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Opposing Pressures of Speed and Efficiency Guide the Evolution of Molecular Machines
Abstract Many biomolecular machines need to be both fast and efficient. How has evolution optimized these machines along the tradeoff between speed and efficiency? We explore this question using optimizable dynamical models along coordinates that are plausible evolutionary degrees of freedom. Data o...
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| Published in: | Molecular biology and evolution 2019-12, Vol.36 (12), p.2813-2822 |
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| Main Authors: | , |
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| Language: | English |
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| cites | cdi_FETCH-LOGICAL-c486t-5ca77d00d304b28c69f8aa6d2628df6e88f6da793dd52e4f0d4a420e857c79a3 |
| container_end_page | 2822 |
| container_issue | 12 |
| container_start_page | 2813 |
| container_title | Molecular biology and evolution |
| container_volume | 36 |
| creator | Wagoner, Jason A Dill, Ken A |
| description | Abstract
Many biomolecular machines need to be both fast and efficient. How has evolution optimized these machines along the tradeoff between speed and efficiency? We explore this question using optimizable dynamical models along coordinates that are plausible evolutionary degrees of freedom. Data on 11 motors and ion pumps are consistent with the hypothesis that evolution seeks an optimal balance of speed and efficiency, where any further small increase in one of these quantities would come at great expense to the other. For FoF1-ATPases in different species, we also find apparent optimization of the number of subunits in the c-ring, which determines the number of protons pumped per ATP synthesized. Interestingly, these ATPases appear to more optimized for efficiency than for speed, which can be rationalized through their key role as energy transducers in biology. The present modeling shows how the dynamical performance properties of biomolecular motors and pumps may have evolved to suit their corresponding biological actions. |
| doi_str_mv | 10.1093/molbev/msz190 |
| format | article |
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Many biomolecular machines need to be both fast and efficient. How has evolution optimized these machines along the tradeoff between speed and efficiency? We explore this question using optimizable dynamical models along coordinates that are plausible evolutionary degrees of freedom. Data on 11 motors and ion pumps are consistent with the hypothesis that evolution seeks an optimal balance of speed and efficiency, where any further small increase in one of these quantities would come at great expense to the other. For FoF1-ATPases in different species, we also find apparent optimization of the number of subunits in the c-ring, which determines the number of protons pumped per ATP synthesized. Interestingly, these ATPases appear to more optimized for efficiency than for speed, which can be rationalized through their key role as energy transducers in biology. The present modeling shows how the dynamical performance properties of biomolecular motors and pumps may have evolved to suit their corresponding biological actions.</description><identifier>ISSN: 0737-4038</identifier><identifier>EISSN: 1537-1719</identifier><identifier>DOI: 10.1093/molbev/msz190</identifier><identifier>PMID: 31432071</identifier><language>eng</language><publisher>United States: Oxford University Press</publisher><subject>Animals ; Discoveries ; Evolution, Molecular ; Models, Biological ; Proton-Translocating ATPases - metabolism</subject><ispartof>Molecular biology and evolution, 2019-12, Vol.36 (12), p.2813-2822</ispartof><rights>The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution 2019</rights><rights>The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c486t-5ca77d00d304b28c69f8aa6d2628df6e88f6da793dd52e4f0d4a420e857c79a3</citedby><cites>FETCH-LOGICAL-c486t-5ca77d00d304b28c69f8aa6d2628df6e88f6da793dd52e4f0d4a420e857c79a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6878954/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6878954/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,1603,27923,27924,53790,53792</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31432071$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wagoner, Jason A</creatorcontrib><creatorcontrib>Dill, Ken A</creatorcontrib><title>Opposing Pressures of Speed and Efficiency Guide the Evolution of Molecular Machines</title><title>Molecular biology and evolution</title><addtitle>Mol Biol Evol</addtitle><description>Abstract
