Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs

Curtis, Bruce A.; Tanifuji, Goro; Burki, Fabien; Gruber, Ansgar; Irimia, Manuel; Maruyama, Shinichiro; Arias, María Cecilia; Ball, Steven; Gile, Gillian H.; Hirakawa, Yoshihisa; Hopkins, Julia F.; Kuo, Alan; Rensing, Stefan A.; Schmutz, Jeremy; Symeonidi, Aikaterini; Eliáš, Marek; Eveleigh, Robert; Herman, Emily K.; Klute, Mary J.; Nakayama, Takuro; Oborník, Miroslav; Reyes‐Prieto, Adrián; Armbrust, E. Virginia; Aves, Stephen J.; Beiko, Robert G.; Coutinho, Pedro M.; Dacks, Joel B.; Durnford, Dion G.; Fast, Naomi M.; Green, Beverley R.; Grisdale, Cameron J.; Hempel, Franziska; Henrissat, Bernard; Höppner, Marc P.; Ishida, Koichi; Kim, Eun-Soo; Kořený, Luděk; Kroth, Peter G.; Liu, Yuan; Malik, Shehre-Banoo; Maier, Uwe G.; McRose, Darcy L.; Möck, Thomas; Neilson, Jonathan A. D.; Onodera, Naoko T.; Poole, Anthony M.; Pritham, Ellen J.; Richards, Thomas A.; Rocap, Gabrielle; Roy, Scott William; Sarai, Chihiro; Schaack, Sarah; Shirato, Shu; Slamovits, Claudio H.; Spencer, David F.; Suzuki, Shigekatsu; Worden, Alexandra Z.; Zauner, Stefan; Barry, Kerrie; Bell, Callum J.; Bharti, Arvind K.; Crow, John A.; Grimwood, Jane; Kramer, Robin; Lindquist, Erika; Lucas, Susan; Salamov, Asaf; McFadden, Geoffrey I.; Lane, Christopher E.; Keeling, Patrick J.; Gray, Michael W.; Grigoriev, Igor V.; Archibald, John M.

doi:10.1038/nature11681

Cited by 362 publications

(415 citation statements)

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“…This may imply that starch granule aggregation could dispense with the postulated debranching mechanism, although the crystallinity of this residual material still needs to be ascertained. Second, some of the secondary endosymbiosis lineages derived from Archaeplastida, as well as some little studied semiamylopectin accumulating cyanobacteria, were reported to lack candidate-direct DBE genes (Deschamps et al, 2006;Ball et al, 2011;Colleoni and Suzuki, 2012;Curtis et al, 2012). This observation would imply a nonessential function of polysaccharide debranching in amylopectin synthesis.…”

Section: Evolution Of Direct Dbes Involved In Amylopectin Maturation mentioning

confidence: 94%

Convergent Evolution of Polysaccharide Debranching Defines a Common Mechanism for Starch Accumulation in Cyanobacteria and Plants

et al. 2013

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Starch, unlike hydrosoluble glycogen particles, aggregates into insoluble, semicrystalline granules. In photosynthetic eukaryotes, the transition to starch accumulation occurred after plastid endosymbiosis from a preexisting cytosolic host glycogen metabolism network. This involved the recruitment of a debranching enzyme of chlamydial pathogen origin. The latter is thought to be responsible for removing misplaced branches that would otherwise yield a water-soluble polysaccharide. We now report the implication of starch debranching enzyme in the aggregation of semicrystalline granules of single-cell cyanobacteria that accumulate both glycogen and starch-like polymers. We show that an enzyme of analogous nature to the plant debranching enzyme but of a different bacterial origin was recruited for the same purpose in these organisms. Remarkably, both the plant and cyanobacterial enzymes have evolved through convergent evolution, showing novel yet identical substrate specificities from a preexisting enzyme that originally displayed the much narrower substrate preferences required for glycogen catabolism.

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Section: Evolution Of Direct Dbes Involved In Amylopectin Maturation mentioning

confidence: 94%

Convergent Evolution of Polysaccharide Debranching Defines a Common Mechanism for Starch Accumulation in Cyanobacteria and Plants

et al. 2013

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“…From a set of ∼6,200 and 7,500 broadly distributed proteins in B. natans and G. theta, respectively, 353 (5.7%) and 508 (6.8%) were found to be of clear algal endosymbiont origin (81). One curious observation is that genes of apparent green and red algal ancestry were found in both genomes.…”

Section: The Fate Of Endosymbiotically Derived Nuclei and Their Genesmentioning

confidence: 99%

“…1). Proteins of algal ancestry were also predicted to be targeted to the host ER/Golgi apparatus and to the mitochondrion (81). The bulk of these algal proteins-76% and 66% in B. natans and G. theta, respectivelyappear to be cytosolic.…”

Section: The Fate Of Endosymbiotically Derived Nuclei and Their Genesmentioning

confidence: 99%

“…Detailed insight into the fate of endosymbiotically derived genes in complex algae has come from investigation of the nuclear genomes of two independently evolved nucleomorphbearing algae, the chlorarachniophyte Bigelowiella natans and the cryptophyte Guillardia theta (81). From a set of ∼6,200 and 7,500 broadly distributed proteins in B. natans and G. theta, respectively, 353 (5.7%) and 508 (6.8%) were found to be of clear algal endosymbiont origin (81).…”

Section: The Fate Of Endosymbiotically Derived Nuclei and Their Genesmentioning

confidence: 99%

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Genomic perspectives on the birth and spread of plastids

Archibald

2015

Proc. Natl. Acad. Sci. U.S.A.

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The endosymbiotic origin of plastids from cyanobacteria was a landmark event in the history of eukaryotic life. Subsequent to the evolution of primary plastids, photosynthesis spread from red and green algae to unrelated eukaryotes by secondary and tertiary endosymbiosis. Although the movement of cyanobacterial genes from endosymbiont to host is well studied, less is known about the migration of eukaryotic genes from one nucleus to the other in the context of serial endosymbiosis. Here I explore the magnitude and potential impact of nucleus-to-nucleus endosymbiotic gene transfer in the evolution of complex algae, and the extent to which such transfers compromise our ability to infer the deep structure of the eukaryotic tree of life. In addition to endosymbiotic gene transfer, horizontal gene transfer events occurring before, during, and after endosymbioses further confound our efforts to reconstruct the ancient mergers that forged multiple lines of photosynthetic microbial eukaryotes.

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“…In the context of the model discussed here, it is important to emphasize that, unlike the genome of their free living ancestors or that of most other eukaryotic cells, the genome of these endosymbionts is separated from host cytoplasm by several membranes (the nuclear envelope and the cellular and phagosomal membranes [26]), which constitute an effective 'physical' barrier and defensive system against exogenous inserting viral elements [18]. In the absence of newly introduced viral elements, the selective pressure associated with insertional mutagenesis had diminished, which led to the elimination of introns and of most jDNA, which are no longer needed as protective mechanisms; interestingly, the presence of membranes and the lack of mobile elements in these endosymbionts might also be responsible for the lack of transfer of their genes to the host genome and, therefore, for their evolutionary survival as nucleomorphs [28].…”

Section: (I) Origin Of Jdna Sequencesmentioning

confidence: 99%