Of early animals, anaerobic mitochondria, and a modern sponge

The origin and early evolution of animals marks an important event in life's history. This event is historically associated with an important variable in Earth history – oxygen. One view has it that an increase in oceanic oxygen levels at the end of the Neoproterozoic Era (roughly 600 million years ago) allowed animals to become large and leave fossils. How important was oxygen for the process of early animal evolution? New data show that some modern sponges can survive for several weeks at low oxygen levels. Many groups of animals have mechanisms to cope with low oxygen or anoxia, and very often, mitochondria – organelles usually associated with oxygen – are involved in anaerobic energy metabolism in animals. It is a good time to refresh our memory about the anaerobic capacities of mitochondria in modern animals and how that might relate to the ecology of early metazoans.

[1]  G. Lapage Parasitic Helminths , 1960, Nature.

[2]  S. Udenfriend Formation of Hydroxyproline in Collagen , 1966, Science.

[3]  K. Towe Oxygen-collagen priority and the early metazoan fossil record. , 1970, Proceedings of the National Academy of Sciences of the United States of America.

[4]  M. Müller,et al.  Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. , 1973, The Journal of biological chemistry.

[5]  H. Reiswig Water transport, respiration and energetics of three tropical marine sponges , 1974 .

[6]  L. Margulis,et al.  Reassessment of roles of oxygen and ultraviolet light in Precambrian evolution , 1976, Nature.

[7]  H. Reiswig Partial Carbon and Energy Budgets of the Bacteriosponge Verohgia fistularis (Porifera: Demospongiae) in Barbados , 1981 .

[8]  G. Thillart,et al.  Anaerobic metabolism of goldfish, Carassius auratus (L.): Ethanol and CO2 excretion rates and anoxia tolerance at 20, 10 and 5°C , 1983 .

[9]  A. Hiraishi,et al.  DISTRIBUTION OF RHODOQUINONE IN RHODOSPIRILLACEAE AND ITS TAXONOMIC IMPLICATIONS , 1984 .

[10]  J. B. Jennings,et al.  Metazoan life without oxygen , 1991 .

[11]  P. S. Larsen,et al.  SUSPENSION-FEEDING IN MARINE SPONGES HALICHONDRIA-PANICEA AND HALICLONA-URCEOLUS - EFFECTS OF TEMPERATURE ON FILTRATION-RATE AND ENERGY-COST OF PUMPING , 1993 .

[12]  H. Pörtner,et al.  Physiological and metabolic responses to hypoxia in invertebrates. , 1994, Reviews of physiology, biochemistry and pharmacology.

[13]  A. Tielens Energy generation in parasitic helminths. , 1994, Parasitology today.

[14]  J. J. van Hellemond,et al.  Rhodoquinone and Complex II of the Electron Transport Chain in Anaerobically Functioning Eukaryotes (*) , 1995, The Journal of Biological Chemistry.

[15]  T. Aoki,et al.  Stage-specific Isoforms of Complex II (Succinate-Ubiquinone Oxidoreductase) in Mitochondria from the Parasitic Nematode, Ascaris suum(*) , 1995, The Journal of Biological Chemistry.

[16]  H. U. Riisgård,et al.  Growth and energetics of the sponge Halichondria panicea , 1995 .

[17]  N. Noro,et al.  Type IV collagen in sponges, the missing link in basement membrane ubiquity * , 1996, Biology of the cell.

[18]  Gapped BLAST and PSI-BLAST: A new , 1997 .

[19]  J. Hackstein,et al.  A hydrogenosome with a genome , 1998, Nature.

[20]  J. J. van Hellemond,et al.  The electron transport chain in anaerobically functioning eukaryotes. , 1998, Biochimica et biophysica acta.

[21]  M. Grieshaber,et al.  Animal adaptations for tolerance and exploitation of poisonous sulfide. , 1998, Annual review of physiology.

