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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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 |
work_keys_str_mv |
AT kellyiramin bacterialtradeoffsingrowthrateandextracellularenzymes AT stevendallison bacterialtradeoffsingrowthrateandextracellularenzymes AT stevendallison bacterialtradeoffsingrowthrateandextracellularenzymes |
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