cells can be explained by the endosymbiotic theory

    
An endosymbiont is a cell which lives inside another cell with mutual benefit

Eukaryotic cells are believed to have evolved from early prokaryotes that were engulfed by phagocytosis

The engulfed prokaryotic cell remained undigested as it contributed new functionality to the engulfing cell (e.g. photosynthesis)

Over generations, the engulfed cell lost some of its independent utility and became a supplemental organelle

Overview of the Process of Endosymbiosis

Evidence for Endosymbiosis

Mitochondria and chloroplasts are both organelles suggested to have arisen via endosymbiosis

Evidence that supports the extracellular origins of these organelles can be seen by looking at certain key features:

• Membranes (double membrane bound)
• Antibiotics (susceptibility)
• Division (mode of replication)
• DNA (presence and structural composition)
• Ribosomes (size)

Mnmemonic:  MAD DR  (mad doctor)

Chloroplast and Mitochondrial Evidence

1. Oborník M. In the beginning was the word: How terminology drives our understanding of endosymbiotic organelles. Microbial Cell. 2019 in press. [Google Scholar]

2. Archibald John M. Endosymbiosis and Eukaryotic Cell Evolution. Curr Biol. 2015;25(19):R911–R921. doi: 10.1016/j.cub.2015.07.055. [PubMed] [CrossRef] [Google Scholar]

3. Sapp J. Oxford University Press; New York: 1994. Evolution by Association: A History of Symbiosis. [Google Scholar]

4. Martin WF, Garg S, Zimorski V. Endosymbiotic theories for eukaryote origin. Philos Trans R Soc Lond B Biol Sci. 2015;370(1678):20140330. doi: 10.1098/rstb.2014.0330. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

5. Ernster L, Schatz G. Mitochondria: a historical review. J Cell Biol. 1981;91(3):227s–255s. doi: 10.1083/jcb.91.3.227s. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

6. Archibald J. Oxford University Press; Oxford: 2014. One Plus One Equals One: Symbiosis and the Evolution of Complex Life. [Google Scholar]

7. Sagan L. On the origin of mitosing cells. J Theor Biol. 1967;14(3):225–274. doi: 10.1016/0022-5193(67)90079-3. [PubMed] [CrossRef] [Google Scholar]

8. Dyall SD, Brown MT, Johnson PJ. Ancient Invasions: From Endosymbionts to Organelles. Science. 2004;304(5668):253–257. doi: 10.1126/science.1094884. [PubMed] [CrossRef] [Google Scholar]

9. Roger AJ, Muñoz-Gómez SA, Kamikawa R. The Origin and Diversification of Mitochondria. Curr Biol. 2017;27(21):R1177–R1192. doi: 10.1016/j.cub.2017.09.015. [PubMed] [CrossRef] [Google Scholar]

10. Kleinig H, Maier U. Gustav Fischer Verlag, Stuttgart Jena Lübeck Ulm; 1999. Zellbiologie: Begründet von Hans Kleinig und Peter Sitte. [Google Scholar]

11. Keeling PJ, McCutcheon JP, Doolittle WF. Symbiosis becoming permanent: Survival of the luckiest. Proc Natl Acad Sci U S A. 2015;112(33):10101–10103. doi: 10.1073/pnas.1513346112. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

12. Gavelis GS, Gile GH. How did cyanobacteria first embark on the path to becoming plastids?: lessons from protist symbioses. FEMS Microbiol Lett. 2018;365(19):fny209. doi: 10.1093/femsle/fny209. [PubMed] [CrossRef] [Google Scholar]

13. Dorrell RG, Howe CJ. What makes a chloroplast? Reconstructing the establishment of photosynthetic symbioses. J Cell Sci. 2012;125(8):1865–1875. doi: 10.1242/jcs.102285. [PubMed] [CrossRef] [Google Scholar]

14. Reyes-Prieto M, Latorre A, Moya A. Scanty microbes, the ‘symbionelle’ concept. Environ Microbiol. 2014;16(2):335–338. doi: 10.1111/1462-2920.12220. [PubMed] [CrossRef] [Google Scholar]

