Single cell genome analysis supports a link between phagotrophy and primary plastid endosymbiosis

Scientific Reports

Volumn 2, Issue , 2012, Pages

  Bhattacharya, Debashish ^a   Price, Dana C ^a   Yoon, Hwan Su ^b   Yang, Eun Chan ^c   Poulton, Nicole J ^c   Andersen, Robert A ^d   Das, Sushma Parankush ^a  

^a RUTGERS UNIVERSITY   (United States)

^b Sungkyunkwan University   (South Korea)

^c BIGELOW LABORATORY FOR OCEAN SCIENCES   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84859738464     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep00356     Document Type: Article

References (49)

1. Cavalier-Smith, T. & Lee, J. J. Protozoa as hosts for endosymbioses and the conversion of symbionts into organelles. J. Protozool. 32, 376-379 (1985).
2. Rodríguez-Ezpeleta, N. et al. Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr. Biol. 15, 1325-1330 (2005). (Pubitemid 41026601)
3. Adl, S. M. et al. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 52, 399-451(2005). (Pubitemid 43923926)
4. Chan, C. X. et al. Red-and-green algal monophyly and extensive gene sharing found in a rich repertoire of red algal genes. Curr. Biol. 21, 328-333 (2011).
5. Archibald, J. M. et al. Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. Proc. Natl. Acad. Sci. USA 100, 7678-7683 (2003). (Pubitemid 36760029)
6. Bhattacharya, D., Yoon, H. S. & Hackett, J. D. Photosynthetic eukaryotes unite: endosymbiosis connects the dots. BioEssays 26, 50-60 (2004). (Pubitemid 38095348)
7. Yoon, H. S. et al. A molecular timeline for the origin of photosynthetic eukaryotes. Mol. Biol. Evol. 21, 809-818 (2004). (Pubitemid 38529723)
8. Martin, W. et al. Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393, 162-165 (1998). (Pubitemid 28242254)
9. Reyes-Prieto, A. et al. Cyanobacterial contribution to algal nuclear genomes is primarily limited to plastid functions. Curr. Biol. 16, 2320-2325 (2006). (Pubitemid 44821835)
10. Bhattacharya, D., Helmchen, T. & Melkonian, M. Molecular evolutionary analyses of nuclear-encoded small subunit ribosomal RNA identify an independent rhizopod lineage containing the Euglyphidae and the Chlorarachniophyta. J. Euk. Microbiol. 42, 65-69 (1995).
11. Lauterborn, R. Protozoenstudien II. Paulinella chromatophora nov. gen., nov. spec., ein beschalter Rhizopode des Süsswassers mit blaugrünen chromatophorenartigen Einschlüssen. Z. Wiss. Zool. 59, 537-544 (1895).
12. Yoon, H. S. et al. Minimal plastid genome evolution in the Paulinella endosymbiont. Curr. Biol. 16, R670-R672 (2006). (Pubitemid 44691803)
13. Bodyl, A., Mackiewicz, P. & Stiller, J. W. The intracellular cyanobacteria of Paulinella chromatophora: endosymbionts or organelles? Trends Microbiol. 15, 295-296 (2007). (Pubitemid 47017710)
14. Yoon, H. S. et al. A single origin of the photosynthetic organelle in different Paulinella lineages. BMC Evol. Biol. 9, 98 (2009).
15. Nowack, E. C. M., Melkonian, M. & Glöckner, G. Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr. Biol. 18, 410-418 (2008).
16. Nowack, E. C. et al. Endosymbiotic gene transfer and transcriptional regulation of transferred genes in Paulinella chromatophora. Mol. Biol. Evol. 28, 407-422 (2011).
17. Marin, B. et al. The ancestor of the Paulinella chromatophore obtained a carboxysomal operon by horizontal gene transfer from a Nitrococcus-like cproteobacterium. BMC Evol. Biol. 7, 85 (2007).
18. Nakayama, T. & Ishida, K. Another acquisition of a primary photosynthetic organelle is underway in Paulinella chromatophora. Curr. Biol. 19, R284-285 (2009).
19. Reyes-Prieto, A. R. et al. Differential gene retention in plastids of common recent origin. Mol. Biol. Evol. 27, 1530-1537 (2010).
20. Johnson, P. W., Hargraves, P. E. & Sieburth, J. M. Ultrastructure and ecology of Calycomonas ovalis Wulff, 1919, (Chrysophyceae) and its redescription as a testate rhizopod, Paulinella ovalis N. Comb. (Filosea: Euglyphina).J. Eukaryot. Microbiol. 35, 618-626 (1988).
21. Vørs, N. 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. J. Eukaryot. Microbiol. 40, 272-287 (1993).
