Pseudomonad reverse carbon catabolite repression, interspecies metabolite exchange, and consortial division of labor
Microorganisms acquire energy and nutrients from dynamic environments, where substrates vary in both type and abundance. The regulatory system responsible for prioritizing preferred substrates is known as carbon catabolite repression (CCR). Two broad classes of CCR have been documented in the litera...
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description | Microorganisms acquire energy and nutrients from dynamic environments, where substrates vary in both type and abundance. The regulatory system responsible for prioritizing preferred substrates is known as carbon catabolite repression (CCR). Two broad classes of CCR have been documented in the literature. The best described CCR strategy, referred to here as classic CCR (cCCR), has been experimentally and theoretically studied using model organisms such as
Escherichia coli
. cCCR phenotypes are often used to generalize universal strategies for fitness, sometimes incorrectly. For instance, extremely competitive microorganisms, such as Pseudomonads, which arguably have broader global distributions than
E. coli
, have achieved their success using metabolic strategies that are nearly opposite of cCCR. These organisms utilize a CCR strategy termed ‘reverse CCR’ (rCCR), because the order of preferred substrates is nearly reverse that of cCCR. rCCR phenotypes prefer organic acids over glucose, may or may not select preferred substrates to optimize growth rates, and do not allocate intracellular resources in a manner that produces an overflow metabolism. cCCR and rCCR have traditionally been interpreted from the perspective of monocultures, even though most microorganisms live in consortia. Here, we review the basic tenets of the two CCR strategies and consider these phenotypes from the perspective of resource acquisition in consortia, a scenario that surely influenced the evolution of cCCR and rCCR. For instance, cCCR and rCCR metabolism are near mirror images of each other; when considered from a consortium basis, the complementary properties of the two strategies can mitigate direct competition for energy and nutrients and instead establish cooperative division of labor. |
doi_str_mv | 10.1007/s00018-019-03377-x |
format | Article |
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Escherichia coli
. cCCR phenotypes are often used to generalize universal strategies for fitness, sometimes incorrectly. For instance, extremely competitive microorganisms, such as Pseudomonads, which arguably have broader global distributions than
E. coli
, have achieved their success using metabolic strategies that are nearly opposite of cCCR. These organisms utilize a CCR strategy termed ‘reverse CCR’ (rCCR), because the order of preferred substrates is nearly reverse that of cCCR. rCCR phenotypes prefer organic acids over glucose, may or may not select preferred substrates to optimize growth rates, and do not allocate intracellular resources in a manner that produces an overflow metabolism. cCCR and rCCR have traditionally been interpreted from the perspective of monocultures, even though most microorganisms live in consortia. Here, we review the basic tenets of the two CCR strategies and consider these phenotypes from the perspective of resource acquisition in consortia, a scenario that surely influenced the evolution of cCCR and rCCR. For instance, cCCR and rCCR metabolism are near mirror images of each other; when considered from a consortium basis, the complementary properties of the two strategies can mitigate direct competition for energy and nutrients and instead establish cooperative division of labor.