15. Nakabachi A, Ishida K, Hongoh Y, Ohkuma M, Miyagishima S-y. Aphid gene of bacterial origin encodes a protein transported to an obligate endosymbiont. Curr Biol. 2014;24(14):R640–R641. doi: 10.1016/j.cub.2014.06.038. [PubMed] [CrossRef] [Google Scholar]

16. Husnik F, McCutcheon JP. Functional horizontal gene transfer from bacteria to eukaryotes. Nat Rev Microbiol. 2017;16:67–79. doi: 10.1038/nrmicro.2017.137. [PubMed] [CrossRef] [Google Scholar]

17. Moran NA, McCutcheon JP, Nakabachi A. Genomics and Evolution of Heritable Bacterial Symbionts. Annu Rev Genet. 2008;42(1):165–190. doi: 10.1146/annurev.genet.41.110306.130119. [PubMed] [CrossRef] [Google Scholar]

18. Nowack ECM, Weber APM. Genomics-Informed Insights into Endosymbiotic Organelle Evolution in Photosynthetic Eukaryotes. Annu Rev Plant Biol. 2018;69(1):51–84. doi: 10.1146/annurev-arplant-042817-040209. [PubMed] [CrossRef] [Google Scholar]

19. Prechtl J, Kneip C, Lockhart P, Wenderoth K, Maier U-G. Intracellular Spheroid Bodies of Rhopalodia gibba Have Nitrogen-Fixing Apparatus of Cyanobacterial Origin. Mol Biol Evol. 2004;21(8):1477–1481. doi: 10.1093/molbev/msh086. [PubMed] [CrossRef] [Google Scholar]

20. Nakayama T, Ishida K-i. Another acquisition of a primary photosynthetic organelle is underway in Paulinella chromatophora. Curr Biol. 2009;19(7):R284–R285. doi: 10.1016/j.cub.2009.02.043. [PubMed] [CrossRef] [Google Scholar]

21. Nowack ECM. Paulinella chromatophora – rethinking the transition from endosymbiont to organelle. Acta Societatis Botanicorum Poloniae. 2014;83(4):387–397. doi: 10.5586/asbp.2014.049. [CrossRef] [Google Scholar]

22. Nowack ECM, Grossman AR. Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora. Proc Natl Acad Sci U S A. 2012;109(14):5340–5345. doi: 10.1073/pnas.1118800109. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

23. Baker AC. Flexibility and Specificity in Coral-Algal Symbiosis: Diversity, Ecology, and Biogeography of Symbiodinium. Annual Review of Ecology, Evolution, and Systematics. 2003;34(1):661–689. doi: 10.1146/annurev.ecolsys.34.011802.132417. [CrossRef] [Google Scholar]

24. Dorrell RG, Howe CJ. Integration of plastids with their hosts: Lessons learned from dinoflagellates. Proc Natl Acad Sci U S A. 2015;112(33):10247–10254. doi: 10.1073/pnas.1421380112. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

25. Hehenberger E, Imanian B, Burki F, Keeling PJ. Evidence for the Retention of Two Evolutionary Distinct Plastids in Dinoflagellates with Diatom Endosymbionts. Genome Biol Evol. 2014;6(9):2321–2334. doi: 10.1093/gbe/evu182. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

26. Marin B, M., Nowack EC, Melkonian M. A Plastid in the Making: Evidence for a Second Primary Endosymbiosis. Protist. 2005;156(4):425–432. doi: 10.1016/j.protis.2005.09.001. [PubMed] [CrossRef] [Google Scholar]

27. Rodríguez-Ezpeleta N, Philippe H. Plastid Origin: Replaying the Tape. Curr Biol. 2006;16(2):R53–R56. doi: 10.1016/j.cub.2006.01.006. [PubMed] [CrossRef] [Google Scholar]

28. Archibald JM. Endosymbiosis: Double-Take on Plastid Origins. Curr Biol. 2006;16(17):R690–R692. doi: 10.1016/j.cub.2006.08.006. [PubMed] [CrossRef] [Google Scholar]

