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Molecular insights into the ecology of a psychrotolerant Pseudomonas syringae
Summary Low temperatures constrain cellular life due to reductions in nutrient uptake, enzyme kinetics, membrane permeability, and function of other biomacromolecules. This has implications for the biophysical limits of life on Earth, and the plausibility of life in extraterrestrial locations. Altho...
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Published in: | Environmental microbiology 2021-07, Vol.23 (7), p.3665-3681 |
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creator | Pavankumar, Theetha L. Mittal, Pragya Hallsworth, John E. |
description | Summary
Low temperatures constrain cellular life due to reductions in nutrient uptake, enzyme kinetics, membrane permeability, and function of other biomacromolecules. This has implications for the biophysical limits of life on Earth, and the plausibility of life in extraterrestrial locations. Although most pseudomonads are mesophilic in nature, isolates such as the Antarctic Pseudomonas syringae Lz4W exhibit considerable psychrotolerance, with an ability to grow even between 4 and 0°C. In this review, we explore the molecular traits and characteristic phenotypes of P. syringae Lz4W that enable life at low temperatures. We describe adaptations that enhance membrane fluidity; examine genes involved in cellular function and survival in the cold; assess capability for energy generation at low temperature; and detail the mechanics of DNA repair and RNA processing at low temperature, and speculate that P. syringae Lz4W can also synthesize glycerol to maintain flexibility of macromolecular systems. In the range 4 to 0ºC, there are considerable changes in the properties and behaviour of water. Specifically, density can have adverse impacts on plasma‐membrane functions, cytoplasmic viscosity, protein behaviour, and other essential properties of cellular system. We identified a combination of adaptations that may be peculiar to cold‐tolerant P. syringae, including increase of unsaturated fatty acids in the plasma membrane; a RNA polymerase able to function at 0°C; RecBCD‐ and RuvAB‐dependent reestablishment of replication fork; and efficiencies of degradosome machinery and RNA processing by RNaseR at low temperature. Several unresolved questions are discussed in the context of astrobiology, and further work needed on the psychrotolerance of P. syringae. |
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Low temperatures constrain cellular life due to reductions in nutrient uptake, enzyme kinetics, membrane permeability, and function of other biomacromolecules. This has implications for the biophysical limits of life on Earth, and the plausibility of life in extraterrestrial locations. Although most pseudomonads are mesophilic in nature, isolates such as the Antarctic Pseudomonas syringae Lz4W exhibit considerable psychrotolerance, with an ability to grow even between 4 and 0°C. In this review, we explore the molecular traits and characteristic phenotypes of P. syringae Lz4W that enable life at low temperatures. We describe adaptations that enhance membrane fluidity; examine genes involved in cellular function and survival in the cold; assess capability for energy generation at low temperature; and detail the mechanics of DNA repair and RNA processing at low temperature, and speculate that P. syringae Lz4W can also synthesize glycerol to maintain flexibility of macromolecular systems. In the range 4 to 0ºC, there are considerable changes in the properties and behaviour of water. Specifically, density can have adverse impacts on plasma‐membrane functions, cytoplasmic viscosity, protein behaviour, and other essential properties of cellular system. We identified a combination of adaptations that may be peculiar to cold‐tolerant P. syringae, including increase of unsaturated fatty acids in the plasma membrane; a RNA polymerase able to function at 0°C; RecBCD‐ and RuvAB‐dependent reestablishment of replication fork; and efficiencies of degradosome machinery and RNA processing by RNaseR at low temperature. Several unresolved questions are discussed in the context of astrobiology, and further work needed on the psychrotolerance of P. syringae.