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Energy Metabolism in Eukaryotes Biochemistry and Evolution Of Biochemistry and Evolution of Anaerobic Downloaded from Energy Metabolism in Eukaryotes Miklós Müller, Marek Mentel, Jaap J. van Hellemond, Katrin Henze, Christian Woehle, Sven B. Gould, Re-Young Yu, Mark van der Giezen, Aloysius G. M. Tielens and William F. Martin Microbiol. Mol. Biol. Rev. 2012, 76(2):444. DOI: http://mmbr.asm.org/ 10.1128/MMBR.05024-11. Updated information and services can be found at: http://mmbr.asm.org/content/76/2/444 on June 18, 2012 by UNIVERSITAETS- UND LANDESBIBLIOTHEK DUESSELDORF These include: SUPPLEMENTAL MATERIAL http://mmbr.asm.org/content/suppl/2012/05/23/76.2.444.DC1.ht ml REFERENCES This article cites 571 articles, 205 of which can be accessed free at: http://mmbr.asm.org/content/76/2/444#ref-list-1 CONTENT ALERTS Receive: RSS Feeds, eTOCs, free email alerts (when new articles cite this article), more» Information about commercial reprint orders: http://journals.asm.org/site/misc/reprints.xhtml To subscribe to to another ASM Journal go to: http://journals.asm.org/site/subscriptions/ Biochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes Downloaded from Miklós Müller,a Marek Mentel,b Jaap J. van Hellemond,c Katrin Henze,d Christian Woehle,d Sven B. Gould,d Re-Young Yu,d Mark van der Giezen,e Aloysius G. M. Tielens,c and William F. Martind The Rockefeller University, New York, New York, USAa; Department of Biochemistry, Faculty of Natural Sciences, Comenius University, Bratislava, Slovakiab; Department of Medical Microbiology and Infectious Diseases, Erasmus University Medical Center, Rotterdam, Netherlandsc; Institute of Molecular Evolution, University of Düsseldorf, Düsseldorf, Germanyd; and Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, United Kingdome http://mmbr.asm.org/ INTRODUCTION ............................................................................................................................................444 A FEW DISTINCTIONS ......................................................................................................................................447 Functional and Environmental Anaerobiosis .............................................................................................................447 Redox Balance through Respiration and Fermentation ..................................................................................................448 Anaerobes and Microaerophiles: Redox Balance with a Pinch of O2 .....................................................................................449 METABOLIC PATHWAYS IN EUKARYOTIC ANAEROBES ...................................................................................................450 Animals...................................................................................................................................................450 Fasciola hepatica (liver fluke)...........................................................................................................................450 Ascaris (giant roundworm).............................................................................................................................453 on June 18, 2012 by UNIVERSITAETS- UND LANDESBIBLIOTHEK DUESSELDORF Mytilus edulis (common mussel) .......................................................................................................................453 Arenicola marina (lugworm) ...........................................................................................................................454 Sipunculus nudus (peanut worm) ......................................................................................................................455 A strictly anoxic animal among the loriciferans ........................................................................................................457 Fungi .....................................................................................................................................................457 Piromyces sp. strain E2 and Neocallimastix .............................................................................................................457 Fusarium oxysporum ...................................................................................................................................458 Microsporidia ..........................................................................................................................................459 Amoebozoa: Entamoeba histolytica ......................................................................................................................459 Excavate Taxa.............................................................................................................................................461 Giardia intestinalis ......................................................................................................................................461 Trichomonas vaginalis..................................................................................................................................462 Tritrichomonas foetus ..................................................................................................................................464 Trypanosoma brucei....................................................................................................................................464 Euglena gracilis.........................................................................................................................................467 Excavate pathogens and metronidazole ..............................................................................................................469 Alveolates and Stramenopiles ............................................................................................................................469 Nyctotherus ovalis ......................................................................................................................................469 Blastocystis .............................................................................................................................................469 Rhizaria and Denitrification...............................................................................................................................472 Archaeplastida............................................................................................................................................472 Chlamydomonas .......................................................................................................................................472 EVOLUTIONARY CONSIDERATIONS .......................................................................................................................473 Evolving Concepts........................................................................................................................................473 Anaerobic Energy Metabolism: Present in the Eukaryote Common Ancestor............................................................................474 Comparing Diversity: Eukaryotes versus Rhodobacter ....................................................................................................478 Forests, Trees, and Vertically Inherited Chimerism........................................................................................................478 Functional Modules and Their Compartmentation.......................................................................................................480 Ecological Implications over Geological Time ............................................................................................................480 CONCLUSION...............................................................................................................................................483 ACKNOWLEDGMENTS......................................................................................................................................484 REFERENCES ................................................................................................................................................484 INTRODUCTION the origin of known eukaryotic groups. Second, the phylogeny of eukaryotic aerobes and anaerobes has been found to interleave he presence and function of mitochondria in eukaryotes that across the diversity of eukaryotic groups, erasing what was once Tinhabit anaerobic environments was long a biochemical and evolutionary puzzle. Major insights into the phylogenetic distri- bution, biochemistry, and evolutionary significance of organelles Address correspondence to Aloysius G. M. Tielens, [email protected], or involved in ATP synthesis (energy metabolism) in eukaryotes that William F. Martin, [email protected]. thrive in anaerobic environments for all or part of their life cycles A.G.M.T. and W.F.M. contributed equally. have accrued in recent years. Underpinned by many exciting ad- Supplemental material for this article may be found at http://mmbr.asm.org/. vances, two central themes of this progress have unfolded. First, Copyright © 2012, American Society for Microbiology. All Rights Reserved. the finding that all known eukaryotic groups possess an organelle doi:10.1128/MMBR.05024-11 of mitochondrial origin has mapped the origin of mitochondria to 444 mmbr.asm.org Microbiology and Molecular Biology Reviews p. 444–495 June 2012 Volume 76 Number 2 Anaerobic Energy Metabolism in Eukaryotes Downloaded from http://mmbr.asm.org/ FIG 1 Two organelles
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