Many biomolecular machines need to be both fast and efficient. How has evolution optimized these machines along the tradeoff between speed and efficiency? We explore this question using optimizable dynamical models along coordinates that are plausible evolutionary degrees of freedom. Data on 11 motors and ion pumps are consistent with the hypothesis that evolution seeks an optimal balance of speed and efficiency, where any further small increase in one of these quantities would come at great expense to the other. For FoF1-ATPases in different species, we also find apparent optimization of the number of subunits in the c-ring, which determines the number of protons pumped per ATP synthesized. Interestingly, these ATPases appear to more optimized for efficiency than for speed, which can be rationalized through their key role as energy transducers in biology. The present modeling shows how the dynamical performance properties of biomolecular motors and pumps may have evolved to suit their corresponding biological actions.</description><subject>Animals</subject><subject>Discoveries</subject><subject>Evolution, Molecular</subject><subject>Models, Biological</subject><subject>Proton-Translocating ATPases - metabolism</subject><issn>0737-4038</issn><issn>1537-1719</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><recordid>eNqFkc1LxDAQxYMoun4cvUqOXqpJkybpRRBZP0BZwb2HbDJxI21Tm3ZB_3orq6uevMwMzI_3hnkIHVNyRknJzutYLWB1Xqd3WpItNKEFkxmVtNxGEyLHmROm9tB-Si-EUM6F2EV7jHKWE0knaD5r25hC84wfO0hpGAuOHj-1AA6bxuGp98EGaOwbvhmCA9wvAU9XsRr6EJtP9iFWYIfKdPjB2GVoIB2iHW-qBEdf_QDNr6fzq9vsfnZzd3V5n1muRJ8V1kjpCHGM8EWurCi9Mka4XOTKeQFKeeGMLJlzRQ7cE8cNzwmoQlpZGnaALtay7bCowVlo-s5Uuu1Cbbo3HU3QfzdNWOrnuNJCSVUWfBQ4_RLo4usAqdd1SBaqyjQQh6RzRpVkRJZkRLM1aruYUgd-Y0OJ_gxCr4PQ6yBG_uT3bRv6-_M_3nFo_9H6AJ2_li0</recordid><startdate>20191201</startdate><enddate>20191201</enddate><creator>Wagoner, Jason A</creator><creator>Dill, Ken A</creator><general>Oxford University Press</general><scope>TOX</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20191201</creationdate><title>Opposing Pressures of Speed and Efficiency Guide the Evolution of Molecular Machines</title><author>Wagoner, Jason A ; Dill, Ken A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c486t-5ca77d00d304b28c69f8aa6d2628df6e88f6da793dd52e4f0d4a420e857c79a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animals</topic><topic>Discoveries</topic><topic>Evolution, Molecular</topic><topic>Models, Biological</topic><topic>Proton-Translocating ATPases - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wagoner, Jason A</creatorcontrib><creatorcontrib>Dill, Ken A</creatorcontrib><collection>Open Access: Oxford University Press Open Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular biology and evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wagoner, Jason A</au><au>Dill, Ken A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Opposing Pressures of Speed and Efficiency Guide the Evolution of Molecular Machines</atitle><jtitle>Molecular biology and evolution</jtitle><addtitle>Mol Biol Evol</addtitle><date>2019-12-01</date><risdate>2019</risdate><volume>36</volume><issue>12</issue><spage>2813</spage><epage>2822</epage><pages>2813-2822</pages><issn>0737-4038</issn><eissn>1537-1719</eissn><abstract>Abstract
Many biomolecular machines need to be both fast and efficient. How has evolution optimized these machines along the tradeoff between speed and efficiency? We explore this question using optimizable dynamical models along coordinates that are plausible evolutionary degrees of freedom. Data on 11 motors and ion pumps are consistent with the hypothesis that evolution seeks an optimal balance of speed and efficiency, where any further small increase in one of these quantities would come at great expense to the other. For FoF1-ATPases in different species, we also find apparent optimization of the number of subunits in the c-ring, which determines the number of protons pumped per ATP synthesized. Interestingly, these ATPases appear to more optimized for efficiency than for speed, which can be rationalized through their key role as energy transducers in biology. The present modeling shows how the dynamical performance properties of biomolecular motors and pumps may have evolved to suit their corresponding biological actions.</abstract><cop>United States</cop><pub>Oxford University Press</pub><pmid>31432071</pmid><doi>10.1093/molbev/msz190</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Molecular biology and evolution, 2019-12, Vol.36 (12), p.2813-2822 |
| issn | 0737-4038 1537-1719 |
| language | eng |
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| source | Open Access: PubMed Central; Open Access: Oxford University Press Open Journals; Full-Text Journals in Chemistry (Open access) |
| subjects | Animals Discoveries Evolution, Molecular Models, Biological Proton-Translocating ATPases - metabolism |
| title | Opposing Pressures of Speed and Efficiency Guide the Evolution of Molecular Machines |
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