29. Theissen U, Martin W. The difference between organelles and endosymbionts. Curr Biol. 2006;16(24):R1016–R1017. doi: 10.1016/j.cub.2006.11.020. [PubMed] [CrossRef] [Google Scholar]

30. Bhattacharya D, Archibald JM. Response to Theissen and Martin. Curr Biol. 2006;16(24):R1017–R1018. doi: 10.1016/j.cub.2006.11.021. [CrossRef] [Google Scholar]

31. Cavalier-Smith T, Lee JJ. Protozoa as Hosts for Endosymbioses and the Conversion of Symbionts into Organelles. J Protozoology. 1985;32(3):376–379. doi: 10.1111/j.1550-7408.1985.tb04031.x. [CrossRef] [Google Scholar]

32. Sitte P. Phylogenetische Aspekte der Zellevolution. Biologische Rundschau. 1990;28(1):1–18. [Google Scholar]

33. Sitte P. “Intertaxonic combination”: introducing and defining a new term in symbiogenesis.. In: Sato S, Ishida M, Ishikawa H, editors. Proceedings of the Fifth International Colloquium on Endocytobiology and Symbiosis; Kyoto. June 23-27, 1992; Tübingen: Tübingen University Press; 1993. pp. 557–558. [Google Scholar]

34. Sitte P. Symbiogenetic Evolution of Complex Cells and Complex Plastids. Eur J Protistol. 1993;29(2):131–143. doi: 10.1016/s0932-4739(11)80266-x. [PubMed] [CrossRef] [Google Scholar]

35. Nowack ECM, Melkonian M, Glöckner G. Chromatophore Genome Sequence of Paulinella Sheds Light on Acquisition of Photosynthesis by Eukaryotes. Curr Biol. 2008;18(6):410–418. doi: 10.1016/j.cub.2008.02.051. [PubMed] [CrossRef] [Google Scholar]

36. Keeling PJ, Archibald JM. Organelle Evolution: What's in a Name? Curr Biol. 2008;18(8):R345–R347. doi: 10.1016/j.cub.2008.02.065. [PubMed] [CrossRef] [Google Scholar]

37. McCutcheon John P, Keeling Patrick J. Endosymbiosis: Protein Targeting Further Erodes the Organelle/Symbiont Distinction. Curr Biol. 2014;24(14):R654–R655. doi: 10.1016/j.cub.2014.05.073. [PubMed] [CrossRef] [Google Scholar]

38. Allen JF. The function of genomes in bioenergetic organelles. Philos Trans R Soc Lond B Biol Sci. 2003;358(1429):19–38. doi: 10.1098/rstb.2002.1191. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

39. Rice DW, Alverson AJ, Richardson AO, Young GJ, Sanchez-Puerta MV, Munzinger J, Barry K, Boore JL, Zhang Y, dePamphilis CW, Knox EB, Palmer JD. Horizontal Transfer of Entire Genomes via Mitochondrial Fusion in the Angiosperm Amborella. Science. 2013;342(6165):1468–1473. doi: 10.1126/science.1246275. [PubMed] [CrossRef] [Google Scholar]

40. Hao W, Richardson AO, Zheng Y, Palmer JD. Gorgeous mosaic of mitochondrial genes created by horizontal transfer and gene conversion. Proc Natl Acad Sci U S A. 2010;107(50):21576–21581. doi: 10.1073/pnas.1016295107. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

41. Martin WF. Too Much Eukaryote LGT. Bioessays. 2017;39(12):1700115. doi: 10.1002/bies.201700115. [PubMed] [CrossRef] [Google Scholar]

42. Leger MM, Eme L, Stairs CW, Roger AJ. Demystifying Eukaryote Lateral Gene Transfer (Response to Martin 2017 DOI: 10.1002/bies.201700115). BioEssays. 2018;40(5):1700242. doi: 10.1002/bies.201700242. [PubMed] [CrossRef] [Google Scholar]

43. Boto L. Are There Really Too Many Eukaryote LGTs? A Reply To William Martin. BioEssays. 2018;40(3):1800001. doi: 10.1002/bies.201800001. [PubMed] [CrossRef] [Google Scholar]

