Skip to main content

Rhopalodia gibba: The First Steps in the Birth of a Novel Organelle?

  • Chapter
  • First Online:
Endosymbiosis

Abstract

The diatom Rhopalodia gibba harbours unusual cell inclusions termed spheroid bodies. Those are separated from the host cytoplasm by an additional membrane, vertically transmitted to the next generation and provide nitrogen autonomy to their host cell. Morphological observations and phylogenetic analyses revealed a cyanobacterial origin of these obligate endosymbionts. Phylogenetic data and fossil records suggest that the origin of this endosymbiosis dates back to late Eocene to Miocene (~25 Ma). Genomic analyses support this determination, as the genomic changes in the spheroid body suggest that the endosymbiosis is in a relatively early stage.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adler S, Dersch LM, Maier U-G (2010) Cultivation of the diatom Rhopalodia gibba. J Endocytobiosis Cell Res 20:109–112

    Article  Google Scholar 

  • Bentley SD, Parkhill J (2004) Comparative genomic structure of prokaryotes. Annu Rev Genet 38:771–791

    Article  PubMed  CAS  Google Scholar 

  • Bergman B, Gallon J, Rai A, Stal L (1997) N2 Fixation by non-heterocystous cyanobacteria1. FEMS Microbiol Rev 19:139–185

    Article  CAS  Google Scholar 

  • Bodył A, Mackiewicz P, Stiller JW (2010) Comparative genomic studies suggest that the cyanobacterial endosymbionts of the amoeba Paulinella chromatophora possess an import apparatus for nuclear-encoded proteins. Plant Biol 12:639–649

    PubMed  Google Scholar 

  • Bolte K, Bullmann L, Hempel F, Bozarth A, Zauner S, Maier U-G (2009) Protein targeting into secondary plastids. J Eukaryot Microbiol 56:9–15

    Article  PubMed  CAS  Google Scholar 

  • Bothe H, Schmitz O, Yates MG, Newton WE (2010a) Nitrogen fixation and hydrogen metabolism in cyanobacteria. Microbiol Mol Biol Rev 74:529–551

    Article  PubMed  CAS  Google Scholar 

  • Bothe H, Tripp HJ, Zehr JP (2010b) Unicellular cyanobacteria with a new mode of life: the lack of photosynthetic oxygen evolution allows nitrogen fixation to proceed. Arch Microbiol 192:783–790

    Article  PubMed  CAS  Google Scholar 

  • Capone DG, Burns JA, Montoya JP, Subramaniam A, Mahaffey C, Gunderson T, Michaels AF, Carpenter EJ (2005) Nitrogen fixation by Trichodesmium spp.: an important source of new nitrogen to the tropical and subtropical North Atlantic Ocean. Global Biogeochem Cy 19:GB2024

    Article  Google Scholar 

  • Carpenter EJ, Janson S (2000) Intracellular cyanobacterial symbionts in the marine diatom Climacodium frauenfeldianum (Bacillariophyceae). J Phycol 36:540–544

    Article  Google Scholar 

  • Cavalier-Smith T, Lee JJ (1985) Protozoa as hosts for endosymbioses and the conversion of symbionts into organelles. J Protozool 32:376–379

    Article  Google Scholar 

  • Cole S, Eiglmeier K, Parkhill J, James K, Thomson N, Wheeler P et al (2001) Massive gene decay in the leprosy bacillus. Nature 409:1007–1011

    Article  PubMed  CAS  Google Scholar 

  • Dagan T, Blekhman R, Graur D (2006) The “domino theory” of gene death: gradual and mass gene extinction events in three lineages of obligate symbiotic bacterial pathogens. Mol Biol Evol 23:310–316

    Article  PubMed  CAS  Google Scholar 

  • DeYoe HR, Lowe RL, Marks JC (1992) Effects of nitrogen and phosphorus on the endosymbiont load of Rhopalodia gibba and Epithemia turgida (Bacillariophyceae). J Phycol 28:773–777

    Article  CAS  Google Scholar 

  • Drum RW, Pankratz S (1965) Fine structure of an unusual cytoplasmic inclusion in the diatom genus, Rhopalodia. Protoplasma 60:141–149

    Article  Google Scholar 

  • Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, Taylor FJR (2004) The evolution of modern eukaryotic phytoplankton. Science 305:354–360

    Article  PubMed  CAS  Google Scholar 

  • Fiore CL, Jarett JK, Olson ND, Lesser MP (2010) Nitrogen fixation and nitrogen transformations in marine symbioses. Trends Microbiol 18:455–463

    Article  PubMed  CAS  Google Scholar 

  • Floener L (1982) Physiologische und biochemische Untersuchungen an dem Cyanellen enthaltenden Flagellat Cyanophora paradoxa und an Rhopalodia gibba, einer Diatomee mit blau-grünen Einschlüssen. Thesis, University of Cologne

