- Email: [email protected]
Endosymbiotic gene transfer: What bioenergetic organelles did for eukaryotic chromosomes
Biochimica et Biophysica Acta 1857 (2016?) e1–e7
Contents lists available at ScienceDirect
Biochimica et Biophysica Acta j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / b b a b i o
Plenary Lectures (in order of presentation)
Peter Mitchell Medal Lecture Chemiosmotic coupling in the respiratory chain: cytochrome oxidase past, present and future Peter R. Rich Glynn Laboratory of Bioenergetics, Institute of Structural and Molecular Biology, UCL, Gower Street, London, UK E-mail address: [email protected] (P.R. Rich) The roots of elucidation of the metabolic pathways of energy provision can be traced back to the work of Warburg in Germany and of Hopkins in the UK. Keilin and others provided the link to how reductants produced by the Krebs cycle and other metabolic pathways are oxidised with oxygen by the respiratory electron transfer chain. In 1961 Peter Mitchell proposed the chemiosmotic mechanism for coupling of respiratory chain electron transfer to the synthesis of cellular ATP. However, it took a great deal of time, experimentation and acrimonious exchanges before the central ideas became generally accepted. Since then, major advances have been made in the elucidation of atomic structures of the molecular machines involved. Together with information from a wide range of functional studies with biochemical and biophysical methods, these structures provide insights into the intricate mechanisms, some foreseen and others not by Mitchell, that have evolved to convert redox energy from products of metabolism into the electrochemical gradient of protons across the inner mitochondrial membrane that powers ATP synthesis. I will review the development of ideas on one of these chemiosmotic molecular machines, mitochondrial cytochrome c oxidase, and will highlight structure/ function aspects that remain to be resolved and features of the supernumerary subunits still to be understood that are relevant to health and disease.
Chloroplasts arose from cyanobacteria, mitochondria arose from proteobacteria. Both organelles have conserved their prokaryotic biochemistry, but their genomes are reduced, and most organelle proteins are encoded in the nucleus. Endosymbiotic theory posits that bacterial genes in eukaryotic genomes entered the eukaryotic lineage via organelle ancestors. It predicts episodic influx of prokaryotic genes into the eukaryotic lineage, with acquisition corresponding to endosymbiotic events. Eukaryotic genome sequences, however, increasingly implicate lateral gene transfer, both from prokaryotes to eukaryotes and among eukaryotes, as a source of gene content variation in eukaryotic genomes, which predicts continuous, lineage-specific acquisition of prokaryotic genes in divergent eukaryotic groups. One can discriminate between these two alternatives by clustering and phylogenetic analysis of eukaryotic gene families having prokaryotic homologues. The results indicate (1) that gene transfer from bacteria to eukaryotes is episodic, as revealed by gene distributions, and coincides with major evolutionary transitions at the origin of chloroplasts and mitochondria; (2) that gene inheritance in eukaryotes is vertical, as revealed by extensive topological comparison, sparse gene distributions stemming from differential loss; and (3) that continuous, lineage-specific lateral gene transfer, although it sometimes occurs, does not contribute to longterm gene content evolution in eukaryotic genomes. doi:10.1016/j.bbabio.2016.04.011
Session I - Electron transfer
Redox-gated NADH oxidation by complex I Thorsten Friedrich Institute of Biochemistry, Albert-Ludwigs-Universität, Freiburg, Germany E-mail address: [email protected] (T. Friedrich)
doi:10.1016/j.bbabio.2016.04.010
Opening Lecture
Endosymbiotic gene transfer: What bioenergetic organelles did for eukaryotic chromosomes William Martin Institute for Molecular Evolution, University of Düsseldorf, 40225 Düsseldorf, Germany E-mail address: [email protected] (W. Martin) 0005-2728/$ – see front matter
Respiratory complex I couples the electron transfer from NADH to ubiquinone with the translocation of protons across the membrane. Electron transfer takes place in the peripheral arm of the complex and is spatially separated from proton translocation in the membrane arm [1]. NADH is oxidized at the top of the peripheral arm by FMN. Electrons are transferred via an 80 Å long chain made up of seven iron-sulfur (Fe/S) clusters to the quinone reduction site. Another conserved Fe/S cluster N1a that is off that pathway is located in electron tunneling distance to the FMN. The chain of Fe/S clusters is not a simple electron wire, but controls the electron tunneling rates [2]. Reduction of the last cluster of the chain, N2, leads to a six-fold slower rate, most likely to synchronize fast electron transfer with slow proton translocation. In addition, a
