Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica

被引:162
作者
Rumpho, Mary E. [1 ]
Worful, Jared M. [1 ]
Lee, Jungho [2 ]
Kannan, Krishna [1 ]
Tyler, Mary S. [3 ]
Bhattacharya, Debashish [4 ,5 ]
Moustafa, Ahmed [4 ,5 ]
Manhart, James R. [6 ]
机构
[1] Univ Maine, Dept Biochem Microbiol & Mol Biol, Orono, ME 04469 USA
[2] Seoul Natl Univ, Green Plant Inst, Suwon 441853, Gyeonggi, South Korea
[3] Univ Maine, Sch Biol & Ecol, Orono, ME 04469 USA
[4] Univ Iowa, Dept Biol Sci, Iowa City, IA 52242 USA
[5] Univ Iowa, Roy J Carver Ctr Comparat Genom, Interdisciplinary Program Genet, Iowa City, IA 52242 USA
[6] Texas A&M Univ, Dept Biol, College Stn, TX 77843 USA
关键词
symbiosis; Vaucheria litorea; evolution; plastid; stramenopile;
D O I
10.1073/pnas.0804968105
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
The sea slug Elysia chlorotica acquires plastids by ingestion of its algal food source Vaucheria litorea. Organelles are sequestered in the mollusc's digestive epithelium, where they photosynthesize for months in the absence of algal nucleocytoplasm. This is perplexing because plastid metabolism depends on the nuclear genome for >90% of the needed proteins. Two possible explanations for the persistence of photosynthesis in the sea slug are (i) the ability of V. litorea plastids to retain genetic autonomy and/or (it) more likely, the mollusc provides the essential plastid proteins. Under the latter scenario, genes supporting photosynthesis have been acquired by the animal via horizontal gene transfer and the encoded proteins are retargeted to the plastid. We sequenced the plastid genome and confirmed that it lacks the full complement of genes required for photosynthesis. In support of the second scenario, we demonstrated that a nuclear gene of oxygenic photosynthesis, psbO, is expressed in the sea slug and has integrated into the germline. The source of psbO in the sea slug is V. litorea because this sequence is identical from the predator and prey genomes. Evidence that the transferred gene has integrated into sea slug nuclear DNA comes from the finding of a highly diverged psbO 3' flanking sequence in the algal and mollusc nuclear homologues and gene absence from the mitochondrial genome of E. chlorotica. We demonstrate that foreign organelle retention generates metabolic novelty ("green animals") and is explained by anastomosis of distinct branches of the tree of life driven by predation and horizontal gene transfer.
引用
收藏
页码:17867 / 17871
页数:5
相关论文
共 56 条
[1]  
Andersson B, 2001, ADV PHOTOSYNTH, V11, P377
[2]   Lateral gene transfer in eukaryotes [J].
Andersson, JO .
CELLULAR AND MOLECULAR LIFE SCIENCES, 2005, 62 (11) :1182-1197
[3]  
[Anonymous], 2003, Acquiring Genomes: A Theory of the Origins of Species
[4]   Two mitochondrial group I introns in a metazoan, the sea anemone Metridium senile: One intron contains genes for subunits 1 and 3 of NADH dehydrogenase [J].
Beagley, CT ;
Okada, NA ;
Wolstenholme, DR .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1996, 93 (11) :5619-5623
[5]   Chloroplast genome sequencing analysis of Heterosigma akashiwo CCMP452 (West Atlantic) and NIES293 (West Pacific) strains [J].
Cattolico, Rose Ann ;
Jacobs, Michael A. ;
Zhou, Yang ;
Chang, Jean ;
Duplessis, Melinda ;
Lybrand, Terry ;
Mckay, John ;
Ong, Han Chuan ;
Sims, Elizabeth ;
Rocap, Gabrielle .
BMC GENOMICS, 2008, 9 (1)
[6]   Protein import pathways in 'complex' chloroplasts derived from secondary endosymbiosis involving a red algal ancestor [J].
Chaal, BK ;
Green, BR .
PLANT MOLECULAR BIOLOGY, 2005, 57 (03) :333-342
[7]   Ancestral genome sizes specify the minimum rate of lateral gene transfer during prokaryote evolution [J].
Dagan, Tal ;
Martin, William .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2007, 104 (03) :870-875
[8]   Analysis of the structure of the PsbO protein and its implications [J].
De Las Rivas, J ;
Barber, J .
PHOTOSYNTHESIS RESEARCH, 2004, 81 (03) :329-343
[9]   Locating proteins in the cell using TargetP, SignalP and related tools [J].
Emanuelsson, Olof ;
Brunak, Soren ;
von Heijne, Gunnar ;
Nielsen, Henrik .
NATURE PROTOCOLS, 2007, 2 (04) :953-971
[10]  
FELSENSTEIN J, 1985, EVOLUTION, V39, P783, DOI 10.1111/j.1558-5646.1985.tb00420.x