Dynamic utilization of low‐molecular‐weight organic substrates across a microbial growth rate gradient
Aim Low‐molecular‐weight organic substances (LMWOSs) are at the nexus between micro‐organisms, plant roots, detritus, and the soil mineral matrix. The nominal oxidation state of carbon (NOSC) has been suggested as a potential parameter for modelling microbial uptake rates of LMWOSs and the efficienc...
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| Veröffentlicht in: | Journal of applied microbiology 2022-09, Vol.133 (3), p.1479-1495 |
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| container_title | Journal of applied microbiology |
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| creator | Cyle, K. Taylor Klein, Annaleise R. Aristilde, Ludmilla Martínez, Carmen Enid |
| description | Aim
Low‐molecular‐weight organic substances (LMWOSs) are at the nexus between micro‐organisms, plant roots, detritus, and the soil mineral matrix. The nominal oxidation state of carbon (NOSC) has been suggested as a potential parameter for modelling microbial uptake rates of LMWOSs and the efficiency of carbon incorporation into new biomass.
Methods and Results
In this study, we assessed the role of compound class and oxidation state on uptake kinetics and substrate‐specific carbon use efficiency (SUE) during the growth of three model soil micro‐organisms, a fungal isolate (Penicillium spinulosum) and two bacterial isolates (Paraburkholderia solitsugae, and Ralstonia pickettii). Isolates were chosen that spanned a growth rate gradient (0.046–0.316 h−1) in media containing 34 common LMWOSs at realistically low initial concentrations (25 μM each). Clustered, co‐utilization of LMWOSs occurred for all three organisms. Potential trends (p |
| doi_str_mv | 10.1111/jam.15652 |
| format | Article |
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Low‐molecular‐weight organic substances (LMWOSs) are at the nexus between micro‐organisms, plant roots, detritus, and the soil mineral matrix. The nominal oxidation state of carbon (NOSC) has been suggested as a potential parameter for modelling microbial uptake rates of LMWOSs and the efficiency of carbon incorporation into new biomass.
Methods and Results
In this study, we assessed the role of compound class and oxidation state on uptake kinetics and substrate‐specific carbon use efficiency (SUE) during the growth of three model soil micro‐organisms, a fungal isolate (Penicillium spinulosum) and two bacterial isolates (Paraburkholderia solitsugae, and Ralstonia pickettii). Isolates were chosen that spanned a growth rate gradient (0.046–0.316 h−1) in media containing 34 common LMWOSs at realistically low initial concentrations (25 μM each). Clustered, co‐utilization of LMWOSs occurred for all three organisms. Potential trends (p < 0.05) for early utilization of more oxidized substrates were present for the two bacterial isolates (P. solitsugae and R. pickettii), but high variability (R2 < 0.15) and a small effect of NOSC indicate these relationships are not useful for prediction. The SUEs of selected substrates ranged from 0.16 to 0.99 and there was no observed relationship between NOSC and SUE.
Conclusion
Our results do not provide compelling population‐level support for NOSC as a predictive tool for either uptake kinetics or the efficiency of use of LMWOS in soil solution.
