Parallelized, Aerobic, Single Carbon-Source Enrichments from Different Natural Environments Contain Divergent Microbial Communities

Microbial communities that inhabit environments such as soil can contain thousands of distinct taxa, yet little is known about how this diversity is maintained in response to environmental perturbations such as changes in the availability of carbon. By utilizing aerobic substrate arrays to examine t...

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Main Authors: Theodore M. Flynn, Jason C. Koval, Stephanie M. Greenwald, Sarah M. Owens, Kenneth M. Kemner, Dionysios A. Antonopoulos
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-11-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2017.02321/full
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spelling doaj-f69392cd52e7436ca7062d0942b92ea52020-11-25T00:25:22ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-11-01810.3389/fmicb.2017.02321295932Parallelized, Aerobic, Single Carbon-Source Enrichments from Different Natural Environments Contain Divergent Microbial CommunitiesTheodore M. FlynnJason C. KovalStephanie M. GreenwaldSarah M. OwensKenneth M. KemnerDionysios A. AntonopoulosMicrobial communities that inhabit environments such as soil can contain thousands of distinct taxa, yet little is known about how this diversity is maintained in response to environmental perturbations such as changes in the availability of carbon. By utilizing aerobic substrate arrays to examine the effect of carbon amendment on microbial communities taken from six distinct environments (soil from a temperate prairie and forest, tropical forest soil, subalpine forest soil, and surface water and soil from a palustrine emergent wetland), we examined how carbon amendment and inoculum source shape the composition of the community in each enrichment. Dilute subsamples from each environment were used to inoculate 96-well microtiter plates containing triplicate wells amended with one of 31 carbon sources from six different classes of organic compounds (phenols, polymers, carbohydrates, carboxylic acids, amines, amino acids). After incubating each well aerobically in the dark for 72 h, we analyzed the composition of the microbial communities on the substrate arrays as well as the initial inocula by sequencing 16S rRNA gene amplicons using the Illumina MiSeq platform. Comparisons of alpha and beta diversity in these systems showed that, while the composition of the communities that grow to inhabit the wells in each substrate array diverges sharply from that of the original community in the inoculum, these enrichment communities are still strongly affected by the inoculum source. We found most enrichments were dominated by one or several OTUs most closely related to aerobes or facultative anaerobes from the Proteobacteria (e.g., Pseudomonas, Burkholderia, and Ralstonia) or Bacteroidetes (e.g., Chryseobacterium). Comparisons within each substrate array based on the class of carbon source further show that the communities inhabiting wells amended with a carbohydrate differ significantly from those enriched with a phenolic compound. Selection therefore seems to play a role in shaping the communities in the substrate arrays, although some stochasticity is also seen whereby several replicate wells within a single substrate array display strongly divergent community compositions. Overall, the use of highly parallel substrate arrays offers a promising path forward to study the response of microbial communities to perturbations in a changing environment.http://journal.frontiersin.org/article/10.3389/fmicb.2017.02321/fullmicrobial ecologycarbon cyclingsoil microbiologymicrocosmenrichment culture
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language English
format Article
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author Theodore M. Flynn
Jason C. Koval
Stephanie M. Greenwald
Sarah M. Owens
Kenneth M. Kemner
Dionysios A. Antonopoulos
spellingShingle Theodore M. Flynn
Jason C. Koval
Stephanie M. Greenwald
Sarah M. Owens
Kenneth M. Kemner
Dionysios A. Antonopoulos
Parallelized, Aerobic, Single Carbon-Source Enrichments from Different Natural Environments Contain Divergent Microbial Communities
Frontiers in Microbiology
microbial ecology
carbon cycling
soil microbiology
microcosm
enrichment culture
author_facet Theodore M. Flynn
Jason C. Koval
Stephanie M. Greenwald
Sarah M. Owens
Kenneth M. Kemner
Dionysios A. Antonopoulos
author_sort Theodore M. Flynn
title Parallelized, Aerobic, Single Carbon-Source Enrichments from Different Natural Environments Contain Divergent Microbial Communities
title_short Parallelized, Aerobic, Single Carbon-Source Enrichments from Different Natural Environments Contain Divergent Microbial Communities
title_full Parallelized, Aerobic, Single Carbon-Source Enrichments from Different Natural Environments Contain Divergent Microbial Communities
title_fullStr Parallelized, Aerobic, Single Carbon-Source Enrichments from Different Natural Environments Contain Divergent Microbial Communities
title_full_unstemmed Parallelized, Aerobic, Single Carbon-Source Enrichments from Different Natural Environments Contain Divergent Microbial Communities
title_sort parallelized, aerobic, single carbon-source enrichments from different natural environments contain divergent microbial communities
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2017-11-01
description Microbial communities that inhabit environments such as soil can contain thousands of distinct taxa, yet little is known about how this diversity is maintained in response to environmental perturbations such as changes in the availability of carbon. By utilizing aerobic substrate arrays to examine the effect of carbon amendment on microbial communities taken from six distinct environments (soil from a temperate prairie and forest, tropical forest soil, subalpine forest soil, and surface water and soil from a palustrine emergent wetland), we examined how carbon amendment and inoculum source shape the composition of the community in each enrichment. Dilute subsamples from each environment were used to inoculate 96-well microtiter plates containing triplicate wells amended with one of 31 carbon sources from six different classes of organic compounds (phenols, polymers, carbohydrates, carboxylic acids, amines, amino acids). After incubating each well aerobically in the dark for 72 h, we analyzed the composition of the microbial communities on the substrate arrays as well as the initial inocula by sequencing 16S rRNA gene amplicons using the Illumina MiSeq platform. Comparisons of alpha and beta diversity in these systems showed that, while the composition of the communities that grow to inhabit the wells in each substrate array diverges sharply from that of the original community in the inoculum, these enrichment communities are still strongly affected by the inoculum source. We found most enrichments were dominated by one or several OTUs most closely related to aerobes or facultative anaerobes from the Proteobacteria (e.g., Pseudomonas, Burkholderia, and Ralstonia) or Bacteroidetes (e.g., Chryseobacterium). Comparisons within each substrate array based on the class of carbon source further show that the communities inhabiting wells amended with a carbohydrate differ significantly from those enriched with a phenolic compound. Selection therefore seems to play a role in shaping the communities in the substrate arrays, although some stochasticity is also seen whereby several replicate wells within a single substrate array display strongly divergent community compositions. Overall, the use of highly parallel substrate arrays offers a promising path forward to study the response of microbial communities to perturbations in a changing environment.
topic microbial ecology
carbon cycling
soil microbiology
microcosm
enrichment culture
url http://journal.frontiersin.org/article/10.3389/fmicb.2017.02321/full
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