Contents lists available at ScienceDirect
Biochimica et Biophysica Acta j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / b b a b i o
Plenary Lectures (in order of presentation)
Peter Mitchell Medal Lecture Chemiosmotic coupling in the respiratory chain: cytochrome oxidase past, present and future Peter R. Rich Glynn Laboratory of Bioenergetics, Institute of Structural and Molecular Biology, UCL, Gower Street, London, UK E-mail address: [email protected] (P.R. Rich) The roots of elucidation of the metabolic pathways of energy provision can be traced back to the work of Warburg in Germany and of Hopkins in the UK. Keilin and others provided the link to how reductants produced by the Krebs cycle and other metabolic pathways are oxidised with oxygen by the respiratory electron transfer chain. In 1961 Peter Mitchell proposed the chemiosmotic mechanism for coupling of respiratory chain electron transfer to the synthesis of cellular ATP. However, it took a great deal of time, experimentation and acrimonious exchanges before the central ideas became generally accepted. Since then, major advances have been made in the elucidation of atomic structures of the molecular machines involved. Together with information from a wide range of functional studies with biochemical and biophysical methods, these structures provide insights into the intricate mechanisms, some foreseen and others not by Mitchell, that have evolved to convert redox energy from products of metabolism into the electrochemical gradient of protons across the inner mitochondrial membrane that powers ATP synthesis. I will review the development of ideas on one of these chemiosmotic molecular machines, mitochondrial cytochrome c oxidase, and will highlight structure/ function aspects that remain to be resolved and features of the supernumerary subunits still to be understood that are relevant to health and disease.
Chloroplasts arose from cyanobacteria, mitochondria arose from proteobacteria. Both organelles have conserved their prokaryotic biochemistry, but their genomes are reduced, and most organelle proteins are encoded in the nucleus. Endosymbiotic theory posits that bacterial genes in eukaryotic genomes entered the eukaryotic lineage via organelle ancestors. It predicts episodic influx of prokaryotic genes into the eukaryotic lineage, with acquisition corresponding to endosymbiotic events. Eukaryotic genome sequences, however, increasingly implicate lateral gene transfer, both from prokaryotes to eukaryotes and among eukaryotes, as a source of gene content variation in eukaryotic genomes, which predicts continuous, lineage-specific acquisition of prokaryotic genes in divergent eukaryotic groups. One can discriminate between these two alternatives by clustering and phylogenetic analysis of eukaryotic gene families having prokaryotic homologues. The results indicate (1) that gene transfer from bacteria to eukaryotes is episodic, as revealed by gene distributions, and coincides with major evolutionary transitions at the origin of chloroplasts and mitochondria; (2) that gene inheritance in eukaryotes is vertical, as revealed by extensive topological comparison, sparse gene distributions stemming from differential loss; and (3) that continuous, lineage-specific lateral gene transfer, although it sometimes occurs, does not contribute to longterm gene content evolution in eukaryotic genomes. doi:10.1016/j.bbabio.2016.04.011
Session I - Electron transfer
Redox-gated NADH oxidation by complex I Thorsten Friedrich Institute of Biochemistry, Albert-Ludwigs-Universität, Freiburg, Germany E-mail address: [email protected] (T. Friedrich)
doi:10.1016/j.bbabio.2016.04.010
Opening Lecture
Endosymbiotic gene transfer: What bioenergetic organelles did for eukaryotic chromosomes William Martin Institute for Molecular Evolution, University of Düsseldorf, 40225 Düsseldorf, Germany E-mail address: [email protected] (W. Martin) 0005-2728/$ – see front matter
Respiratory complex I couples the electron transfer from NADH to ubiquinone with the translocation of protons across the membrane. Electron transfer takes place in the peripheral arm of the complex and is spatially separated from proton translocation in the membrane arm [1]. NADH is oxidized at the top of the peripheral arm by FMN. Electrons are transferred via an 80 Å long chain made up of seven iron-sulfur (Fe/S) clusters to the quinone reduction site. Another conserved Fe/S cluster N1a that is off that pathway is located in electron tunneling distance to the FMN. The chain of Fe/S clusters is not a simple electron wire, but controls the electron tunneling rates [2]. Reduction of the last cluster of the chain, N2, leads to a six-fold slower rate, most likely to synchronize fast electron transfer with slow proton translocation. In addition, a