Genomic Features Predict Bacterial Life History Strategies in Soil, as Identified by Metagenomic Stable Isotope Probing

ABSTRACT Bacteria catalyze the formation and destruction of soil organic matter, but the bacterial dynamics in soil that govern carbon (C) cycling are not well understood. Life history strategies explain the complex dynamics of bacterial populations and activities based on trade-offs in energy alloc...

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Main Authors: Samuel E. Barnett, Rob Egan, Brian Foster, Emiley A. Eloe-Fadrosh, Daniel H. Buckley
Format: Article
Language:English
Published: American Society for Microbiology 2023-04-01
Series:mBio
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/mbio.03584-22
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author Samuel E. Barnett
Rob Egan
Brian Foster
Emiley A. Eloe-Fadrosh
Daniel H. Buckley
author_facet Samuel E. Barnett
Rob Egan
Brian Foster
Emiley A. Eloe-Fadrosh
Daniel H. Buckley
author_sort Samuel E. Barnett
collection DOAJ
description ABSTRACT Bacteria catalyze the formation and destruction of soil organic matter, but the bacterial dynamics in soil that govern carbon (C) cycling are not well understood. Life history strategies explain the complex dynamics of bacterial populations and activities based on trade-offs in energy allocation to growth, resource acquisition, and survival. Such trade-offs influence the fate of soil C, but their genomic basis remains poorly characterized. We used multisubstrate metagenomic DNA stable isotope probing to link genomic features of bacteria to their C acquisition and growth dynamics. We identify several genomic features associated with patterns of bacterial C acquisition and growth, notably genomic investment in resource acquisition and regulatory flexibility. Moreover, we identify genomic trade-offs defined by numbers of transcription factors, membrane transporters, and secreted products, which match predictions from life history theory. We further show that genomic investment in resource acquisition and regulatory flexibility can predict bacterial ecological strategies in soil. IMPORTANCE Soil microbes are major players in the global carbon cycle, yet we still have little understanding of how the carbon cycle operates in soil communities. A major limitation is that carbon metabolism lacks discrete functional genes that define carbon transformations. Instead, carbon transformations are governed by anabolic processes associated with growth, resource acquisition, and survival. We use metagenomic stable isotope probing to link genome information to microbial growth and carbon assimilation dynamics as they occur in soil. From these data, we identify genomic traits that can predict bacterial ecological strategies which define bacterial interactions with soil carbon.
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spelling doaj.art-81af6afbaac14d9b981fab3d2f0747212023-04-25T13:04:57ZengAmerican Society for MicrobiologymBio2150-75112023-04-0114210.1128/mbio.03584-22Genomic Features Predict Bacterial Life History Strategies in Soil, as Identified by Metagenomic Stable Isotope ProbingSamuel E. Barnett0Rob Egan1Brian Foster2Emiley A. Eloe-Fadrosh3Daniel H. Buckley4School of Integrative Plant Science, Cornell University, Ithaca, New York, USADOE Joint Genome Institute, Berkeley, California, USADOE Joint Genome Institute, Berkeley, California, USADOE Joint Genome Institute, Berkeley, California, USASchool of Integrative Plant Science, Cornell University, Ithaca, New York, USAABSTRACT Bacteria catalyze the formation and destruction of soil organic matter, but the bacterial dynamics in soil that govern carbon (C) cycling are not well understood. Life history strategies explain the complex dynamics of bacterial populations and activities based on trade-offs in energy allocation to growth, resource acquisition, and survival. Such trade-offs influence the fate of soil C, but their genomic basis remains poorly characterized. We used multisubstrate metagenomic DNA stable isotope probing to link genomic features of bacteria to their C acquisition and growth dynamics. We identify several genomic features associated with patterns of bacterial C acquisition and growth, notably genomic investment in resource acquisition and regulatory flexibility. Moreover, we identify genomic trade-offs defined by numbers of transcription factors, membrane transporters, and secreted products, which match predictions from life history theory. We further show that genomic investment in resource acquisition and regulatory flexibility can predict bacterial ecological strategies in soil. IMPORTANCE Soil microbes are major players in the global carbon cycle, yet we still have little understanding of how the carbon cycle operates in soil communities. A major limitation is that carbon metabolism lacks discrete functional genes that define carbon transformations. Instead, carbon transformations are governed by anabolic processes associated with growth, resource acquisition, and survival. We use metagenomic stable isotope probing to link genome information to microbial growth and carbon assimilation dynamics as they occur in soil. From these data, we identify genomic traits that can predict bacterial ecological strategies which define bacterial interactions with soil carbon.https://journals.asm.org/doi/10.1128/mbio.03584-22stable isotope probingmetagenomesoilcarbon cyclemicrobialgenome
spellingShingle Samuel E. Barnett
Rob Egan
Brian Foster
Emiley A. Eloe-Fadrosh
Daniel H. Buckley
Genomic Features Predict Bacterial Life History Strategies in Soil, as Identified by Metagenomic Stable Isotope Probing
mBio
stable isotope probing
metagenome
soil
carbon cycle
microbial
genome
title Genomic Features Predict Bacterial Life History Strategies in Soil, as Identified by Metagenomic Stable Isotope Probing
title_full Genomic Features Predict Bacterial Life History Strategies in Soil, as Identified by Metagenomic Stable Isotope Probing
title_fullStr Genomic Features Predict Bacterial Life History Strategies in Soil, as Identified by Metagenomic Stable Isotope Probing
title_full_unstemmed Genomic Features Predict Bacterial Life History Strategies in Soil, as Identified by Metagenomic Stable Isotope Probing
title_short Genomic Features Predict Bacterial Life History Strategies in Soil, as Identified by Metagenomic Stable Isotope Probing
title_sort genomic features predict bacterial life history strategies in soil as identified by metagenomic stable isotope probing
topic stable isotope probing
metagenome
soil
carbon cycle
microbial
genome
url https://journals.asm.org/doi/10.1128/mbio.03584-22
work_keys_str_mv AT samuelebarnett genomicfeaturespredictbacteriallifehistorystrategiesinsoilasidentifiedbymetagenomicstableisotopeprobing
AT robegan genomicfeaturespredictbacteriallifehistorystrategiesinsoilasidentifiedbymetagenomicstableisotopeprobing
AT brianfoster genomicfeaturespredictbacteriallifehistorystrategiesinsoilasidentifiedbymetagenomicstableisotopeprobing
AT emileyaeloefadrosh genomicfeaturespredictbacteriallifehistorystrategiesinsoilasidentifiedbymetagenomicstableisotopeprobing
AT danielhbuckley genomicfeaturespredictbacteriallifehistorystrategiesinsoilasidentifiedbymetagenomicstableisotopeprobing