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Bacterial Tradeoffs in Growth Rate and Extracellular Enzymes

Like larger organisms, bacteria possess traits, or phenotypic characteristics, that influence growth and impact ecosystem processes. Still, it remains unclear how these traits are organized across bacterial lineages. Using 49 bacterial strains isolated from leaf litter in Southern California, we tes...

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Autores principales: Ramin, Kelly I., Allison, Steven D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6933949/
https://www.ncbi.nlm.nih.gov/pubmed/31921094
http://dx.doi.org/10.3389/fmicb.2019.02956
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author Ramin, Kelly I.
Allison, Steven D.
author_facet Ramin, Kelly I.
Allison, Steven D.
author_sort Ramin, Kelly I.
collection PubMed
description Like larger organisms, bacteria possess traits, or phenotypic characteristics, that influence growth and impact ecosystem processes. Still, it remains unclear how these traits are organized across bacterial lineages. Using 49 bacterial strains isolated from leaf litter in Southern California, we tested the hypothesis that bacterial growth rates trade off against extracellular enzyme investment. We also tested for phylogenetic conservation of these traits under high and low resource conditions represented, respectively, by Luria broth (LB) and a monomer-dominated medium extracted from plant litter. In support of our hypotheses, we found a negative correlation between the maximum growth rate and the total activity of carbon-, nitrogen-, and phosphorus-degrading extracellular enzymes. However, this tradeoff was only observed under high resource conditions. We also found significant phylogenetic signal in maximum growth rate and extracellular enzyme investment under high and low resource conditions. Driven by our bacterial trait data, we proposed three potential life history strategies. Resource acquisition strategists invest heavily in extracellular enzyme production. Growth strategists invest in high growth rates. Bacteria in a third category showed lower potential for enzyme production and growth, so we tentatively classified them as maintenance strategists that may perform better under conditions we did not measure. These strategies were related to bacterial phylogeny, with most growth strategists belonging to the phylum Proteobacteria and most maintenance and resource acquisition strategists belonging to the phylum Actinobacteria. By accounting for extracellular enzyme investment, our proposed life history strategies complement existing frameworks, such as the copiotroph-oligotroph continuum and Grime’s competitor-stress tolerator-ruderal triangle. Our results have biogeochemical implications because allocation to extracellular enzymes versus growth or stress tolerance can determine the fate and form of organic matter cycling through surface soil.
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spelling pubmed-69339492020-01-09 Bacterial Tradeoffs in Growth Rate and Extracellular Enzymes Ramin, Kelly I. Allison, Steven D. Front Microbiol Microbiology Like larger organisms, bacteria possess traits, or phenotypic characteristics, that influence growth and impact ecosystem processes. Still, it remains unclear how these traits are organized across bacterial lineages. Using 49 bacterial strains isolated from leaf litter in Southern California, we tested the hypothesis that bacterial growth rates trade off against extracellular enzyme investment. We also tested for phylogenetic conservation of these traits under high and low resource conditions represented, respectively, by Luria broth (LB) and a monomer-dominated medium extracted from plant litter. In support of our hypotheses, we found a negative correlation between the maximum growth rate and the total activity of carbon-, nitrogen-, and phosphorus-degrading extracellular enzymes. However, this tradeoff was only observed under high resource conditions. We also found significant phylogenetic signal in maximum growth rate and extracellular enzyme investment under high and low resource conditions. Driven by our bacterial trait data, we proposed three potential life history strategies. Resource acquisition strategists invest heavily in extracellular enzyme production. Growth strategists invest in high growth rates. Bacteria in a third category showed lower potential for enzyme production and growth, so we tentatively classified them as maintenance strategists that may perform better under conditions we did not measure. These strategies were related to bacterial phylogeny, with most growth strategists belonging to the phylum Proteobacteria and most maintenance and resource acquisition strategists belonging to the phylum Actinobacteria. By accounting for extracellular enzyme investment, our proposed life history strategies complement existing frameworks, such as the copiotroph-oligotroph continuum and Grime’s competitor-stress tolerator-ruderal triangle. Our results have biogeochemical implications because allocation to extracellular enzymes versus growth or stress tolerance can determine the fate and form of organic matter cycling through surface soil. Frontiers Media S.A. 2019-12-20 /pmc/articles/PMC6933949/ /pubmed/31921094 http://dx.doi.org/10.3389/fmicb.2019.02956 Text en Copyright © 2019 Ramin and Allison. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Ramin, Kelly I.
Allison, Steven D.
Bacterial Tradeoffs in Growth Rate and Extracellular Enzymes
title Bacterial Tradeoffs in Growth Rate and Extracellular Enzymes
title_full Bacterial Tradeoffs in Growth Rate and Extracellular Enzymes
title_fullStr Bacterial Tradeoffs in Growth Rate and Extracellular Enzymes
title_full_unstemmed Bacterial Tradeoffs in Growth Rate and Extracellular Enzymes
title_short Bacterial Tradeoffs in Growth Rate and Extracellular Enzymes
title_sort bacterial tradeoffs in growth rate and extracellular enzymes
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6933949/
https://www.ncbi.nlm.nih.gov/pubmed/31921094
http://dx.doi.org/10.3389/fmicb.2019.02956
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