Significance and Impact of the Study
Metabolic strategies of organisms are likely more important than chemical identity in determining LMWOS cycling in soils. Previous community‐level observations may be biased towards fast‐responding bacterial community members.</description><identifier>ISSN: 1364-5072</identifier><identifier>EISSN: 1365-2672</identifier><identifier>DOI: 10.1111/jam.15652</identifier><identifier>PMID: 35665577</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Bacteria ; Carbon ; Detritus ; Efficiency ; Fungi ; Growth rate ; Kinetics ; Microorganisms ; Organisms ; Oxidation ; Plant roots ; Soil bacteria ; Soil solution ; Soils ; Substrates ; Utilization ; Valence</subject><ispartof>Journal of applied microbiology, 2022-09, Vol.133 (3), p.1479-1495</ispartof><rights>2022 Society for Applied Microbiology.</rights><rights>This article is protected by copyright. All rights reserved.</rights><rights>Copyright © 2022 The Society for Applied Microbiology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3882-e5d895b3d71b76dff3d62d00b79df8c754e2f79f2b58564a1df01cd60496cc293</citedby><cites>FETCH-LOGICAL-c3882-e5d895b3d71b76dff3d62d00b79df8c754e2f79f2b58564a1df01cd60496cc293</cites><orcidid>0000-0003-0647-5341</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fjam.15652$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fjam.15652$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35665577$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Cyle, K. Taylor</creatorcontrib><creatorcontrib>Klein, Annaleise R.</creatorcontrib><creatorcontrib>Aristilde, Ludmilla</creatorcontrib><creatorcontrib>Martínez, Carmen Enid</creatorcontrib><title>Dynamic utilization of low‐molecular‐weight organic substrates across a microbial growth rate gradient</title><title>Journal of applied microbiology</title><addtitle>J Appl Microbiol</addtitle><description>Aim
Low‐molecular‐weight organic substances (LMWOSs) are at the nexus between micro‐organisms, plant roots, detritus, and the soil mineral matrix. The nominal oxidation state of carbon (NOSC) has been suggested as a potential parameter for modelling microbial uptake rates of LMWOSs and the efficiency of carbon incorporation into new biomass.
Methods and Results
In this study, we assessed the role of compound class and oxidation state on uptake kinetics and substrate‐specific carbon use efficiency (SUE) during the growth of three model soil micro‐organisms, a fungal isolate (Penicillium spinulosum) and two bacterial isolates (Paraburkholderia solitsugae, and Ralstonia pickettii). Isolates were chosen that spanned a growth rate gradient (0.046–0.316 h−1) in media containing 34 common LMWOSs at realistically low initial concentrations (25 μM each). Clustered, co‐utilization of LMWOSs occurred for all three organisms. Potential trends (p < 0.05) for early utilization of more oxidized substrates were present for the two bacterial isolates (P. solitsugae and R. pickettii), but high variability (R2 < 0.15) and a small effect of NOSC indicate these relationships are not useful for prediction. The SUEs of selected substrates ranged from 0.16 to 0.99 and there was no observed relationship between NOSC and SUE.
Conclusion
Our results do not provide compelling population‐level support for NOSC as a predictive tool for either uptake kinetics or the efficiency of use of LMWOS in soil solution.
Significance and Impact of the Study
Metabolic strategies of organisms are likely more important than chemical identity in determining LMWOS cycling in soils. Previous community‐level observations may be biased towards fast‐responding bacterial community members.</description><subject>Bacteria</subject><subject>Carbon</subject><subject>Detritus</subject><subject>Efficiency</subject><subject>Fungi</subject><subject>Growth rate</subject><subject>Kinetics</subject><subject>Microorganisms</subject><subject>Organisms</subject><subject>Oxidation</subject><subject>Plant roots</subject><subject>Soil bacteria</subject><subject>Soil solution</subject><subject>Soils</subject><subject>Substrates</subject><subject>Utilization</subject><subject>Valence</subject><issn>1364-5072</issn><issn>1365-2672</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNp1kctOxCAUhonReBld-AKmiRtdVIEWaJdmvEfjRteEchmZ0KLQZjKufASf0ScRZ0YXJrI5f8KXL3B-APYRPEHpnE5Fe4IIJXgNbKOCkhxThtcXucwJZHgL7MQ4hRAVkNBNsFUQSglhbBtMz-edaK3Mht46-yZ667vMm8z52ef7R-udloMTIeWZtpPnPvNhIrrEx6GJfRC9jpmQwcc0suQJvrHCZZPgZ_1z9n2fslBWd_0u2DDCRb23miPwdHnxOL7O7x6ubsZnd7ksqgrnmqiqJk2hGGoYVcYUimIFYcNqZSrJSKmxYbXBDakILQVSBiKpKCxrKiWuixE4Wnpfgn8ddOx5a6PUzolO-yHytJwSJrpACT38g079ELr0Oo4ZrKuK4oXweEkt_hm04S_BtiLMOYL8uwCeCuCLAhJ7sDIOTavVL_mz8QScLoGZdXr-v4nfnt0vlV_5v5KS</recordid><startdate>202209</startdate><enddate>202209</enddate><creator>Cyle, K. Taylor</creator><creator>Klein, Annaleise R.