Potential Role of Acetyl-CoA Synthetase (acs) and Malate Dehydrogenase (mae) in the Evolution of the Acetate Switch in Bacteria and Archaea

Barnhart, Elliott P.; McClure, Marcella A.; Johnson, Kiki; Cleveland, Sean; Hunt, Kristopher A.; Fields, Matthew W.

doi:10.1038/srep12498

Title: Potential Role of Acetyl-CoA Synthetase (acs) and Malate Dehydrogenase (mae) in the Evolution of the Acetate Switch in Bacteria and Archaea

Journal Article · Mon Aug 03 00:00:00 EDT 2015 · Scientific Reports

DOI:https://doi.org/10.1038/srep12498· OSTI ID:1256055

Barnhart, Elliott P. ^[1]; McClure, Marcella A. ^[2]; Johnson, Kiki ^[2]; Cleveland, Sean ^[2]; Hunt, Kristopher A. ^[2]; Fields, Matthew W. ^[3]

Montana State Univ., Bozeman, MT (United States); US Geological Survey, Helena, MT (United States)
Montana State Univ., Bozeman, MT (United States)
Montana State Univ., Bozeman, MT (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). ENIGMA; National Center for Genome Resources, Santa Fe, NM (United States)

Although many Archaea have AMP-Acs (acetyl-coenzyme A synthetase) and ADP-Acs, the extant methanogenic genus Methanosarcina is the only identified Archaeal genus that can utilize acetate via acetate kinase (Ack) and phosphotransacetylase (Pta). Despite the importance of ack as the potential urkinase in the ASKHA phosphotransferase superfamily, an origin hypothesis does not exist for the acetate kinase in Bacteria, Archaea, or Eukarya. Here we demonstrate that Archaeal AMP-Acs and ADP-Acs contain paralogous ATPase motifs previously identified in Ack, which demonstrate a novel relation between these proteins in Archaea. The identification of ATPase motif conservation and resulting structural features in AMP- and ADP-acetyl-CoA synthetase proteins in this study expand the ASKHA superfamily to include acetyl-CoA synthetase. Additional phylogenetic analysis showed that Pta and MaeB sequences had a common ancestor, and that the Pta lineage within the halophilc archaea was an ancestral lineage. Lastly, these results suggested that divergence of a duplicated maeB within an ancient halophilic, archaeal lineage formed a putative pta ancestor. These results provide a potential scenario for the establishment of the Ack/Pta pathway and provide novel insight into the evolution of acetate metabolism for all three domains of life.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; FC26-04NT42262

OSTI ID:: 1256055

Journal Information:: Scientific Reports, Vol. 5; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 5 works

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References (58)

