Bonora, M. et al. ATP synthesis and storage. Purinergic Signal. 8, 343–357 (2012).
Ruprecht, J. J. & Kunji, E. R. S. Structural mechanism of transport of mitochondrial carriers. Annu. Rev. Biochem. 90, 535–558 (2021).
Omsland, A., Sixt, B. S., Horn, M. & Hackstadt, T. Chlamydial metabolism revisited: interspecies metabolic variability and developmental stage-specific physiologic activities. FEMS Microbiol. Rev. 38, 779–801 (2014).
Ende, R. J. & Derre, I. Host and bacterial glycolysis during Chlamydia trachomatis infection. Infect. Immun. 88, e00545-20 (2020).
Winkler, H. H. Rickettsial permeability. An ADP-ATP transport system. J. Biol. Chem. 251, 389–396 (1976).
Hatch, T. P., Al-Hossainy, E. & Silverman, J. A. Adenine nucleotide and lysine transport in Chlamydia psittaci. J. Bacteriol. 150, 662–670 (1982).
Krause, D. C., Winkler, H. H. & Wood, D. O. Cloning and expression of the Rickettsia prowazekii ADP/ATP translocator in Escherichia coli. Proc. Natl Acad. Sci. USA 82, 3015–3019 (1985).
Stephens, R. S. et al. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282, 754–759 (1998).
Andersson, S. G. et al. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396, 133–140 (1998).
Kalman, S. et al. Comparative genomes of Chlamydia pneumoniae and C. trachomatis. Nat. Genet. 21, 385–389 (1999).
Tjaden, J. et al. Two nucleotide transport proteins in Chlamydia trachomatis, one for net nucleoside triphosphate uptake and the other for transport of energy. J. Bacteriol. 181, 1196–1202 (1999).
Katinka, M. D. et al. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414, 450–453 (2001).
Tsaousis, A. D. et al. A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature 453, 553–556 (2008).
Winkler, H. H. & Neuhaus, H. E. Non-mitochondrial ATP transport. Trends Biochem. Sci. 24, 64–68 (1999).
Linka, N. et al. Phylogenetic relationships of non-mitochondrial nucleotide transport proteins in bacteria and eukaryotes. Gene 306, 27–35 (2003).
Schmitz-Esser, S. et al. ATP/ADP translocases: a common feature of obligate intracellular amoebal symbionts related to Chlamydiae and Rickettsiae. J. Bacteriol. 186, 683–691 (2004).
Schmitz-Esser, S. et al. Lawsonia intracellularis contains a gene encoding a functional rickettsia-like ATP/ADP translocase for host exploitation. J. Bacteriol. 190, 5746–5752 (2008).
Vahling, C. M., Duan, Y. & Lin, H. Characterization of an ATP translocase identified in the destructive plant pathogen “Candidatus Liberibacter asiaticus”. J. Bacteriol. 192, 834–840 (2010).
Knab, S., Mushak, T. M., Schmitz-Esser, S., Horn, M. & Haferkamp, I. Nucleotide parasitism by Simkania negevensis (Chlamydiae). J. Bacteriol. 193, 225–235 (2011).
Graf, J. S. et al. Anaerobic endosymbiont generates energy for ciliate host by denitrification. Nature 591, 445–450 (2021).
Husnik, F. et al. Bacterial and archaeal symbioses with protists. Curr. Biol. 31, R862–R877 (2021).
Needham, D. M. et al. The microbiome of a bacterivorous marine choanoflagellate contains a resource-demanding obligate bacterial associate. Nat. Microbiol. 7, 1466–1479 (2022).
Heldt, H. W. Adenine nucleotide translocation in spinach chloroplasts. FEBS Lett. 5, 11–14 (1969).
Neuhaus, H. E., Thom, E., Mohlmann, T., Steup, M. & Kampfenkel, K. Characterization of a novel eukaryotic ATP/ADP translocator located in the plastid envelope of Arabidopsis thaliana L. Plant J. 11, 73–82 (1997).
