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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Main Authors: Kelly I. Ramin, Steven D. Allison
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-12-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.02956/full
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spelling doaj-96423073c6cf4340a36cf49be14a8e582020-11-25T00:16:07ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-12-011010.3389/fmicb.2019.02956494333Bacterial Tradeoffs in Growth Rate and Extracellular EnzymesKelly I. Ramin0Steven D. Allison1Steven D. Allison2Department of Ecology and Evolutionary Biology, University of California, Irvine, Irvine, CA, United StatesDepartment of Ecology and Evolutionary Biology, University of California, Irvine, Irvine, CA, United StatesDepartment of Earth System Science, University of California, Irvine, Irvine, CA, United StatesLike 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.https://www.frontiersin.org/article/10.3389/fmicb.2019.02956/fullextracellular enzymeleaf litterlife history strategymaximum growth ratephylogenetic conservationsoil bacteria
collection DOAJ
language English
format Article
sources DOAJ
author Kelly I. Ramin
Steven D. Allison
Steven D. Allison
spellingShingle Kelly I. Ramin
Steven D. Allison
Steven D. Allison
Bacterial Tradeoffs in Growth Rate and Extracellular Enzymes
Frontiers in Microbiology
extracellular enzyme
leaf litter
life history strategy
maximum growth rate
phylogenetic conservation
soil bacteria
author_facet Kelly I. Ramin
Steven D. Allison
Steven D. Allison
author_sort Kelly I. Ramin
title Bacterial Tradeoffs in Growth Rate and Extracellular Enzymes
title_short 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_sort bacterial tradeoffs in growth rate and extracellular enzymes
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2019-12-01
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.
topic extracellular enzyme
leaf litter
life history strategy
maximum growth rate
phylogenetic conservation
soil bacteria
url https://www.frontiersin.org/article/10.3389/fmicb.2019.02956/full
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