44. Tonk L, Sampayo EM, Weeks S, Magno-Canto M, Hoegh-Guldberg O. Host-Specific Interactions with Environmental Factors Shape the Distribution of Symbiodinium across the Great Barrier Reef. PLoS One. 2013;8(7):e68533. doi: 10.1371/journal.pone.0068533. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

45. O'Malley MA. From endosymbiosis to holobionts: Evaluating a conceptual legacy. J Theor Biol. 2017;434:34–41. doi: 10.1016/j.jtbi.2017.03.008. [PubMed] [CrossRef] [Google Scholar]

46. Weis VM, Reynolds WS, deBoer MD, Krupp DA. Host-symbiont specificity during onset of symbiosis between the dinoflagellates Symbiodinium spp. and planula larvae of the scleractinian coral Fungia scutaria. Coral Reefs. 2001;20(3):301–308. doi: 10.1007/s003380100179. [CrossRef] [Google Scholar]

47. Coffroth MA, Lewis CF, Santos SR, Weaver JL. Environmental populations of symbiotic dinoflagellates in the genus Symbiodinium can initiate symbioses with reef cnidarians. Curr Biol. 2006;16(23):R985–R987. doi: 10.1016/j.cub.2006.10.049. [PubMed] [CrossRef] [Google Scholar]

48. Aranda M, Li Y, Liew YJ, Baumgarten S, Simakov O, Wilson MC, Piel J, Ashoor H, Bougouffa S, Bajic VB, Ryu T, Ravasi T, Bayer T, Micklem G, Kim H, Bhak J, LaJeunesse TC, Voolstra CR. Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. Sci Rep. 2016;6:39734. doi: 10.1038/srep39734. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

49. Lin S, Cheng S, Song B, Zhong X, Lin X, Li W, Li L, Zhang Y, Zhang H, Ji Z, Cai M, Zhuang Y, Shi X, Lin L, Wang L, Wang Z, Liu X, Yu S, Zeng P, Hao H, Zou Q, Chen C, Li Y, Wang Y, Xu C, Meng S, Xu X, Wang J, Yang H, Campbell DA, et al. The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science. 2015;350(6261):691–694. doi: 10.1126/science.aad0408. [PubMed] [CrossRef] [Google Scholar]

50. Voolstra CR, Li Y, Liew YJ, Baumgarten S, Zoccola D, Flot J-F, Tambutté S, Allemand D, Aranda M. Comparative analysis of the genomes of Stylophora pistillata and Acropora digitifera provides evidence for extensive differences between species of corals. Sci Rep. 2017;7(1):17583. doi: 10.1038/s41598-017-17484-x. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

51. Ziegler M, Arif C, Burt JA, Dobretsov S, Roder C, LaJeunesse TC, Voolstra CR. Biogeography and molecular diversity of coral symbionts in the genus Symbiodinium around the Arabian Peninsula. J Biogeogr. 2017;44(3):674–686. doi: 10.1111/jbi.12913. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

52. Karnkowska A, Vacek V, Zubáčová Z, Treitli SC, Petrželková R, Eme L, Novák L, Žárský V, Barlow LD, Herman EK, Soukal P, Hroudová M, Doležal P, Stairs CW, Roger AJ, Eliáš M, Dacks JB, Vlček Č, Hampl V. A Eukaryote without a Mitochondrial Organelle. Curr Biol. 2016;26(10):1274–1284. doi: 10.1016/j.cub.2016.03.053. [PubMed] [CrossRef] [Google Scholar]

53. Greiner S, Sobanski J, Bock R. Why are most organelle genomes transmitted maternally? BioEssays. 2015;37(1):80–94. doi: 10.1002/bies.201400110. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

54. Hill GE. The mitonuclear compatibility species concept. The Auk. 2017;134(2):393–409. doi: 10.1642/auk-16-201.1. [CrossRef] [Google Scholar]