The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools Thompson, J. Nucleic Acids Research, Vol. 25, Issue 24 https://doi.org/10.1093/nar/25.24.4876	journal	December 1997
Evolution of Acetoclastic Methanogenesis in Methanosarcina via Horizontal Gene Transfer from Cellulolytic Clostridia Fournier, G. P.; Gogarten, J. P. Journal of Bacteriology, Vol. 190, Issue 3 https://doi.org/10.1128/JB.01382-07	journal	November 2007
The rocky roots of the acetyl-CoA pathway Russell, Michael J.; Martin, William Trends in Biochemical Sciences, Vol. 29, Issue 7 https://doi.org/10.1016/j.tibs.2004.05.007	journal	July 2004
Higher-level classification of the Archaea: evolution of methanogenesis and methanogens Bapteste, Éric; Brochier, Céline; Boucher, Yan Archaea, Vol. 1, Issue 5 https://doi.org/10.1155/2005/859728	journal	January 2005
Control of carbon flux through enzymes of central and intermediary metabolism during growth of Escherichia coli on acetate El-Mansi, Mansi; Cozzone, Alain J.; Shiloach, Joseph Current Opinion in Microbiology, Vol. 9, Issue 2 https://doi.org/10.1016/j.mib.2006.02.002	journal	April 2006
Protein homology detection by HMM-HMM comparison Soding, J. Bioinformatics, Vol. 21, Issue 7 https://doi.org/10.1093/bioinformatics/bti125	journal	November 2004
Acetyl-CoA Synthetase from the Amitochondriate Eukaryote Giardia lamblia Belongs to the Newly Recognized Superfamily of Acyl-CoA Synthetases (Nucleoside Diphosphate-forming) Sánchez, Lidya B.; Galperin, Michael Y.; Müller, Miklós Journal of Biological Chemistry, Vol. 275, Issue 8 https://doi.org/10.1074/jbc.275.8.5794	journal	February 2000
Sequence and Structure Classification of Kinases Cheek, Sara; Zhang, Hong; Grishin, Nick V. Journal of Molecular Biology, Vol. 320, Issue 4 https://doi.org/10.1016/S0022-2836(02)00538-7	journal	July 2002
High level of intergenera gene exchange shapes the evolution of haloarchaea in an isolated Antarctic lake DeMaere, M. Z.; Williams, T. J.; Allen, M. A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 42 https://doi.org/10.1073/pnas.1307090110	journal	September 2013
How to Make a Living by Exhaling Methane Ferry, James G. Annual Review of Microbiology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev.micro.112408.134051	journal	October 2010
An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. Bork, P.; Sander, C.; Valencia, A. Proceedings of the National Academy of Sciences, Vol. 89, Issue 16 https://doi.org/10.1073/pnas.89.16.7290	journal	August 1992
Acetyl Coenzyme A Synthetase (ADP Forming) from the Hyperthermophilic Archaeon Pyrococcus furiosus: Identification, Cloning, Separate Expression of the Encoding Genes,acdAI and acdBI, in Escherichia coli, and In Vitro Reconstitution of the Active Heterotetrameric Enzyme from Its Recombinant Subunits Musfeldt, Meike; Selig, Martina; Schönheit, Peter Journal of Bacteriology, Vol. 181, Issue 18 https://doi.org/10.1128/JB.181.18.5885-5888.1999	journal	September 1999
Evidence from fluid inclusions for microbial methanogenesis in the early Archaean era Ueno, Yuichiro; Yamada, Keita; Yoshida, Naohiro Nature, Vol. 440, Issue 7083 https://doi.org/10.1038/nature04584	journal	March 2006
BEAST: Bayesian evolutionary analysis by sampling trees Drummond, Alexei J.; Rambaut, Andrew BMC Evolutionary Biology, Vol. 7, Issue 1 https://doi.org/10.1186/1471-2148-7-214	journal	January 2007
A detailed structural description of Escherichia coli succinyl-CoA synthetase 1 1Edited by D. Rees Fraser, Marie E.; James, Michael N. G.; Bridger, William A. Journal of Molecular Biology, Vol. 285, Issue 4 https://doi.org/10.1006/jmbi.1998.2324	journal	January 1999
Acetoclastic and hydrogenotrophic methane production and methanogenic populations in an acidic West-Siberian peat bog Kotsyurbenko, Oleg R.; Chin, Kuk-Jeong; Glagolev, Mikhail V. Environmental Microbiology, Vol. 6, Issue 11 https://doi.org/10.1111/j.1462-2920.2004.00634.x	journal	November 2004
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
The HHpred interactive server for protein homology detection and structure prediction Soding, J.; Biegert, A.; Lupas, A. N. Nucleic Acids Research, Vol. 33, Issue Web Server https://doi.org/10.1093/nar/gki408	journal	July 2005
Sir2-Dependent Activation of Acetyl-CoA Synthetase by Deacetylation of Active Lysine Starai, V. J.; Celic, I.; Cole, R. N. Science, Vol. 298, Issue 5602, p. 2390-2392 https://doi.org/10.1126/science.1077650	journal	December 2002