Tjaden, J., Schwoppe, C., Mohlmann, T., Quick, P. W. & Neuhaus, H. E. Expression of a plastidic ATP/ADP transporter gene in Escherichia coli leads to a functional adenine nucleotide transport system in the bacterial cytoplasmic membrane. J. Biol. Chem. 273, 9630–9636 (1998).
Mohlmann, T. et al. Occurrence of two plastidic ATP/ADP transporters in Arabidopsis thaliana L.—molecular characterisation and comparative structural analysis of similar ATP/ADP translocators from plastids and Rickettsia prowazekii. Eur. J. Biochem. 252, 353–359 (1998).
Haferkamp, I., Fernie, A. R. & Neuhaus, H. E. Adenine nucleotide transport in plants: much more than a mitochondrial issue. Trends Plant Sci. 16, 507–515 (2011).
Greub, G. & Raoult, D. History of the ADP/ATP-translocase-encoding gene, a parasitism gene transferred from a Chlamydiales ancestor to plants 1 billion years ago. Appl. Environ. Microbiol. 69, 5530–5535 (2003).
Huang, J. & Gogarten, J. P. Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? Genome Biol. 8, R99 (2007).
Tyra, H. M., Linka, M., Weber, A. P. & Bhattacharya, D. Host origin of plastid solute transporters in the first photosynthetic eukaryotes. Genome Biol. 8, R212 (2007).
Nowack, E. C. M. & Weber, A. P. M. Genomics-informed insights into endosymbiotic organelle evolution in photosynthetic eukaryotes. Annu. Rev. Plant. Biol. 69, 51–84 (2018).
Mehta, A. P. et al. Engineering yeast endosymbionts as a step toward the evolution of mitochondria. Proc. Natl Acad. Sci. USA 115, 11796–11801 (2018).
Mehta, A. P. et al. Toward a synthetic yeast endosymbiont with a minimal genome. J. Am. Chem. Soc. 141, 13799–13802 (2019).
Cournoyer, J. E. et al. Engineering artificial photosynthetic life-forms through endosymbiosis. Nat. Commun. 13, 2254 (2022).
Saier, M. H. Jr. Families of transmembrane sugar transport proteins. Mol. Microbiol. 35, 699–710 (2000).
Trentmann, O., Horn, M., van Scheltinga, A. C., Neuhaus, H. E. & Haferkamp, I. Enlightening energy parasitism by analysis of an ATP/ADP transporter from chlamydiae. PLoS Biol. 5, e231 (2007).
Trentmann, O., Jung, B., Neuhaus, H. E. & Haferkamp, I. Nonmitochondrial ATP/ADP transporters accept phosphate as third substrate. J. Biol. Chem. 283, 36486–36493 (2008).
Winkler, H. H. & Daugherty, R. M. Regulatory role of phosphate and other anions in transport of ADP and ATP by Rickettsia prowazekii. J. Bacteriol. 160, 76–79 (1984).
Deniaud, A. et al. Oligomeric status and nucleotide binding properties of the plastid ATP/ADP transporter 1: toward a molecular understanding of the transport mechanism. PLoS ONE 7, e32325 (2012).
Haferkamp, I. et al. A candidate NAD+ transporter in an intracellular bacterial symbiont related to Chlamydiae. Nature 432, 622–625 (2004).
Haferkamp, I. et al. Tapping the nucleotide pool of the host: novel nucleotide carrier proteins of Protochlamydia amoebophila. Mol. Microbiol. 60, 1534–1545 (2006).
Audia, J. P. & Winkler, H. H. Study of the five Rickettsia prowazekii proteins annotated as ATP/ADP translocases (Tlc): only Tlc1 transports ATP/ADP, while Tlc4 and Tlc5 transport other ribonucleotides. J. Bacteriol. 188, 6261–6268 (2006).
Ast, M. et al. Diatom plastids depend on nucleotide import from the cytosol. Proc. Natl Acad. Sci. USA 106, 3621–3626 (2009).
Fisher, D. J., Fernandez, R. E. & Maurelli, A. T. Chlamydia trachomatis transports NAD via the Npt1 ATP/ADP translocase. J. Bacteriol. 195, 3381–3386 (2013).