22. Hannah, F., Rogerson, A. & Anderson, O. R. A description of Paulinella indentata n. sp. (Filosea: Euglyphina) from subtidal coastal benthic sediments. J. Eukaryot. Microbiol. 43, 1-4 (1996).
23. Zinser, E. R. et al. Prochlorococcus ecotype abundances in the North Atlantic Ocean as revealed by an improved quantitative PCR method. Appl. Environ. Microbiol. 72, 723-732 (2006).
24. Tai, V. & Palenik, B. Temporal variation of Synechococcus clades at a coastal Pacific Ocean monitoring site. ISME J. 3, 903-915 (2009).
25. Zhang, K. et al. Sequencing genomes from single cells by polymerase cloning. Nat. Biotechnol. 24, 680-686 (2006). (Pubitemid 43882119)
26. Marcy, Y. et al. Dissecting biological "dark matter" with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth. Proc. Natl. Acad. Sci. USA 104, 11889-1194 (2007).
27. Stepanauskas, R. & Sieracki, M. E. Matching phylogeny and metabolism in the uncultured marine bacteria, one cell at a time. Proc. Natl. Acad. Sci. USA 104, 9052-9057 (2007). (Pubitemid 47175435)
28. Yoon, H. S. et al. Single cell genomics reveals trophic interactions and evolutionary history of uncultured protists. Science 332, 714-717 (2011).
29. Heywood, J. L. et al. Capturing diversity of marine heterotrophic protists: one cell at a time. ISME J. 5, 674-684 (2010).
30. Rodrigue, S. et al. Whole genome amplification and de novo assembly of single bacterial cells. PLoS ONE 4, e6864 (2009).
31. Woyke, T. et al. Assembling the marine metagenome, one cell at a time. PLoS ONE 4, e5299 (2009).
32. Mann, N. H. et al. The Genome of S-PM2, a "photosynthetic" T4-type bacteriophage that infects marine Synechococcus strains. J. Bacteriol. 187, 3188-3200 (2005). (Pubitemid 40571612)
33. Sullivan, M. B. et al. Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol. 3, e144 (2005).
34. Sharon, I. et al. PhotosystemI gene cassettes are present in marine virus genomes. Nature 461, 258-262 (2009).
35. Doolittle, W. F. You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet. 14, 307-311 (1998).
36. Criscuolo, A. & Gribaldo, S. Large-scale phylogenomic analyses indicate a deep origin of primary plastids within cyanobacteria. Mol. Biol. Evol. 28, 3019-32 (2011).
37. Sieracki, M., Poulton, N. & Crosbie, N. Automated isolation techniques for microalgae. In Algal Culturing Techniques (ed R. A. Andersen) 101-116 (Elsevier Academic, New York, 2005)
38. Andersson, J. O. Horizontal gene transfer between microbial eukaryotes. Methods Mol. Biol. 532, 473-487 (2009).
39. Nosenko, T. & Bhattacharya, D. Horizontal gene transfer in chromalveolates. BMC Evol. Biol. 7, 173 (2007).
40. Keeling, P. J. & Palmer, J. D. Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 9, 605-618 (2008).
41. Timmis, J. N. et al. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 5, 123-135 (2004). (Pubitemid 38160279)
42. Gross, J. & Bhattacharya, D. Mitochondrial and plastid evolution in eukaryotes: an outsider's perspective. Nat. Rev. Genet. 10, 495-505 (2009).
43. Sun, G. & Huang, J. Horizontally acquired DAP pathway as a unit of selfregulation. J. Evol. Biol. 24, 587-595 (2011).
44. Partensky, F., Hess, W. R. & Vaulot, D. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63, 106-127 (1999). (Pubitemid 29116088)
45. Rose, J. M. et al. Counting heterotrophic nanoplanktonic protists in cultures and in aquatic communities by flow cytometry. Aquat. Microb. Ecol. 34, 263-277 (2004). (Pubitemid 39098820)
46. Dean, F. B. et al. Comprehensive human genome amplification using multiple displacement amplification. Proc. Natl. Acad. Sci. USA 99, 5261-5266 (2002). (Pubitemid 34411536)
47. Raghunathan, A. et al. Genomic DNA amplification from a single bacterium. Appl. Environ. Microbiol. 71, 3342-3347 (2005). (Pubitemid 40807247)
48. Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa andmixed models. Bioinformatics 22, 2688-2690 (2006). (Pubitemid 44642609)
49. Guindon, S. & Gascuel, O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704 (2003). (Pubitemid 37365050)