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.15304</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Adaptation ; Astrobiology ; Deoxyribonucleic acid ; DNA ; DNA repair ; DNA-directed RNA polymerase ; Enzyme kinetics ; Extraterrestrial life ; Extraterrestrial materials ; Fatty acids ; Fluidity ; Genes ; Glycerol ; Kinetics ; Low temperature ; Macromolecules ; Mechanics ; Membrane fluidity ; Membrane permeability ; Membrane proteins ; Membranes ; Nucleic acids ; Nutrient uptake ; Permeability ; Phenotypes ; Properties ; Pseudomonas ; Pseudomonas syringae ; Ribonucleic acid ; RNA ; RNA polymerase ; RNA processing ; Survival ; Temperature ; Uptake ; Viscosity</subject><ispartof>Environmental microbiology, 2021-07, Vol.23 (7), p.3665-3681</ispartof><rights>2020 Society for Applied Microbiology and John Wiley & Sons Ltd</rights><rights>2021 Society for Applied Microbiology and John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3894-3689ad8dec4337adcfa8e826bf47b818fab4e421876064afb538f631760249023</citedby><cites>FETCH-LOGICAL-c3894-3689ad8dec4337adcfa8e826bf47b818fab4e421876064afb538f631760249023</cites><orcidid>0000-0001-6797-9362 ; 0000-0003-1845-9592</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids></links><search><creatorcontrib>Pavankumar, Theetha L.</creatorcontrib><creatorcontrib>Mittal, Pragya</creatorcontrib><creatorcontrib>Hallsworth, John E.</creatorcontrib><title>Molecular insights into the ecology of a psychrotolerant Pseudomonas syringae</title><title>Environmental microbiology</title><description>Summary
Low temperatures constrain cellular life due to reductions in nutrient uptake, enzyme kinetics, membrane permeability, and function of other biomacromolecules. This has implications for the biophysical limits of life on Earth, and the plausibility of life in extraterrestrial locations. Although most pseudomonads are mesophilic in nature, isolates such as the Antarctic Pseudomonas syringae Lz4W exhibit considerable psychrotolerance, with an ability to grow even between 4 and 0°C. In this review, we explore the molecular traits and characteristic phenotypes of P. syringae Lz4W that enable life at low temperatures. We describe adaptations that enhance membrane fluidity; examine genes involved in cellular function and survival in the cold; assess capability for energy generation at low temperature; and detail the mechanics of DNA repair and RNA processing at low temperature, and speculate that P. syringae Lz4W can also synthesize glycerol to maintain flexibility of macromolecular systems. In the range 4 to 0ºC, there are considerable changes in the properties and behaviour of water. Specifically, density can have adverse impacts on plasma‐membrane functions, cytoplasmic viscosity, protein behaviour, and other essential properties of cellular system. We identified a combination of adaptations that may be peculiar to cold‐tolerant P. syringae, including increase of unsaturated fatty acids in the plasma membrane; a RNA polymerase able to function at 0°C; RecBCD‐ and RuvAB‐dependent reestablishment of replication fork; and efficiencies of degradosome machinery and RNA processing by RNaseR at low temperature. Several unresolved questions are discussed in the context of astrobiology, and further work needed on the psychrotolerance of P. syringae.</description><subject>Adaptation</subject><subject>Astrobiology</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA repair</subject><subject>DNA-directed RNA polymerase</subject><subject>Enzyme kinetics</subject><subject>Extraterrestrial life</subject><subject>Extraterrestrial materials</subject><subject>Fatty acids</subject><subject>Fluidity</subject><subject>Genes</subject><subject>Glycerol</subject><subject>Kinetics</subject><subject>Low temperature</subject><subject>Macromolecules</subject><subject>Mechanics</subject><subject>Membrane fluidity</subject><subject>Membrane permeability</subject><subject>Membrane proteins</subject><subject>Membranes</subject><subject>Nucleic acids</subject><subject>Nutrient uptake</subject><subject>Permeability</subject><subject>Phenotypes</subject><subject>Properties</subject><subject>Pseudomonas</subject><subject>Pseudomonas syringae</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA polymerase</subject><subject>RNA processing</subject><subject>Survival</subject><subject>Temperature</subject><subject>Uptake</subject><subject>Viscosity</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNqFkL1PwzAQxS0EEqUws1piYQn1d5wRVQUqtYIBZstx7DZVGhc7Ecp_j0tQBxZuuXun3zudHgC3GD3gVDPMBMlIQZLkFLEzMDltzk8zJpfgKsYdQjinOZqA9do31vSNDrBuY73ZdjENnYfd1kJrfOM3A_QOaniIg9kG3yU-6LaDb9H2ld_7VkcYh1C3G22vwYXTTbQ3v30KPp4W7_OXbPX6vJw_rjJDZcEyKmShK1lZwyjNdWWcllYSUTqWlxJLp0tmGcEyF0gw7UpOpRMUJ0lYgQidgvvx7iH4z97GTu3raGzT6Nb6PirCeEE5JpQl9O4PuvN9aNN3inAuMJOUokTNRsoEH2OwTh1CvddhUBipY7zqGKA6hql-4k0OPjq-6sYO_-FqsV6Ovm93fXtU</recordid><startdate>202107</startdate><enddate>202107</enddate><creator>Pavankumar, Theetha L.</creator><creator>Mittal, Pragya</creator><creator>Hallsworth, John E.</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7QH</scope><scope>7QL</scope><scope>7ST</scope><scope>7T7</scope><scope>7TN</scope><scope>7U9</scope><scope>7UA</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H94</scope><scope>H95</scope><scope>H97</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>SOI</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-6797-9362</orcidid><orcidid>https://orcid.org/0000-0003-1845-9592</orcidid></search><sort><creationdate>202107</creationdate><title>Molecular insights into the ecology of a psychrotolerant Pseudomonas syringae</title><author>Pavankumar, Theetha L. ; Mittal, Pragya ; Hallsworth, John E.