    Google Scholar 

  • Floener L, Bothe H (1980) Nitrogen fixation in Rhopalodia gibba, a diatom containing bluegreenish inclusions symbiotically. In: Schwemmler W, Schenk H (eds) Endocytobiology: endosymbiosis and cell biology, a synthesis of recent research, 1st edn. Walter de Gruyter and Co., Berlin, pp 541–552

    Google Scholar 

  • Geitler L (1977) Zur Entwicklungsgeschichte der Epithemiaceen: Epithemia, Rhopalodia und Denticula (Diatomophyceae) und ihre vermutlich symbiotischen Sphäroidkörper. Plant Syst Evol 128:259–275

    Article  Google Scholar 

  • Goebel NL, Edwards CA, Church MJ, Zehr JP (2007) Modeled contributions of three types of diazotrophs to nitrogen fixation at Station ALOHA. ISME J 1:606–619

    Article  PubMed  CAS  Google Scholar 

  • Hajos M (1973) The Mediterranean diatoms. Initial Rep Deep Sea 13:944–969

    Google Scholar 

  • Hempel F, Bozarth A, Sommer MS, Zauner S, Przyborski JM, Maier U-G (2007) Transport of nuclear-encoded proteins into secondarily evolved plastids. Biol Chem 388:899–906

    Article  PubMed  CAS  Google Scholar 

  • Hoek CVD, Jahns HM, Mann DG (1993) Algen, 3rd edn. George Thieme Verlag, Stuttgart

    Google Scholar 

  • Keeling PJ, Archibald JM (2008) Organelle evolution: what’s in a name? Curr Biol 18:R345–R347

    Article  PubMed  CAS  Google Scholar 

  • Kies L (1992) Glaucocystophyceae and other protists harbouring prokaryotic endocytobionts. In: Reiser W (ed) Algae and symbioses. Biopress Limited, Bristol, pp 353–377

    Google Scholar 

  • Klebahn H (1896) Beiträge zur Kenntnis der Auxosporenbildung. I. Rhopalodia gibba. Jahrbücher der wissenschaftlichen Botanik 29:595–654

    Google Scholar 

  • Kneip C, Lockhart P, Voss C, Maier U-G (2007) Nitrogen fixation in eukaryotes – new models for symbiosis. BMC Evol Biol 7:55

    Article  PubMed  Google Scholar 

  • Kneip C, Voss C, Lockhart PJ, Maier U-G (2008) The cyanobacterial endosymbiont of the unicellular algae Rhopalodia gibba shows reductive genome evolution. BMC Evol Biol 8:30

    Article  PubMed  Google Scholar 

  • Lauterborn R (1895) Protozoenstudien. II. Paulinella chromatophora nov. gen. spec., ein beschalter Rhizopode des Süßwassers mit blaugrünen chromatophorenartigen Einschlüssen. Z Wiss Zool 59:537–544

    Google Scholar 

  • Marin B, Nowack EC, Melkonian M (2005) A plastid in the making: evidence for a second primary endosymbiosis. Protist 156:425–432

    Article  PubMed  CAS  Google Scholar 

  • Moran NA, Mira A (2001) The process of genome shrinkage in the obligate symbiont Buchnera aphidicola. Genome Biol 2:research0054.1–research0054.12

    Article  Google Scholar 

  • Moran NA, Plague GR (2004) Genomic changes following host restriction in bacteria. Curr Opin Genet Dev 14:627–633

    Article  PubMed  CAS  Google Scholar 

  • Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190

    Article  PubMed  CAS  Google Scholar 

  • Moustafa A, Beszteri B, Maier U-G, Bowler C, Valentin K, Bhattacharya D (2009) Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324:1724–1726

    Article  PubMed  CAS  Google Scholar 

  • Nakabachi A, Yamashita A, Toh H, Ishikawa H, Dunbar HE, Moran NA, Hattori M (2006) The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314:267

    Article  PubMed  CAS  Google Scholar 

  • Nakayama T, Ishida K-I (2009) Another acquisition of a primary photosynthetic organelle is underway in Paulinella chromatophora. Curr Biol 19:R284–R285

    Article  PubMed  CAS  Google Scholar 

  • Nakayama T, Ikegami Y, Nakayama T, Ishida K-I, Inagaki Y, Inouye I (2011) Spheroid bodies in Rhopalodiacean diatoms were derived from a single endosymbiotic cyanobacterium. J Plant Res 124:93–97

    Article  PubMed  Google Scholar 

  • Nowack EC, Melkonian M, Glöckner G (2008) Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol 18:410–418

