Evolution of the F0F1 ATP Synthase Complex in Light of the Patchy Distribution of Different Bioenergetic Pathways across Prokaryotes

Bacteria and archaea are characterized by an amazing metabolic diversity, which allows them to persist in diverse and often extreme habitats. Apart from oxygenic photosynthesis and oxidative phosphorylation, well-studied processes from chloroplasts and mitochondria of plants and animals, prokaryotes utilize various chemo- or lithotrophic modes, such as anoxygenic photosynthesis, iron oxidation and reduction, sulfate reduction, and methanogenesis. Most bioenergetic pathways have a similar general structure, with an electron transport chain composed of protein complexes acting as electron donors and acceptors, as well as a central cytochrome complex, mobile electron carriers, and an ATP synthase. While each pathway has been studied in considerable detail in isolation, not much is known about their relative evolutionary relationships. Wanting to address how this metabolic diversity evolved, we mapped the distribution of nine bioenergetic modes on a phylogenetic tree based on 16S rRNA sequences from 272 species representing the full diversity of prokaryotic lineages. This highlights the patchy distribution of many pathways across different lineages, and suggests either up to 26 independent origins or 17 horizontal gene transfer events. Next, we used comparative genomics and phylogenetic analysis of all subunits of the F0F1 ATP synthase, common to most bacterial lineages regardless of their bioenergetic mode. Our results indicate an ancient origin of this protein complex, and no clustering based on bioenergetic mode, which suggests that no special modifications are needed for the ATP synthase to work with different electron transport chains. Moreover, examination of the ATP synthase genetic locus indicates various gene rearrangements in the different bacterial lineages, ancient duplications of atpI and of the beta subunit of the F0 subcomplex, as well as more recent stochastic lineage-specific and species-specific duplications of all subunits. We discuss the implications of the overall pattern of conservation and flexibility of the F0F1 ATP synthase genetic locus.

[1]  Natalia N. Ivanova,et al.  A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea , 2009, Nature.

[2]  Philip Hugenholtz,et al.  Impact of Culture-Independent Studies on the Emerging Phylogenetic View of Bacterial Diversity , 1998, Journal of bacteriology.

[3]  K. Weber,et al.  Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction , 2006, Nature Reviews Microbiology.

[4]  A. Walburger,et al.  Supramolecular organization in prokaryotic respiratory systems. , 2012, Advances in microbial physiology.

[5]  Thomas J Naughton,et al.  Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified , 2006, BMC Evolutionary Biology.

[6]  Se-Ran Jun,et al.  Whole-proteome phylogeny of prokaryotes by feature frequency profiles: An alignment-free method with optimal feature resolution , 2009, Proceedings of the National Academy of Sciences.

[7]  E. Rocha,et al.  Horizontal Transfer, Not Duplication, Drives the Expansion of Protein Families in Prokaryotes , 2011, PLoS genetics.

[8]  C. Soares,et al.  Sulphate respiration from hydrogen in Desulfovibrio bacteria: a structural biology overview. , 2005, Progress in biophysics and molecular biology.

[9]  C. Ouzounis,et al.  The balance of driving forces during genome evolution in prokaryotes. , 2003, Genome research.

[10]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[11]  D. Harris,et al.  How much data are needed to resolve a difficult phylogeny?: case study in Lamiales. , 2005, Systematic biology.

[12]  Gabriel Moreno-Hagelsieb,et al.  Phylogenomic clustering for selecting non-redundant genomes for comparative genomics , 2013, Bioinform..

[13]  S. Dunn,et al.  Functional Incorporation of Chimeric b Subunits into F1Fo ATP Synthase , 2007, Journal of bacteriology.

[14]  E. Delong,et al.  Characterization of an Autotrophic Sulfide-Oxidizing Marine Arcobacter sp. That Produces Filamentous Sulfur , 2002, Applied and Environmental Microbiology.

[15]  Radhey S. Gupta,et al.  Critical issues in bacterial phylogeny. , 2002, Theoretical population biology.

[16]  John D. Kececioglu,et al.  Multiple alignment by aligning alignments , 2007, ISMB/ECCB.

[17]  Gabriele Deckers-Hebestreit,et al.  Individual Interactions of the b Subunits within the Stator of the Escherichia coli ATP Synthase* , 2013, The Journal of Biological Chemistry.

[18]  David Posada,et al.  ProtTest: selection of best-fit models of protein evolution , 2005, Bioinform..

[19]  Michael Y. Galperin,et al.  Inventing the dynamo machine: the evolution of the F-type and V-type ATPases , 2007, Nature Reviews Microbiology.

[20]  S. Hedges,et al.  A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land , 2004, BMC Evolutionary Biology.

[21]  John P. Huelsenbeck,et al.  MrBayes 3: Bayesian phylogenetic inference under mixed models , 2003, Bioinform..

[22]  James R. Cole,et al.  The Ribosomal Database Project: improved alignments and new tools for rRNA analysis , 2008, Nucleic Acids Res..