Heinz, E. et al. Plasma membrane-located purine nucleotide transport proteins are key components for host exploitation by microsporidian intracellular parasites. PLoS Pathog. 10, e1004547 (2014).
Major, P., Embley, T. M. & Williams, T. A. Phylogenetic diversity of NTT nucleotide transport proteins in free-living and parasitic bacteria and eukaryotes. Genome Biol. Evol. 9, 480–487 (2017).
Dean, P. et al. Transporter gene acquisition and innovation in the evolution of Microsporidia intracellular parasites. Nat. Commun. 9, 1709 (2018).
Malyshev, D. A. et al. A semi-synthetic organism with an expanded genetic alphabet. Nature 509, 385–388 (2014).
Zhang, Y. et al. A semi-synthetic organism that stores and retrieves increased genetic information. Nature 551, 644–647 (2017).
Trentmann, O., Decker, C., Winkler, H. H. & Neuhaus, H. E. Charged amino-acid residues in transmembrane domains of the plastidic ATP/ADP transporter from Arabidopsis are important for transport efficiency, substrate specificity, and counter exchange properties. Eur. J. Biochem. 267, 4098–4105 (2000).
Alexeyev, M. F. & Winkler, H. H. Membrane topology of the Rickettsia prowazekii ATP/ADP translocase revealed by novel dual pho–lac reporters. J. Mol. Biol. 285, 1503–1513 (1999).
Pebay-Peyroula, E. et al. Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426, 39–44 (2003).
Ruprecht, J. J. et al. The molecular mechanism of transport by the mitochondrial ADP/ATP carrier. Cell 176, 435–447 (2019).
Traut, T. W. Physiological concentrations of purines and pyrimidines. Mol. Cell. Biochem. 140, 1–22 (1994).
Law, C. J., Maloney, P. C. & Wang, D. N. Ins and outs of major facilitator superfamily antiporters. Annu. Rev. Microbiol. 62, 289–305 (2008).
Yan, N. Structural biology of the major facilitator superfamily transporters. Annu. Rev. Biophys. 44, 257–283 (2015).
Moodie, S. L., Mitchell, J. B. & Thornton, J. M. Protein recognition of adenylate: an example of a fuzzy recognition template. J. Mol. Biol. 263, 486–500 (1996).
Mavridou, V. et al. Substrate binding in the mitochondrial ADP/ATP carrier is a step-wise process guiding the structural changes in the transport cycle. Nat. Commun. 13, 3585 (2022).
Kunji, E. R. S. & Ruprecht, J. J. The mitochondrial ADP/ATP carrier exists and functions as a monomer. Biochem. Soc. Trans. 48, 1419–1432 (2020).
Feldman, A. W. et al. A tool for the import of natural and unnatural nucleoside triphosphates into bacteria. J. Am. Chem. Soc. 140, 1447–1454 (2018).
Goehring, A. et al. Screening and large-scale expression of membrane proteins in mammalian cells for structural studies. Nat. Protoc. 9, 2574–2585 (2014).
Zimmermann, I. et al. Generation of synthetic nanobodies against delicate proteins. Nat. Protoc. 15, 1707–1741 (2020).
Wu, X. & Rapoport, T. A. Cryo-EM structure determination of small proteins by nanobody-binding scaffolds (Legobodies). Proc. Natl Acad. Sci. USA 118, e2115001118 (2021).
Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. CryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).
Terwilliger, T. C., Ludtke, S. J., Read, R. J., Adams, P. D. & Afonine, P. V. Improvement of cryo-EM maps by density modification. Nat. Methods 17, 923–927 (2020).
Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta. Crystallogr. D Biol. Crystallogr. 66, 213–221 (2010).
Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta. Crystallogr. D Biol. Crystallogr. 66, 486–501 (2010).
Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta. Crystallogr. D Biol. Crystallogr. 66, 12–21 (2010).
PyMOL Molecular Graphics System v.2.0 (Schrödinger, 2017).
Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
Pettersen, E. F. et al. UCSF ChimeraX: structure visualization for researchers, educators, and developers. Protein Sci. 30, 70–82 (2021).