[22]  C. Kurland,et al.  Origins of mitochondria and hydrogenosomes. , 1999, Current opinion in microbiology.

[23]  M. Grieshaber,et al.  Chemolithoheterotrophy in a metazoan tissue : thiosulfate production matches ATP demand in ciliated mussel gills , 2001 .

[24]  J. Brouwers,et al.  Fasciola hepatica miracidia are dependent on respiration and endogenous glycogen degradation for their energy generation , 2001, Parasitology.

[25]  A. Knoll,et al.  Morphological and ecological complexity in early eukaryotic ecosystems , 2001, Nature.

[26]  N. Lane Oxygen: The molecule that made the world , 2002 .

[27]  W. Martin,et al.  Mitochondria as We Don't Know Them , 2002 .

[28]  W. Martin,et al.  Single eubacterial origin of eukaryotic sulfide:quinone oxidoreductase, a mitochondrial enzyme conserved from the early evolution of eukaryotes during anoxic and sulfidic times. , 2003, Molecular biology and evolution.

[29]  J. J. van Hellemond,et al.  Biochemical and evolutionary aspects of anaerobically functioning mitochondria. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[30]  J. Sharp,et al.  In situ feeding and element removal in the symbiont‐bearing sponge Theonella swinhoei: Bulk DOC is the major source for carbon , 2003 .

[31]  A. Bekker,et al.  Dating the rise of atmospheric oxygen , 2004, Nature.

[32]  J. Long,et al.  The Greatest Step in Vertebrate History: A Paleobiological Review of the Fish‐Tetrapod Transition* , 2004, Physiological and Biochemical Zoology.

[33]  F. Delsuc,et al.  The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils? , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[34]  W. Martin,et al.  Euglena gracilis Rhodoquinone:Ubiquinone Ratio and Mitochondrial Proteome Differ under Aerobic and Anaerobic Conditions* , 2004, Journal of Biological Chemistry.

[35]  C. Hoppel,et al.  Mitochondrial Oxidative Phosphorylation Is Defective in the Long-lived Mutant clk-1* , 2004, Journal of Biological Chemistry.

[36]  M. Huynen,et al.  An anaerobic mitochondrion that produces hydrogen , 2005, Nature.

[37]  A. Knoll,et al.  Eukaryotic organisms in Proterozoic oceans , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[38]  Miklós Müller Origin of Mitochondria and Hydrogenosomes , 2007 .

[39]  Nicholas H. Putnam,et al.  The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans , 2008, Nature.

[40]  G. Budd The earliest fossil record of the animals and its significance , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[41]  A. Roger,et al.  Supplemental Data Organelles in Blastocystis That Blur the Distinction between Mitochondria and Hydrogenosomes , 2022 .

[42]  K. Tan,et al.  Biochemical characterization of a mitochondrial-like organelle from Blastocystis sp. subtype 7. , 2008, Microbiology.

[43]  David Q. Matus,et al.  Broad phylogenomic sampling improves resolution of the animal tree of life , 2008, Nature.

[44]  Tatjana M. Hildebrandt,et al.  Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and invertebrate mitochondria , 2008, The FEBS journal.

[45]  W. Martin,et al.  Energy metabolism among eukaryotic anaerobes in light of Proterozoic ocean chemistry , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[46]  Anastasios D. Tsaousis,et al.  Localization and functionality of microsporidian iron–sulphur cluster assembly proteins , 2008, Nature.

[47]  M. Ilan,et al.  Oxygen consumption by a coral reef sponge , 2008, Journal of Experimental Biology.

[48]  Philip M. Novack-Gottshall,et al.  Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity , 2009, Proceedings of the National Academy of Sciences.

[49]  M. van der Giezen Hydrogenosomes and Mitosomes: Conservation and Evolution of Functions 1 , 2009, The Journal of eukaryotic microbiology.

[50]  张志峰,et al.  Sulfide-based ATP production in Urechis unicinctus , 2010 .

