Mining the Drilosphere: Bacterial Communities and Denitrifier Abundance in a No-Till Wheat Cropping System

Earthworms play important roles in no-till cropping systems by redistributing crop residue to lower soil horizons, providing macropores for root growth, increasing water infiltration, enhancing soil quality and organic matter, and stimulating nitrogen cycling. The soil impacted by earthworm activity...

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Main Authors: Daniel C. Schlatter, Catherine L. Reardon, Jodi Johnson-Maynard, Erin Brooks, Kendall Kahl, Jessica Norby, David Huggins, Timothy C. Paulitz
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-06-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.01339/full
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author Daniel C. Schlatter
Catherine L. Reardon
Jodi Johnson-Maynard
Erin Brooks
Kendall Kahl
Jessica Norby
David Huggins
Timothy C. Paulitz
author_facet Daniel C. Schlatter
Catherine L. Reardon
Jodi Johnson-Maynard
Erin Brooks
Kendall Kahl
Jessica Norby
David Huggins
Timothy C. Paulitz
author_sort Daniel C. Schlatter
collection DOAJ
description Earthworms play important roles in no-till cropping systems by redistributing crop residue to lower soil horizons, providing macropores for root growth, increasing water infiltration, enhancing soil quality and organic matter, and stimulating nitrogen cycling. The soil impacted by earthworm activity, including burrows, casts, and middens, is termed the drilosphere. The objective of this study was to determine the effect of earthworms on soil microbial community composition in the drilosphere at different landscape slope positions. Soil cores (50 cm depth) were extracted from three landscape locations (top, middle, and bottom slope positions) on a sloping aspect of a no-till wheat farm. Soil was sampled at the bottom of the soil core from inside multiple earthworm (Lumbricus terrestris) channels (drilosphere) and from adjacent bulk soil. Bacterial communities were characterized for 16S rRNA gene diversity using high-throughput sequencing and functional denitrifier gene abundance (nirK, nirS, and nosZ) by quantitative PCR. Bacterial communities were structured primarily by the landscape slope position of the soil core followed by source (bulk versus drilosphere soil), with a significant interaction between core position and source. The families AKIW874, Chitinophagaceae, and Comamonadaceae and the genera Amycolatopsis, Caulobacter, Nocardioides, and Variovorax were more abundant in the drilosphere compared to the bulk soil. Most of the individual bacterial taxa enriched in the drilosphere versus bulk soil were members of Actinobacteria, including Micrococcales, Gaiellaceae, Solirubrobacterales, and Mycobacterium. In general, the greatest differences in communities were observed in comparisons of the top and bottom slope positions in which the bottom slope communities had significantly greater richness, diversity, and denitrifier abundance than the top slope position. Populations of denitrifiers (i.e., ratio of nirK+nirS to 16S rRNA) were more abundant in earthworm-impacted soils and there was a significant impact of L. terrestris on soil community composition which was observed only in the top landscape position. There were significant correlations between the abundance of nirK and nirS and taxa within Proteobacteria, Acidobacteria, Actinobacteria, Verrucomicrobia, and Chloroflexi, suggesting a broad diversity of denitrifying bacteria. Earthworms influence the soil microbial communities, but the impact depends on the slope location in a variable landscape, which likely reflects different soil characteristics.
