Complete genome of a nonphotosynthetic cyanobacterium in a diatom reveals recent adaptations to an intracellular lifestyle

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 31, 2014, Pages 11407-11412

  Nakayama, Takuro ^a,b,c   Kamikawa, Ryoma ^a,d   Tanifuji, Goro ^a,b   Kashiyama, Yuichiro ^e,f,g   Ohkouchi, Naohiko ^e   Archibald, John M ^b   Inagaki, Yuji ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b DALHOUSIE UNIVERSITY   (Canada)

^c NATIONAL INSTITUTE FOR ENVIRONMENTAL STUDIES   (Japan)

^d KYOTO UNIVERSITY   (Japan)

^e JAPAN AGENCY FOR MARINE EARTH SCIENCE AND TECHNOLOGY   (Japan)

^f FUKUI UNIVERSITY OF TECHNOLOGY   (Japan)

^g JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Organelle evolution; Photosynthesis; Pseudogenization

Indexed keywords

RIBOSOME PROTEIN;

ADAPTATION; AMINO ACID METABOLISM; ARTICLE; AUTOFLUORESCENCE; BACTERIAL GENOME; BIOSYNTHESIS; CARBOHYDRATE METABOLISM; CITRIC ACID CYCLE; DIATOM; ENDOSYMBIONT; ENERGY METABOLISM; EPITHEMIA TURGIDA; EUKARYOTIC CELL; GENE AMPLIFICATION; GENE CLUSTER; GENOME SIZE; HAPTOPHYTA; HOST CELL; LIFESTYLE; MEMBRANE TRANSPORT; METABOLIC CAPACITY; NITROGEN FIXATION; NONHUMAN; NUCLEOTIDE METABOLISM; OPERON; PENTOSE PHOSPHATE CYCLE; PHOTOSYSTEM I; PHOTOSYSTEM II; PHOTOTROPHIC BACTERIUM; PHYCOBILISOME; PHYLOGENY; PRIORITY JOURNAL; PSEUDOGENE; RESPIRATORY CHAIN; SIGNAL TRANSDUCTION; STOP CODON; SYMBIONT; THYLAKOID MEMBRANE;

ORGANELLE EVOLUTION; PHOTOSYNTHESIS; PSEUDOGENIZATION;

ADAPTATION, PHYSIOLOGICAL; CHROMOSOMES, BACTERIAL; CYANOBACTERIA; DIATOMS; ELECTRON TRANSPORT; GENOME SIZE; GENOME, BACTERIAL; INTRACELLULAR SPACE; MOLECULAR SEQUENCE DATA; NITROGEN FIXATION; ORGANELLES; PHOTOSYNTHESIS; SYMBIOSIS; THYLAKOIDS;

EID: 84905659677     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1405222111     Document Type: Article

References (44)

1. Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science 283(5407):1476-1481.
2. Dyall SD, Brown MT, Johnson PJ (2004) Ancient invasions: From endosymbionts to organelles. Science 304(5668):253-257. (Pubitemid 38452171)
3. Gould SB, Waller RF, McFadden GI (2008) Plastid evolution. Annu Rev Plant Biol 59:491-517. (Pubitemid 351813040)
4. Archibald JM (2009) The puzzle of plastid evolution. Curr Biol 19(2):R81-R88.
5. Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 21(5):809-818. (Pubitemid 38529723)
6. Parfrey LW, Lahr DJG, Knoll AH, Katz LA (2011) Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci USA 108(33):13624-13629.
7. Drum RW, Pankratz S (1965) Fine structure of an unusual cytoplasmic inclusion in the diatom genus, Rhopalodia. Protoplasma 60:141-149.
8. Prechtl J, Kneip C, Lockhart P, Wenderoth K, Maier U-G (2004) Intracellular spheroid bodies of Rhopalodia gibba have nitrogen-fixing apparatus of cyanobacterial origin. Mol Biol Evol 21(8):1477-1481. (Pubitemid 38971758)
9. Nakayama T, et al. (2011) Spheroid bodies in rhopalodiacean diatoms were derived from a single endosymbiotic cyanobacterium. J Plant Res 124(1):93-97.
10. Geitler L (1977) Zur Entwicklungsgeschichte der Epithemiaceen Epithemia, Rhopalodia und Denticula (Diatomophyceae) und ihre vermutlich symbiotischen Sphäroidkörper. Plant Syst Evol 128:259-275.
11. Floener L, Bothe H (1980) Nitrogen fixation in Rhopalodia gibba, a diatom containing blue?greenish inclusions symbiotically. Endocytobiology: Endosymbiosis and Cell Biology, a Synthesis of Recent Research, eds Schwemmler W, Schenk H (Walter de Gruyter, Berlin), 1st Ed, pp 541-552.
12. 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.
13. Kies L (1992) Glaucocystophyceae and other Protists Harbouring Prokaryotic Endocytobionts. Algae and Symbioses, ed Reisser W (Biopress, Bristol, UK), pp 353-377.
14. Marin B, Nowack ECM, Melkonian M (2005) A plastid in the making: Evidence for a second primary endosymbiosis. Protist 156(4):425-432. (Pubitemid 41682020)
15. Nowack EC, Melkonian M, Glöckner G (2008) Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol 18(6):410-418.
16. Nakayama T, Archibald JM (2012) Evolving a photosynthetic organelle. BMC Biol 10:35.
17. Trapp EM, Adler S, Zauner S, Maier U-G (2012) Rhopalodia gibba and its endosymbionts as a model for early steps in a cyanobacterial primary endosymbiosis. J Endocytobiosis Cell Res 23:21-24.
18. Adler S, Trapp EM, Dede C, Maier U-G, Zauner S (2014) Rhopalodia gibba: The first steps in the birth of a novel organelle? Endosymbiosis, ed Löffelhardt W (Springer, Vienna), pp 167-179.
19. Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18(5):821-829. (Pubitemid 351645072)
20. Bandyopadhyay A, et al. (2011) Novel metabolic attributes of the genus Cyanothece, comprising a group of unicellular nitrogen-fixing cyanobacteria. MBio 2(5):e00214-11.
21. Welsh EA, et al. (2008) The genome of Cyanothece 51142, a unicellular diazotrophic cyanobacterium important in the marine nitrogen cycle. Proc Natl Acad Sci USA 105(39):15094-15099.
22. Tripp HJ, et al. (2010) Metabolic streamlining in an open-ocean nitrogen-fixing cyanobacterium. Nature 464(7285):90-94.
23. Thompson AW, et al. (2012) Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science 337(6101):1546-1550.
24. Wernegreen JJ (2002) Genome evolution in bacterial endosymbionts of insects. Nat Rev Genet 3(11):850-861.
25. Kuwahara H, et al. (2007) Reduced genome of the thioautotrophic intracellular symbiont in a deep-sea clam, Calyptogena okutanii. Curr Biol 17(10):881-886. (Pubitemid 46702672)
26. Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165-190.
27. Ran L, et al. (2010) Genome erosion in a nitrogen-fixing vertically transmitted endosymbiotic multicellular cyanobacterium. PLoS ONE 5(7):e11486.
28. Hagino K, Onuma R, Kawachi M, Horiguchi T (2013) Discovery of an endosymbiotic nitrogen-fixing cyanobacterium UCYN-A in Braarudosphaera bigelowii (Prymnesiophyceae). PLoS ONE 8(12):e81749.
29. Hilton JA, et al. (2013) Genomic deletions disrupt nitrogen metabolism pathways of a cyanobacterial diatom symbiont. Nat Commun 4:1767.
30. Vermaas WFJ (2001) Photosynthesis and respiration in cyanobacteria. eLS (Wiley, Chichester, UK), www.els.net, 10.1038/npg.els.0001670.
31. Tamagnini P, et al. (2002) Hydrogenases and hydrogen metabolism of cyanobacteria. Microbiol Mol Biol Rev 66(1):1-20. (Pubitemid 34213966)
32. 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(6800):81-86.
33. Seefeldt LC, Hoffman BM, Dean DR (2009) Mechanism of Mo-dependent nitrogenase. Annu Rev Biochem 78:701-722.
34. Cavalier-Smith T, Lee JJ (1985) Protozoa as hosts for endosymbioses and the conversion of symbionts into organelles. J Protozool 32:376-379.
35. Theissen U, Martin W (2006) The difference between organelles and endosymbionts. Curr Biol 16(24):R1016-R1017. (Pubitemid 44894922)
36. Besemer J, Lomsadze A, Borodovsky M (2001) GeneMarkS: A self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res 29(12):2607-2618. (Pubitemid 32600318)
37. Schattner P, Brooks AN, Lowe TM (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33(Web server issue): W686-W689.
38. Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J (2009) DNAPlotter: Circular and linear interactive genome visualization. Bioinformatics 25(1):119-120.
39. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: An automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35(Web server issue):W182-W185.
40. Kawashima S, Katayama T, Sato Y, Kanehisa M (2003) KEGG API: A Web service using SOAP/WSDL to access the KEGG system. Genome Inform 14:673-674.
41. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M (2012) KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 40(database issue):D109-D114.
42. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792-1797.
43. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312-1313.
44. Tyler J, et al. (2010) Tracking aquatic change using chlorine-specific carbon and nitrogen isotopes: The last glacial-interglacial transition at Lake Suigetsu, Japan. Geochemistry Geophys Geosystems 11:Q09010.