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3894-3689ad8dec4337adcfa8e826bf47b818fab4e421876064afb538f631760249023</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Adaptation</topic><topic>Astrobiology</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA repair</topic><topic>DNA-directed RNA polymerase</topic><topic>Enzyme kinetics</topic><topic>Extraterrestrial life</topic><topic>Extraterrestrial materials</topic><topic>Fatty acids</topic><topic>Fluidity</topic><topic>Genes</topic><topic>Glycerol</topic><topic>Kinetics</topic><topic>Low temperature</topic><topic>Macromolecules</topic><topic>Mechanics</topic><topic>Membrane fluidity</topic><topic>Membrane permeability</topic><topic>Membrane proteins</topic><topic>Membranes</topic><topic>Nucleic acids</topic><topic>Nutrient uptake</topic><topic>Permeability</topic><topic>Phenotypes</topic><topic>Properties</topic><topic>Pseudomonas</topic><topic>Pseudomonas syringae</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA polymerase</topic><topic>RNA processing</topic><topic>Survival</topic><topic>Temperature</topic><topic>Uptake</topic><topic>Viscosity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Pavankumar, Theetha L.</creatorcontrib><creatorcontrib>Mittal, Pragya</creatorcontrib><creatorcontrib>Hallsworth, John E.</creatorcontrib><collection>CrossRef</collection><collection>Aqualine</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Oceanic Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Water Resources Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Pavankumar, Theetha L.</au><au>Mittal, Pragya</au><au>Hallsworth, John E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Molecular insights into the ecology of a psychrotolerant Pseudomonas syringae</atitle><jtitle>Environmental microbiology</jtitle><date>2021-07</date><risdate>2021</risdate><volume>23</volume><issue>7</issue><spage>3665</spage><epage>3681</epage><pages>3665-3681</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Summary
Low temperatures constrain cellular life due to reductions in nutrient uptake, enzyme kinetics, membrane permeability, and function of other biomacromolecules. This has implications for the biophysical limits of life on Earth, and the plausibility of life in extraterrestrial locations. Although most pseudomonads are mesophilic in nature, isolates such as the Antarctic Pseudomonas syringae Lz4W exhibit considerable psychrotolerance, with an ability to grow even between 4 and 0°C. In this review, we explore the molecular traits and characteristic phenotypes of P. syringae Lz4W that enable life at low temperatures. We describe adaptations that enhance membrane fluidity; examine genes involved in cellular function and survival in the cold; assess capability for energy generation at low temperature; and detail the mechanics of DNA repair and RNA processing at low temperature, and speculate that P. syringae Lz4W can also synthesize glycerol to maintain flexibility of macromolecular systems. In the range 4 to 0ºC, there are considerable changes in the properties and behaviour of water. Specifically, density can have adverse impacts on plasma‐membrane functions, cytoplasmic viscosity, protein behaviour, and other essential properties of cellular system. We identified a combination of adaptations that may be peculiar to cold‐tolerant P. syringae, including increase of unsaturated fatty acids in the plasma membrane; a RNA polymerase able to function at 0°C; RecBCD‐ and RuvAB‐dependent reestablishment of replication fork; and efficiencies of degradosome machinery and RNA processing by RNaseR at low temperature. Several unresolved questions are discussed in the context of astrobiology, and further work needed on the psychrotolerance of P. syringae.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><doi>10.1111/1462-2920.15304</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0001-6797-9362</orcidid><orcidid>https://orcid.org/0000-0003-1845-9592</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adaptation Astrobiology Deoxyribonucleic acid DNA DNA repair DNA-directed RNA polymerase Enzyme kinetics Extraterrestrial life Extraterrestrial materials Fatty acids Fluidity Genes Glycerol Kinetics Low temperature Macromolecules Mechanics Membrane fluidity Membrane permeability Membrane proteins Membranes Nucleic acids Nutrient uptake Permeability Phenotypes Properties Pseudomonas Pseudomonas syringae Ribonucleic acid RNA RNA polymerase RNA processing Survival Temperature Uptake Viscosity |
title | Molecular insights into the ecology of a psychrotolerant Pseudomonas syringae |
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