55. Sloan DB, Havird JC, Sharbrough J. The on-again, off-again relationship between mitochondrial genomes and species boundaries. Mol Ecol. 2017;26(8):2212–2236. doi: 10.1111/mec.13959. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

56. Barreto FS, Watson ET, Lima TG, Willett CS, Edmands S, Li W, Burton RS. Genomic signatures of mitonuclear coevolution across populations of Tigriopus californicus. Nat Ecol Evol. 2018;2(8):1250–1257. doi: 10.1038/s41559-018-0588-1. [PubMed] [CrossRef] [Google Scholar]

57. Mastrantonio V, Porretta D, Urbanelli S, Crasta G, Nascetti G. Dynamics of mtDNA introgression during species range expansion: insights from an experimental longitudinal study. Sci Rep. 2016;6:30355. doi: 10.1038/srep30355. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

58. Stegemann S, Keuthe M, Greiner S, Bock R. Horizontal transfer of chloroplast genomes between plant species. Proc Natl Acad Sci U S A. 2012;109(7):2434–2438. doi: 10.1073/pnas.1114076109. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

59. Stegemann S, Bock R. Exchange of Genetic Material Between Cells in Plant Tissue Grafts. Science. 2009;324(5927):649–651. doi: 10.1126/science.1170397. [PubMed] [CrossRef] [Google Scholar]

60. Lauterborn R. Protozoenstudien II. Paulinella chromatophora nov. gen., nov. spec., ein beschalter Rhizopode des Süßwassers mit blaugrünen chromatophorenartigen Einschlüssen. Z Wiss Zool. 1895;59:537–544. [Google Scholar]

61. Mann C. Lynn Margulis: Science's Unruly Earth Mother. Science. 1991;252(5004):378–381. doi: 10.1126/science.252.5004.378. [PubMed] [CrossRef] [Google Scholar]

62. Doolittle WF. Darwinizing Gaia. J Theor Biol. 2017;434:11–19. doi: 10.1016/j.jtbi.2017.02.015. [PubMed] [CrossRef] [Google Scholar]

63. Matsuoka Y. Evolution of Polyploid Triticum Wheats under Cultivation: The Role of Domestication, Natural Hybridization and Allopolyploid Speciation in their Diversification. Plant Cell Physiol. 2011;52(5):750–764. doi: 10.1093/pcp/pcr018. [PubMed] [CrossRef] [Google Scholar]

64. Fields KA, Heinzen RA, Carabeo R. The Obligate Intracellular Lifestyle. Front Microbiol. 2011;2:99. doi: 10.3389/fmicb.2011.00099. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

65. Young VB. The role of the microbiome in human health and disease: an introduction for clinicians. BMJ. 2017;356:j831. doi: 10.1136/bmj.j831. [PubMed] [CrossRef] [Google Scholar]

66. Rodríguez JM, Murphy K, Stanton C, Ross RP, Kober OI, Juge N, Avershina E, Rudi K, Narbad A, Jenmalm MC, Marchesi JR, Collado MC. The composition of the gut microbiota throughout life, with an emphasis on early life. Microb Ecol Health Dis. 2015;26:26050. doi: 10.3402/mehd.v26.26050. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

67. Gupta S, Allen-Vercoe E, Petrof EO. Fecal microbiota transplantation: in perspective. Therap Adv Gastroenterol. 2016;9(2):229–239. doi: 10.1177/1756283X15607414. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

68. DeBruyn JM, Hauther KA. Postmortem succession of gut microbial communities in deceased human subjects. PeerJ. 2017;5:e3437. doi: 10.7717/peerj.3437. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

69. Schenk HEA. Some thoughts towards a discussion of terms and definitions in endocytobiology.. In: Sato S, Ishida M, Ishikawa H, editors. Proceedings of the Fifth International Colloquium on Endocytobiology and Symbiosis; Kyoto. June 23-27, 1992; Tübingen: Tübingen University Press; 1993. pp. 547–556. [Google Scholar]

70. Schenk HEA. Is endocytobiology an independent science? Endocytobiosis and Cell Research. 1993;10:229–240. [Google Scholar]

Page 2

Criteria for and consequences of sexual symbiont integration.