</creator><creator>Aristilde, Ludmilla</creator><creator>Martínez, Carmen Enid</creator><general>Oxford University Press</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QO</scope><scope>7T7</scope><scope>7TM</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-0647-5341</orcidid></search><sort><creationdate>202209</creationdate><title>Dynamic utilization of low‐molecular‐weight organic substrates across a microbial growth rate gradient</title><author>Cyle, K. Taylor ; Klein, Annaleise R. ; Aristilde, Ludmilla ; Martínez, Carmen Enid</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3882-e5d895b3d71b76dff3d62d00b79df8c754e2f79f2b58564a1df01cd60496cc293</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Bacteria</topic><topic>Carbon</topic><topic>Detritus</topic><topic>Efficiency</topic><topic>Fungi</topic><topic>Growth rate</topic><topic>Kinetics</topic><topic>Microorganisms</topic><topic>Organisms</topic><topic>Oxidation</topic><topic>Plant roots</topic><topic>Soil bacteria</topic><topic>Soil solution</topic><topic>Soils</topic><topic>Substrates</topic><topic>Utilization</topic><topic>Valence</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Cyle, K. Taylor</creatorcontrib><creatorcontrib>Klein, Annaleise R.</creatorcontrib><creatorcontrib>Aristilde, Ludmilla</creatorcontrib><creatorcontrib>Martínez, Carmen Enid</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of applied microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Cyle, K. Taylor</au><au>Klein, Annaleise R.</au><au>Aristilde, Ludmilla</au><au>Martínez, Carmen Enid</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dynamic utilization of low‐molecular‐weight organic substrates across a microbial growth rate gradient</atitle><jtitle>Journal of applied microbiology</jtitle><addtitle>J Appl Microbiol</addtitle><date>2022-09</date><risdate>2022</risdate><volume>133</volume><issue>3</issue><spage>1479</spage><epage>1495</epage><pages>1479-1495</pages><issn>1364-5072</issn><eissn>1365-2672</eissn><abstract>Aim
Low‐molecular‐weight organic substances (LMWOSs) are at the nexus between micro‐organisms, plant roots, detritus, and the soil mineral matrix. The nominal oxidation state of carbon (NOSC) has been suggested as a potential parameter for modelling microbial uptake rates of LMWOSs and the efficiency of carbon incorporation into new biomass.
Methods and Results
In this study, we assessed the role of compound class and oxidation state on uptake kinetics and substrate‐specific carbon use efficiency (SUE) during the growth of three model soil micro‐organisms, a fungal isolate (Penicillium spinulosum) and two bacterial isolates (Paraburkholderia solitsugae, and Ralstonia pickettii). Isolates were chosen that spanned a growth rate gradient (0.046–0.316 h−1) in media containing 34 common LMWOSs at realistically low initial concentrations (25 μM each). Clustered, co‐utilization of LMWOSs occurred for all three organisms. Potential trends (p < 0.05) for early utilization of more oxidized substrates were present for the two bacterial isolates (P. solitsugae and R. pickettii), but high variability (R2 < 0.15) and a small effect of NOSC indicate these relationships are not useful for prediction. The SUEs of selected substrates ranged from 0.16 to 0.99 and there was no observed relationship between NOSC and SUE.
Conclusion
Our results do not provide compelling population‐level support for NOSC as a predictive tool for either uptake kinetics or the efficiency of use of LMWOS in soil solution.
Significance and Impact of the Study
Metabolic strategies of organisms are likely more important than chemical identity in determining LMWOS cycling in soils. Previous community‐level observations may be biased towards fast‐responding bacterial community members.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>35665577</pmid><doi>10.1111/jam.15652</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0003-0647-5341</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Bacteria Carbon Detritus Efficiency Fungi Growth rate Kinetics Microorganisms Organisms Oxidation Plant roots Soil bacteria Soil solution Soils Substrates Utilization Valence |
| title | Dynamic utilization of low‐molecular‐weight organic substrates across a microbial growth rate gradient |
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