    Article  PubMed  CAS  Google Scholar 

  • Nowack EC, Vogel H, Groth M, Grossman AR, Melkonian M, Glöckner G (2011) Endosymbiotic gene transfer and transcriptional regulation of transferred genes in Paulinella chromatophora. Mol Biol Evol 28:407–422

    Article  PubMed  CAS  Google Scholar 

  • Pfitzer E (1869) Über den Bau und die Zellteilung der Diatomeen. Botanische Zeitung 27:774–776

    Google Scholar 

  • Prechtl J, Kneip C, Lockhart PJ, Wenderoth K, Maier U-G (2004) Intracellular spheroid bodies of Rhopalodia gibba have nitrogen-fixing apparatus of cyanobacterial origin. Mol Biol Evol 21:1477–1481

    Article  PubMed  CAS  Google Scholar 

  • Reyes-Prieto A, Yoon HS, Moustafa A, Yang EC, Andersen RA, Boo SM, Nakayama T, Ishida K-I, Bhattacharya D (2010) Differential gene retention in plastids of common recent origin. Mol Biol Evol 27:1530–1537

    Article  PubMed  CAS  Google Scholar 

  • Round FE, Crawford RM, Mann DG (1990) The diatoms – biology and morphology of the genera. Cambridge University Press, Cambridge, p 125

    Google Scholar 

  • Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407:81–86

    Article  PubMed  CAS  Google Scholar 

  • Silva FJ, Latorre A, Moya A (2001) Genome size reduction through multiple events of gene disintegration in Buchnera APS. Trends Genet 17:615–618

    Article  PubMed  CAS  Google Scholar 

  • Simonsen R (1979) The diatom system: ideas on phylogeny. Bacillaria 2:9–71

    Google Scholar 

  • Tamas I, Klasson L, Canbäck B, Näslund AK, Eriksson A-S, Wernegreen JJ, Sandström JP, Moran NA, Andersson SGE (2002) 50 million years of genomic stasis in endosymbiotic bacteria. Science 296:2376–2379

    Article  PubMed  CAS  Google Scholar 

  • Theissen U, Martin W (2006) The difference between organelles and endosymbionts. Curr Biol 16:R1016–R1017

    Article  PubMed  CAS  Google Scholar 

  • Toh H, Weiss BL, Perkin SA, Yamashita A, Oshima K, Hattori M, Aksoy S (2006) Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Genome Res 16:149–156

    Article  PubMed  CAS  Google Scholar 

  • Tripp HJ, Bench SR, Turk KA, Foster RA, Desany BA, Niazi F, Affourtit JP, Zehr JP (2010) Metabolic streamlining in an open-ocean nitrogen-fixing cyanobacterium. Nature 464:90–94

    Article  PubMed  CAS  Google Scholar 

  • Ward BB, Capone DG, Zehr JP (2007) What’s new in the nitrogen cycle ? Oceanography 20:101–109

    Article  Google Scholar 

  • Welsh EA, Liberton M, Stöckel J, Loh T, Elvitigala T, Wang C et al (2008) The genome of Cyanothece 51142, a unicellular diazotrophic cyanobacterium important in the marine nitrogen cycle. PNAS 105:15094–15099

    Article  PubMed  Google Scholar 

  • Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R, Brownlie JC et al (2004) Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol 2:0327–0341

    Article  CAS  Google Scholar 

  • Yoon HS, Nakayama T, Reyes-Prieto A, Andersen RA, Boo SM, Ishida K-I, Bhattacharya D (2009) A single origin of the photosynthetic organelle in different Paulinella lineages. BMC Evol Biol 9:98

    Article  PubMed  Google Scholar 

  • Yoon HS, Yang EC, Qiu H, Bhattacharya D (2013) Photosynthetic Paulinella–recapitulation of primary plastid establishment. In: Löffelhardt W (ed) Endosymbiosis. Springer, Vienna

    Google Scholar 

  • Zehr JP (2011) Nitrogen fixation by marine cyanobacteria. Trends Microbiol 19:162–173

    Article  PubMed  CAS  Google Scholar 

  • Zehr JP, Bench SR, Carter BJ, Hewson I, Niazi F, Shi T, Tripp HJ, Affourtit JP (2008) Globally distributed uncultivated oceanic N2-fixing cyanobacteria lack oxygenic photosystem II. Science 322:1110–1112

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants of the Deutsche Forschungsgemeinschaft (DFG SFB TR1). We would like to thank Helen Rennie for critical notes on the manuscript and Magnus Rath for microscopic support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stefan Zauner .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Wien

About this chapter

Cite this chapter

Adler, S., Trapp, E.M., Dede, C., Maier, U.G., Zauner, S. (2014). Rhopalodia gibba: The First Steps in the Birth of a Novel Organelle?. In: Löffelhardt, W. (eds) Endosymbiosis. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1303-5_9

Download citation

Publish with us

Policies and ethics