</description><identifier>ISSN: 1420-682X</identifier><identifier>EISSN: 1420-9071</identifier><identifier>DOI: 10.1007/s00018-019-03377-x</identifier><identifier>PMID: 31768608</identifier><language>eng</language><publisher>Cham: Springer International Publishing</publisher><subject>Biochemistry ; Biomedical and Life Sciences ; Biomedicine ; Business competition ; Carbon ; Carbon - metabolism ; Catabolite repression ; Catabolite Repression - physiology ; Cell Biology ; Consortia ; Division of labor ; E coli ; Escherichia coli - metabolism ; Glucose - metabolism ; Growth rate ; Humans ; Labor ; Life Sciences ; Metabolism ; Metabolites ; Microorganisms ; Monoculture ; Nutrients ; Organic acids ; Overflow ; Phenotype ; Phenotypes ; Pseudomonadaceae - metabolism ; Review ; Substrates</subject><ispartof>Cellular and molecular life sciences : CMLS, 2020-02, Vol.77 (3), p.395-413</ispartof><rights>Springer Nature Switzerland AG 2019</rights><rights>Cellular and Molecular Life Sciences is a copyright of Springer, (2019). All Rights Reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c474t-43e2c5b3858a90a21dcd9e039ae0b72eef8845d22f078a1c273abe9fc98d58cd3</citedby><cites>FETCH-LOGICAL-c474t-43e2c5b3858a90a21dcd9e039ae0b72eef8845d22f078a1c273abe9fc98d58cd3</cites><orcidid>0000-0002-2464-7111</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7015805/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7015805/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27923,27924,41487,42556,51318,53790,53792</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31768608$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Park, Heejoon</creatorcontrib><creatorcontrib>McGill, S. Lee</creatorcontrib><creatorcontrib>Arnold, Adrienne D.</creatorcontrib><creatorcontrib>Carlson, Ross P.</creatorcontrib><title>Pseudomonad reverse carbon catabolite repression, interspecies metabolite exchange, and consortial division of labor</title><title>Cellular and molecular life sciences : CMLS</title><addtitle>Cell. Mol. Life Sci</addtitle><addtitle>Cell Mol Life Sci</addtitle><description>Microorganisms acquire energy and nutrients from dynamic environments, where substrates vary in both type and abundance. The regulatory system responsible for prioritizing preferred substrates is known as carbon catabolite repression (CCR). Two broad classes of CCR have been documented in the literature. The best described CCR strategy, referred to here as classic CCR (cCCR), has been experimentally and theoretically studied using model organisms such as
Escherichia coli
. cCCR phenotypes are often used to generalize universal strategies for fitness, sometimes incorrectly. For instance, extremely competitive microorganisms, such as Pseudomonads, which arguably have broader global distributions than
E. coli
, have achieved their success using metabolic strategies that are nearly opposite of cCCR. These organisms utilize a CCR strategy termed ‘reverse CCR’ (rCCR), because the order of preferred substrates is nearly reverse that of cCCR. rCCR phenotypes prefer organic acids over glucose, may or may not select preferred substrates to optimize growth rates, and do not allocate intracellular resources in a manner that produces an overflow metabolism. cCCR and rCCR have traditionally been interpreted from the perspective of monocultures, even though most microorganisms live in consortia. Here, we review the basic tenets of the two CCR strategies and consider these phenotypes from the perspective of resource acquisition in consortia, a scenario that surely influenced the evolution of cCCR and rCCR. For instance, cCCR and rCCR metabolism are near mirror images of each other; when considered from a consortium basis, the complementary properties of the two strategies can mitigate direct competition for energy and nutrients and instead establish cooperative division of labor.</description><subject>Biochemistry</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Business competition</subject><subject>Carbon</subject><subject>Carbon - metabolism</subject><subject>Catabolite repression</subject><subject>Catabolite Repression - physiology</subject><subject>Cell Biology</subject><subject>Consortia</subject><subject>Division of labor</subject><subject>E coli</subject><subject>Escherichia coli - metabolism</subject><subject>Glucose - metabolism</subject><subject>Growth rate</subject><subject>Humans</subject><subject>Labor</subject><subject>Life Sciences</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Microorganisms</subject><subject>Monoculture</subject><subject>Nutrients</subject><subject>Organic