Selection, Succession, and Stabilization of Soil Microbial Consortia

ABSTRACT Soil microorganisms play fundamental roles in cycling of soil carbon, nitrogen, and other nutrients, yet we have a poor understanding of how soil microbiomes are shaped by their nutritional and physical environment. In this study, we investigated the successional dynamics of a soil microbio...

Full description

Bibliographic Details
Main Authors: Elias K. Zegeye, Colin J. Brislawn, Yuliya Farris, Sarah J. Fansler, Kirsten S. Hofmockel, Janet K. Jansson, Aaron T. Wright, Emily B. Graham, Dan Naylor, Ryan S. McClure, Hans C. Bernstein
Format: Article
Language:English
Published: American Society for Microbiology 2019-08-01
Series:mSystems
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/mSystems.00055-19
_version_ 1818345256872050688
author Elias K. Zegeye
Colin J. Brislawn
Yuliya Farris
Sarah J. Fansler
Kirsten S. Hofmockel
Janet K. Jansson
Aaron T. Wright
Emily B. Graham
Dan Naylor
Ryan S. McClure
Hans C. Bernstein
author_facet Elias K. Zegeye
Colin J. Brislawn
Yuliya Farris
Sarah J. Fansler
Kirsten S. Hofmockel
Janet K. Jansson
Aaron T. Wright
Emily B. Graham
Dan Naylor
Ryan S. McClure
Hans C. Bernstein
author_sort Elias K. Zegeye
collection DOAJ
description ABSTRACT Soil microorganisms play fundamental roles in cycling of soil carbon, nitrogen, and other nutrients, yet we have a poor understanding of how soil microbiomes are shaped by their nutritional and physical environment. In this study, we investigated the successional dynamics of a soil microbiome during 21 weeks of enrichment on chitin and its monomer, N-acetylglucosamine. We examined succession of the soil communities in a physically heterogeneous soil matrix as well as a homogeneous liquid medium. The guiding hypothesis was that the initial species richness would influence the tendency for the selected consortia to stabilize and maintain a relatively constant community structure over time. We also hypothesized that long-term, substrate-driven growth would result in consortia with reduced species richness compared to the parent microbiome and that this process would be deterministic with relatively little variation between replicates. We found that the initial species richness does influence the long-term community stability in both liquid media and soil and that lower initial richness results in a more rapid convergence to stability. Despite use of the same soil inoculum and access to the same major substrate, the resulting community composition differed greatly in soil from that in liquid medium. Hence, distinct selective pressures in soils relative to homogenous liquid media exist and can control community succession dynamics. This difference is likely related to the fact that soil microbiomes are more likely to thrive, with fewer compositional changes, in a soil matrix than in liquid environments. IMPORTANCE The soil microbiome carries out important ecosystem functions, but interactions between soil microbial communities have been difficult to study due to the high microbial diversity and complexity of the soil habitat. In this study, we successfully obtained stable consortia with reduced complexity that contained species found in the original source soil. These consortia and the methods used to obtain them can be a valuable resource for exploration of specific mechanisms underlying soil microbial community ecology. The results of this study also provide new experimental context to better inform how soil microbial communities are shaped by new environments and how a combination of initial taxonomic structure and physical environment influences stability. Author Video: An author video summary of this article is available.
first_indexed 2024-12-13T16:59:29Z
format Article
id doaj.art-1baa4b3c42bf4c0e87e37baef2c56bb5
institution Directory Open Access Journal
issn 2379-5077
language English
last_indexed 2024-12-13T16:59:29Z
publishDate 2019-08-01
publisher American Society for Microbiology
record_format Article
series mSystems
spelling doaj.art-1baa4b3c42bf4c0e87e37baef2c56bb52022-12-21T23:37:50ZengAmerican Society for MicrobiologymSystems2379-50772019-08-014410.1128/mSystems.00055-19Selection, Succession, and Stabilization of Soil Microbial ConsortiaElias K. Zegeye0Colin J. Brislawn1Yuliya Farris2Sarah J. Fansler3Kirsten S. Hofmockel4Janet K. Jansson5Aaron T. Wright6Emily B. Graham7Dan Naylor8Ryan S. McClure9Hans C. Bernstein10Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USABiological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USABiological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USABiological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USAEnvironmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, USABiological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USABiological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USABiological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USABiological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USABiological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USABiological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USAABSTRACT