[23]  V. Müller,et al.  Bioenergetics of archaea: ancient energy conserving mechanisms developed in the early history of life. , 2006, Biochimica et biophysica acta.

[24]  S. Shima,et al.  Structure and function of enzymes involved in the methanogenic pathway utilizing carbon dioxide and molecular hydrogen. , 2002, Journal of bioscience and bioengineering.

[25]  Tal Dagan,et al.  Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution , 2008, Proceedings of the National Academy of Sciences.

[26]  A. Knoll,et al.  The evolution of ecological tolerance in prokaryotes , 1989, Earth and Environmental Science Transactions of the Royal Society of Edinburgh.

[27]  J. Castresana,et al.  Comparative genomics and bioenergetics. , 2001, Biochimica et biophysica acta.

[28]  A. Persson,et al.  Specific Evolution of F1-Like ATPases in Mycoplasmas , 2012, PloS one.

[29]  Masasuke Yoshida,et al.  The product of uncI gene in F1Fo-ATP synthase operon plays a chaperone-like role to assist c-ring assembly , 2007, Proceedings of the National Academy of Sciences.

[30]  J. Olson,et al.  Thinking About the Evolution of Photosynthesis , 2004, Photosynthesis Research.

[31]  B. Schoepp‐Cothenet,et al.  The redox protein construction kit: pre-last universal common ancestor evolution of energy-conserving enzymes. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[32]  Michael Y. Galperin,et al.  Characterization of the N-ATPase, a distinct, laterally transferred Na+-translocating form of the bacterial F-type membrane ATPase , 2010, Bioinform..

[33]  J. Weber,et al.  Escherichia coli F1Fo-ATP Synthase with a b/δ Fusion Protein Allows Analysis of the Function of the Individual b Subunits* , 2013, The Journal of Biological Chemistry.

[34]  W. Doolittle,et al.  Alternative methods for concatenation of core genes indicate a lack of resolution in deep nodes of the prokaryotic phylogeny. , 2007, Molecular biology and evolution.

[35]  Robert Eugene Blankenship.  Molecular mechanisms of photosynthesis , 2002 .

[36]  U. Deppenmeier.  Redox-driven proton translocation in methanogenic Archaea , 2002, Cellular and Molecular Life Sciences CMLS.

[37]  A. Janssen,et al.  Acquisition of 1,000 eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea , 2012, Proceedings of the National Academy of Sciences.

[38]  A. Ducluzeau,et al.  On the universal core of bioenergetics. , 2013, Biochimica et biophysica acta.

[39]  Y. Kamagata,et al.  Metagenomic and Biochemical Characterizations of Sulfur Oxidation Metabolism in Uncultured Large Sausage-Shaped Bacterium in Hot Spring Microbial Mats , 2012, PloS one.

[40]  Jillian F. Banfield,et al.  Genomics and the Geosciences , 2000, Science.

[41]  David A. Baltrus,et al.  Exploring the costs of horizontal gene transfer. , 2013, Trends in ecology & evolution.

[42]  D. Bryant,et al.  Prokaryotic photosynthesis and phototrophy illuminated. , 2006, Trends in microbiology.

[43]  Jason Raymond,et al.  Conservation of distantly related membrane proteins: photosynthetic reaction centers share a common structural core. , 2006, Molecular biology and evolution.

[44]  Everett Shock,et al.  Merging Genomes with Geochemistry in Hydrothermal Ecosystems , 2002, Science.

[45]  Yutetsu Kuruma,et al.  UncI protein can mediate ring-assembly of c-subunits of FoF1-ATP synthase in vitro. , 2008, Biochemical and biophysical research communications.

[46]  W. Doolittle,et al.  Lateral gene transfer and the origins of prokaryotic groups. , 2003, Annual review of genetics.

[47]  Peter Williams,et al.  IMG: the integrated microbial genomes database and comparative analysis system , 2011, Nucleic Acids Res..

[48]  Gregory C. Finnigan,et al.  Evolution of increased complexity in a molecular machine , 2012, Nature.

[49]  Alexandros Stamatakis,et al.  RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models , 2006, Bioinform..

[50]  Jonathan A. Eisen,et al.  Phylogeny of Bacterial and Archaeal Genomes Using Conserved Genes: Supertrees and Supermatrices , 2013, PloS one.

[51]  R. L. Cross,et al.  The evolution of A‐, F‐, and V‐type ATP synthases and ATPases: reversals in function and changes in the H+/ATP coupling ratio , 2004, FEBS letters.

[52]  M. Engelhard,et al.  Bioenergetics of the Archaea , 1999, Microbiology and Molecular Biology Reviews.

[53]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[54]  Ji Qi,et al.  Prokaryote phylogeny meets taxonomy: An exhaustive comparison of composition vector trees with systematic bacteriology , 2007, Science in China Series C: Life Sciences.