acids</subject><subject>Overflow</subject><subject>Phenotype</subject><subject>Phenotypes</subject><subject>Pseudomonadaceae - metabolism</subject><subject>Review</subject><subject>Substrates</subject><issn>1420-682X</issn><issn>1420-9071</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNp9kc2OFCEUhYnROOPoC7gwJG5cTOkFqhrYmEwmOppMogtN3BEKbs0wqYIWqjrt20vbPe3PwtUlOd85cDmEPGfwmgHINwUAmGqA6QaEkLLZPiCnrOXQaJDs4eG8UvzbCXlSyl2lO8VXj8mJYHKlVqBOyfy54OLTlKL1NOMGc0HqbO5TrGO2fRrDjFVZZywlpHhOQ5wrtUYXsNAJjwxu3a2NN3hObfTUpVhSnoMdqQ-bsLPSNNCx0vkpeTTYseCzwzwjX9-_-3L5obn-dPXx8uK6ca1s56YVyF3XC9Upq8Fy5p3XCEJbhF5yxEGptvOcDyCVZY5LYXvUg9PKd8p5cUbe7nPXSz-hdxjnbEezzmGy-YdJNpi_lRhuzU3aGLn7KehqwKtDQE7fFyyzmUJxOI42YlqK4YIpybVud-jLf9C7tORY16tUx5WWnWaV4nvK5VRKxuH4GAZmV6rZl2pqqeZXqWZbTS_-XONouW-xAmIPlCrVBvLvu_8T-xOSzLGS</recordid><startdate>20200201</startdate><enddate>20200201</enddate><creator>Park, Heejoon</creator><creator>McGill, S. 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Lee</au><au>Arnold, Adrienne D.</au><au>Carlson, Ross P.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Pseudomonad reverse carbon catabolite repression, interspecies metabolite exchange, and consortial division of labor</atitle><jtitle>Cellular and molecular life sciences : CMLS</jtitle><stitle>Cell. Mol. Life Sci</stitle><addtitle>Cell Mol Life Sci</addtitle><date>2020-02-01</date><risdate>2020</risdate><volume>77</volume><issue>3</issue><spage>395</spage><epage>413</epage><pages>395-413</pages><issn>1420-682X</issn><eissn>1420-9071</eissn><abstract>Microorganisms acquire energy and nutrients from dynamic environments, where substrates vary in both type and abundance. The regulatory system responsible for prioritizing preferred substrates is known as carbon catabolite repression (CCR). Two broad classes of CCR have been documented in the literature. The best described CCR strategy, referred to here as classic CCR (cCCR), has been experimentally and theoretically studied using model organisms such as
Escherichia coli
. cCCR phenotypes are often used to generalize universal strategies for fitness, sometimes incorrectly. For instance, extremely competitive microorganisms, such as Pseudomonads, which arguably have broader global distributions than
E. coli
, have achieved their success using metabolic strategies that are nearly opposite of cCCR. These organisms utilize a CCR strategy termed ‘reverse CCR’ (rCCR), because the order of preferred substrates is nearly reverse that of cCCR. rCCR phenotypes prefer organic acids over glucose, may or may not select preferred substrates to optimize growth rates, and do not allocate intracellular resources in a manner that produces an overflow metabolism. cCCR and rCCR have traditionally been interpreted from the perspective of monocultures, even though most microorganisms live in consortia. Here, we review the basic tenets of the two CCR strategies and consider these phenotypes from the perspective of resource acquisition in consortia, a scenario that surely influenced the evolution of cCCR and rCCR. For instance, cCCR and rCCR metabolism are near mirror images of each other; when considered from a consortium basis, the complementary properties of the two strategies can mitigate direct competition for energy and nutrients and instead establish cooperative division of labor.</abstract><cop>Cham</cop><pub>Springer International Publishing</pub><pmid>31768608</pmid><doi>10.1007/s00018-019-03377-x</doi><tpages>19</tpages><orcidid>https://orcid.org/0000-0002-2464-7111</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Biochemistry Biomedical and Life Sciences Biomedicine Business competition Carbon Carbon - metabolism Catabolite repression Catabolite Repression - physiology Cell Biology Consortia Division of labor E coli Escherichia coli - metabolism Glucose - metabolism Growth rate Humans Labor Life Sciences Metabolism Metabolites Microorganisms Monoculture Nutrients Organic acids Overflow Phenotype Phenotypes Pseudomonadaceae - metabolism Review Substrates |
title | Pseudomonad reverse carbon catabolite repression, interspecies metabolite exchange, and consortial division of labor |
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