Soil microorganisms play fundamental roles in cycling of soil carbon, nitrogen, and other nutrients, yet we have a poor understanding of how soil microbiomes are shaped by their nutritional and physical environment. In this study, we investigated the successional dynamics of a soil microbiome during 21 weeks of enrichment on chitin and its monomer, N-acetylglucosamine. We examined succession of the soil communities in a physically heterogeneous soil matrix as well as a homogeneous liquid medium. The guiding hypothesis was that the initial species richness would influence the tendency for the selected consortia to stabilize and maintain a relatively constant community structure over time. We also hypothesized that long-term, substrate-driven growth would result in consortia with reduced species richness compared to the parent microbiome and that this process would be deterministic with relatively little variation between replicates. We found that the initial species richness does influence the long-term community stability in both liquid media and soil and that lower initial richness results in a more rapid convergence to stability. Despite use of the same soil inoculum and access to the same major substrate, the resulting community composition differed greatly in soil from that in liquid medium. Hence, distinct selective pressures in soils relative to homogenous liquid media exist and can control community succession dynamics. This difference is likely related to the fact that soil microbiomes are more likely to thrive, with fewer compositional changes, in a soil matrix than in liquid environments. IMPORTANCE The soil microbiome carries out important ecosystem functions, but interactions between soil microbial communities have been difficult to study due to the high microbial diversity and complexity of the soil habitat. In this study, we successfully obtained stable consortia with reduced complexity that contained species found in the original source soil. These consortia and the methods used to obtain them can be a valuable resource for exploration of specific mechanisms underlying soil microbial community ecology. The results of this study also provide new experimental context to better inform how soil microbial communities are shaped by new environments and how a combination of initial taxonomic structure and physical environment influences stability. Author Video: An author video summary of this article is available.https://journals.asm.org/doi/10.1128/mSystems.00055-19chitinmicrobial consortiamicrobiomemicrobiome stabilitymodel microbiomeN-acetylglucosamine
spellingShingle Elias K. Zegeye
Colin J. Brislawn
Yuliya Farris
Sarah J. Fansler
Kirsten S. Hofmockel
Janet K. Jansson
Aaron T. Wright
Emily B. Graham
Dan Naylor
Ryan S. McClure
Hans C. Bernstein
Selection, Succession, and Stabilization of Soil Microbial Consortia
mSystems
chitin
microbial consortia
microbiome
microbiome stability
model microbiome
N-acetylglucosamine
title Selection, Succession, and Stabilization of Soil Microbial Consortia
title_full Selection, Succession, and Stabilization of Soil Microbial Consortia
title_fullStr Selection, Succession, and Stabilization of Soil Microbial Consortia
title_full_unstemmed Selection, Succession, and Stabilization of Soil Microbial Consortia
title_short Selection, Succession, and Stabilization of Soil Microbial Consortia
title_sort selection succession and stabilization of soil microbial consortia
topic chitin
microbial consortia
microbiome
microbiome stability
model microbiome
N-acetylglucosamine
url https://journals.asm.org/doi/10.1128/mSystems.00055-19
work_keys_str_mv AT eliaskzegeye selectionsuccessionandstabilizationofsoilmicrobialconsortia
AT colinjbrislawn selectionsuccessionandstabilizationofsoilmicrobialconsortia
AT yuliyafarris selectionsuccessionandstabilizationofsoilmicrobialconsortia
AT sarahjfansler selectionsuccessionandstabilizationofsoilmicrobialconsortia
AT kirstenshofmockel selectionsuccessionandstabilizationofsoilmicrobialconsortia
AT janetkjansson selectionsuccessionandstabilizationofsoilmicrobialconsortia
AT aarontwright selectionsuccessionandstabilizationofsoilmicrobialconsortia
AT emilybgraham selectionsuccessionandstabilizationofsoilmicrobialconsortia
AT dannaylor selectionsuccessionandstabilizationofsoilmicrobialconsortia
AT ryansmcclure selectionsuccessionandstabilizationofsoilmicrobialconsortia
AT hanscbernstein selectionsuccessionandstabilizationofsoilmicrobialconsortia