An Ancient Pathway Combining Carbon Dioxide Fixation with the Generation and Utilization of a Sodium Ion Gradient for ATP Synthesis Poehlein, Anja; Schmidt, Silke; Kaster, Anne-Kristin PLoS ONE, Vol. 7, Issue 3 https://doi.org/10.1371/journal.pone.0033439	journal	March 2012
Rapid evolutionary innovation during an Archaean genetic expansion David, Lawrence A.; Alm, Eric J. Nature, Vol. 469, Issue 7328 https://doi.org/10.1038/nature09649	journal	December 2010
Archaeal genetics — the third way Allers, Thorsten; Mevarech, Moshe Nature Reviews Genetics, Vol. 6, Issue 1 https://doi.org/10.1038/nrg1504	journal	January 2005
The 1.75 Å Crystal Structure of Acetyl-CoA Synthetase Bound to Adenosine-5‘-propylphosphate and Coenzyme A ^† Gulick, Andrew M.; Starai, Vincent J.; Horswill, Alexander R. Biochemistry, Vol. 42, Issue 10, p. 2866-2873 https://doi.org/10.1021/bi0271603	journal	March 2003
Structural and mechanistic investigations on Salmonella typhimurium acetate kinase (AckA): identification of a putative ligand binding pocket at the dimeric interface Chittori, Sagar; Savithri, Handanahal S.; Murthy, Mathur RN BMC Structural Biology, Vol. 12, Issue 1 https://doi.org/10.1186/1472-6807-12-24	journal	January 2012
Evidence from phylogenetic and genome fingerprinting analyses suggests rapidly changing variation in Halorubrum and Haloarcula populations Ram Mohan, Nikhil; Fullmer, Matthew S.; Makkay, Andrea M. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00143	journal	April 2014
Contribution of anthropogenic and natural sources to atmospheric methane variability Bousquet, P.; Ciais, P.; Miller, J. B. Nature, Vol. 443, Issue 7110 https://doi.org/10.1038/nature05132	journal	September 2006
The Jpred 3 secondary structure prediction server Cole, C.; Barber, J. D.; Barton, G. J. Nucleic Acids Research, Vol. 36, Issue Web Server https://doi.org/10.1093/nar/gkn238	journal	May 2008
Unusual ADP-forming acetyl-coenzyme A synthetases from the mesophilic halophilic euryarchaeon Haloarcula marismortui and from the hyperthermophilic crenarchaeon Pyrobaculum aerophilum Br�sen, Christopher; Sch�nheit, Peter Archives of Microbiology, Vol. 182, Issue 4 https://doi.org/10.1007/s00203-004-0702-4	journal	August 2004
Paleophysiology and end-Permian mass extinction Knoll, Andrew H.; Bambach, Richard K.; Payne, Jonathan L. Earth and Planetary Science Letters, Vol. 256, Issue 3-4 https://doi.org/10.1016/j.epsl.2007.02.018	journal	April 2007
Acetate kinase: not just a bacterial enzyme Ingram-Smith, Cheryl; Martin, Stephen R.; Smith, Kerry S. Trends in Microbiology, Vol. 14, Issue 6 https://doi.org/10.1016/j.tim.2006.04.001	journal	June 2006
Urkinase: Structure of Acetate Kinase, a Member of the ASKHA Superfamily of Phosphotransferases Buss, Kathryn A.; Cooper, David R.; Ingram-Smith, Cheryl Journal of Bacteriology, Vol. 183, Issue 2 https://doi.org/10.1128/JB.183.2.680-686.2001	journal	January 2001
The Stepwise Evolution of Early Life Driven by Energy Conservation Ferry, J. G. Molecular Biology and Evolution, Vol. 23, Issue 6 https://doi.org/10.1093/molbev/msk014	journal	March 2006
Acetyl-coenzyme A synthetase (AMP forming) Starai, V. J.; Escalante-Semerena, J. C. Cellular and Molecular Life Sciences, Vol. 61, Issue 16 https://doi.org/10.1007/s00018-004-3448-x	journal	August 2004
Three decades of global methane sources and sinks Kirschke, Stefanie; Bousquet, Philippe; Ciais, Philippe Nature Geoscience, Vol. 6, Issue 10 https://doi.org/10.1038/ngeo1955	journal	September 2013
Explosive eruption of coal and basalt and the end-Permian mass extinction Ogden, D. E.; Sleep, N. H. Proceedings of the National Academy of Sciences, Vol. 109, Issue 1 https://doi.org/10.1073/pnas.1118675109	journal	December 2011
Methane from acetate. Ferry, J. G. Journal of Bacteriology, Vol. 174, Issue 17 https://doi.org/10.1128/jb.174.17.5489-5495.1992	journal	September 1992
Reaction Mechanism and Structural Model of ADP-forming Acetyl-CoA Synthetase from the Hyperthermophilic Archaeon Pyrococcus furiosus: EVIDENCE FOR A SECOND ACTIVE SITE HISTIDINE RESIDUE Bräsen, Christopher; Schmidt, Marcel; Grötzinger, Joachim Journal of Biological Chemistry, Vol. 283, Issue 22 https://doi.org/10.1074/jbc.M710218200	journal	March 2008
Trace Metal Requirements for Microbial Enzymes Involved in the Production and Consumption of Methane and Nitrous Oxide Glass, Jennifer B.; Orphan, Victoria J. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00061	journal	January 2012