[51]  E. Koonin,et al.  A late origin of the extant eukaryotic diversity: divergence time estimates using rare genomic changes , 2011, Biology Direct.

[52]  D. Erwin,et al.  Possible animal-body fossils in pre-Marinoan limestones from South Australia , 2010 .

[53]  L. Hug,et al.  Phylogenetic distributions and histories of proteins involved in anaerobic pyruvate metabolism in eukaryotes. , 2010, Molecular biology and evolution.

[54]  D. Erwin,et al.  The Cambrian Conundrum: Early Divergence and Later Ecological Success in the Early History of Animals , 2011, Science.

[55]  D. Newman,et al.  Microaerobic steroid biosynthesis and the molecular fossil record of Archean life , 2011, Proceedings of the National Academy of Sciences.

[56]  A. Roger,et al.  The tangled past of eukaryotic enzymes involved in anaerobic metabolism , 2011, Mobile genetic elements.

[57]  A. Roger,et al.  Eukaryotic pyruvate formate lyase and its activating enzyme were acquired laterally from a Firmicute. , 2011, Molecular biology and evolution.

[58]  Daniel J. G. Lahr,et al.  Estimating the timing of early eukaryotic diversification with multigene molecular clocks , 2011, Proceedings of the National Academy of Sciences.

[59]  A. Knoll The Multiple Origins of Complex Multicellularity , 2011 .

[60]  W. Martin,et al.  Biochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes , 2012, Microbiology and Molecular Reviews.

[61]  M. Clapham,et al.  Environmental and biotic controls on the evolutionary history of insect body size , 2012, Proceedings of the National Academy of Sciences.

[62]  K. Kita,et al.  Crystal structure of mitochondrial quinol-fumarate reductase from the parasitic nematode Ascaris suum. , 2012, Journal of biochemistry.

[63]  L. Katz Origin and diversification of eukaryotes. , 2012, Annual review of microbiology.

[64]  A. Anbar,et al.  Ocean oxygenation in the wake of the Marinoan glaciation , 2012, Nature.

[65]  Molluscs , 2012, Current Biology.

[66]  G. Wörheide,et al.  Novel scenarios of early animal evolution--is it time to rewrite textbooks? , 2013, Integrative and comparative biology.

[67]  S. J. DeCamp My Oldest Sister Is a Sea Walnut ? , 2013 .

[68]  P. Bangalore,et al.  Nearly complete 28S rRNA gene sequences confirm new hypotheses of sponge evolution. , 2013, Integrative and comparative biology.

[69]  M. W. Gray,et al.  Evidence for a Hydrogenosomal-Type Anaerobic ATP Generation Pathway in Acanthamoeba castellanii , 2013, PloS one.

[70]  Nicholas H. Putnam,et al.  The Genome of the Ctenophore Mnemiopsis leidyi and Its Implications for Cell Type Evolution , 2013, Science.

[71]  S. Leys,et al.  The analysis of eight transcriptomes from all poriferan classes reveals surprising genetic complexity in sponges. , 2014, Molecular biology and evolution.

[72]  Victor V. Solovyev,et al.  The Ctenophore Genome and the Evolutionary Origins of Neural Systems , 2014, Nature.

[73]  N. Planavsky,et al.  The rise of oxygen in Earth’s early ocean and atmosphere , 2014, Nature.

[74]  S. Baldauf,et al.  An Alternative Root for the Eukaryote Tree of Life , 2014, Current Biology.

[75]  D. Daffonchio,et al.  Evolution of Mitochondria Reconstructed from the Energy Metabolism of Living Bacteria , 2014, PloS one.

[76]  J. Antcliffe,et al.  Giving the early fossil record of sponges a squeeze , 2014, Biological reviews of the Cambridge Philosophical Society.

[77]  D. Canfield,et al.  Oxygen requirements of the earliest animals , 2014, Proceedings of the National Academy of Sciences.