Jalview Version 2--a multiple sequence alignment editor and analysis workbench Waterhouse, A. M.; Procter, J. B.; Martin, D. M. A. Bioinformatics, Vol. 25, Issue 9 https://doi.org/10.1093/bioinformatics/btp033	journal	January 2009
Evaluation of the emission characteristics of trace metals from coal and fuel oil fired power plants and their fate during combustion Reddy, M. Srinivasa; Basha, Shaik; Joshi, H. V. Journal of Hazardous Materials, Vol. 123, Issue 1-3 https://doi.org/10.1016/j.jhazmat.2005.04.008	journal	August 2005
Evolutionary primacy of sodium bioenergetics Mulkidjanian, Armen Y.; Galperin, Michael Y.; Makarova, Kira S. Biology Direct, Vol. 3, Issue 1 https://doi.org/10.1186/1745-6150-3-13	journal	January 2008
Methanogenic burst in the end-Permian carbon cycle Rothman, D. H.; Fournier, G. P.; French, K. L. Proceedings of the National Academy of Sciences, Vol. 111, Issue 15 https://doi.org/10.1073/pnas.1318106111	journal	March 2014
Gene synteny and evolution of genome architecture in trypanosomatids Ghedin, Elodie; Bringaud, Frederic; Peterson, Jeremy Molecular and Biochemical Parasitology, Vol. 134, Issue 2 https://doi.org/10.1016/j.molbiopara.2003.11.012	journal	April 2004
Molecular phylogenetics: state-of-the-art methods for looking into the past Whelan, Simon; Liò, Pietro; Goldman, Nick Trends in Genetics, Vol. 17, Issue 5 https://doi.org/10.1016/s0168-9525(01)02272-7	journal	May 2001
Physiological Ecology of Methanogens Zinder, Stephen H. Methanogenesis https://doi.org/10.1007/978-1-4615-2391-8_4	book	January 1993
Kinetics of Acetate Utilization by Two Thermophilic Acetotrophic Methanogens: Methanosarcina sp. Strain CALS-1 and Methanothrix sp. Strain CALS-1 Min, Hang; Zinder, Stephen H. Applied and Environmental Microbiology, Vol. 55, Issue 2 https://doi.org/10.1128/aem.55.2.488-491.1989	journal	January 1989
The Role of Histidines in the Acetate Kinase from Methanosarcina thermophila Ingram-Smith, Cheryl; Barber, Robert D.; Ferry, James G. Journal of Biological Chemistry, Vol. 275, Issue 43 https://doi.org/10.1074/jbc.m005303200	journal	August 2000
Cycles in fossil diversity Rohde, Robert A.; Muller, Richard A. Nature, Vol. 434, Issue 7030 https://doi.org/10.1038/nature03339	journal	March 2005
Transmission of Creutzfeldt-Jakob disease from man to the guinea pig Manuelidis, E. Science, Vol. 190, Issue 4214 https://doi.org/10.1126/science.1103289	journal	November 1975
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Cooperation and Competition in the Evolution of ATP-Producing Pathways Pfeiffer, T.; Schuster, S.; Bonhoeffer, S. Science, Vol. 292, Issue 5516 https://doi.org/10.1126/science.1058079	journal	April 2001
Structural and Functional Studies Suggest a Catalytic Mechanism for the Phosphotransacetylase from Methanosarcina thermophila Lawrence, S. H.; Luther, K. B.; Schindelin, H. Journal of Bacteriology, Vol. 188, Issue 3 https://doi.org/10.1128/jb.188.3.1143-1154.2006	journal	January 2006
Steady-State Kinetic Analysis of Phosphotransacetylase from Methanosarcina thermophila Lawrence, Sarah H.; Ferry, James G. Journal of Bacteriology, Vol. 188, Issue 3 https://doi.org/10.1128/jb.188.3.1155-1158.2006	journal	February 2006
Energetics of syntrophic cooperation in methanogenic degradation. Schink, B. Microbiology and molecular biology reviews : MMBR, Vol. 61, Issue 2 https://doi.org/10.1128/.61.2.262-280.1997	journal	January 1997
The Acetate Switch Wolfe, Alan Microbiology and Molecular Biology Reviews, Vol. 69, Issue 1, p. 12-50 https://doi.org/10.1128/MMBR.69.1.12-50.2005	journal	March 2005
Overflow Metabolism in Escherichia coli during Steady-State Growth: Transcriptional Regulation and Effect of the Redox Ratio Vemuri, G. N.; Altman, E.; Sangurdekar, D. P. Applied and Environmental Microbiology, Vol. 72, Issue 5 https://doi.org/10.1128/AEM.72.5.3653-3661.2006	journal	May 2006
Escherichia coli Malic Enzymes: Two Isoforms with Substantial Differences in Kinetic Properties, Metabolic Regulation, and Structure Bologna, F. P.; Andreo, C. S.; Drincovich, M. F. Journal of Bacteriology, Vol. 189, Issue 16 https://doi.org/10.1128/JB.00428-07	journal	June 2007
Crystal structures of acetate kinases from the eukaryotic pathogens Entamoeba histolytica and Cryptococcus neoformans Thaker, Tarjani M.; Tanabe, Mikio; Fowler, Matthew L. Journal of Structural Biology, Vol. 181, Issue 2 https://doi.org/10.1016/j.jsb.2012.11.001	journal	February 2013

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