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spelling doaj.art-f4997dbb64ae4691af230ad8eecaf9392022-12-21T20:35:59ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-06-011010.3389/fmicb.2019.01339452477Mining the Drilosphere: Bacterial Communities and Denitrifier Abundance in a No-Till Wheat Cropping SystemDaniel C. Schlatter0Catherine L. Reardon1Jodi Johnson-Maynard2Erin Brooks3Kendall Kahl4Jessica Norby5David Huggins6Timothy C. Paulitz7Wheat Health, Genetics and Quality Research Unit, Agricultural Research Service, United States Department of Agriculture, Pullman, WA, United StatesSoil and Water Conservation Research Unit, Agricultural Research Service, United States Department of Agriculture, Adams, OR, United StatesDepartment of Soil and Water Systems, University of Idaho, Moscow, ID, United StatesDepartment of Soil and Water Systems, University of Idaho, Moscow, ID, United StatesDepartment of Soil and Water Systems, University of Idaho, Moscow, ID, United StatesDepartment of Soil and Water Systems, University of Idaho, Moscow, ID, United StatesNorthwest Sustainable Agroecosystems Research Unit, Agricultural Research Service, United States Department of Agriculture, Pullman, WA, United StatesWheat Health, Genetics and Quality Research Unit, Agricultural Research Service, United States Department of Agriculture, Pullman, WA, United StatesEarthworms play important roles in no-till cropping systems by redistributing crop residue to lower soil horizons, providing macropores for root growth, increasing water infiltration, enhancing soil quality and organic matter, and stimulating nitrogen cycling. The soil impacted by earthworm activity, including burrows, casts, and middens, is termed the drilosphere. The objective of this study was to determine the effect of earthworms on soil microbial community composition in the drilosphere at different landscape slope positions. Soil cores (50 cm depth) were extracted from three landscape locations (top, middle, and bottom slope positions) on a sloping aspect of a no-till wheat farm. Soil was sampled at the bottom of the soil core from inside multiple earthworm (Lumbricus terrestris) channels (drilosphere) and from adjacent bulk soil. Bacterial communities were characterized for 16S rRNA gene diversity using high-throughput sequencing and functional denitrifier gene abundance (nirK, nirS, and nosZ) by quantitative PCR. Bacterial communities were structured primarily by the landscape slope position of the soil core followed by source (bulk versus drilosphere soil), with a significant interaction between core position and source. The families AKIW874, Chitinophagaceae, and Comamonadaceae and the genera Amycolatopsis, Caulobacter, Nocardioides, and Variovorax were more abundant in the drilosphere compared to the bulk soil. Most of the individual bacterial taxa enriched in the drilosphere versus bulk soil were members of Actinobacteria, including Micrococcales, Gaiellaceae, Solirubrobacterales, and Mycobacterium. In general, the greatest differences in communities were observed in comparisons of the top and bottom slope positions in which the bottom slope communities had significantly greater richness, diversity, and denitrifier abundance than the top slope position. Populations of denitrifiers (i.e., ratio of nirK+nirS to 16S rRNA) were more abundant in earthworm-impacted soils and there was a significant impact of L. terrestris on soil community composition which was observed only in the top landscape position. There were significant correlations between the abundance of nirK and nirS and taxa within Proteobacteria, Acidobacteria, Actinobacteria, Verrucomicrobia, and Chloroflexi, suggesting a broad diversity of denitrifying bacteria. Earthworms influence the soil microbial communities, but the impact depends on the slope location in a variable landscape, which likely reflects different soil characteristics.https://www.frontiersin.org/article/10.3389/fmicb.2019.01339/fullearthwormssoilmicrobiomenext-generation sequencingdirect seedPacific Northwest
spellingShingle Daniel C. Schlatter
Catherine L. Reardon
Jodi Johnson-Maynard
Erin Brooks
Kendall Kahl
Jessica Norby
David Huggins
Timothy C. Paulitz
Mining the Drilosphere: Bacterial Communities and Denitrifier Abundance in a No-Till Wheat Cropping System
Frontiers in Microbiology
earthworms
soil
microbiome
next-generation sequencing
direct seed
Pacific Northwest
title Mining the Drilosphere: Bacterial Communities and Denitrifier Abundance in a No-Till Wheat Cropping System
title_full Mining the Drilosphere: Bacterial Communities and Denitrifier Abundance in a No-Till Wheat Cropping System
title_fullStr Mining the Drilosphere: Bacterial Communities and Denitrifier Abundance in a No-Till Wheat Cropping System
title_full_unstemmed Mining the Drilosphere: Bacterial Communities and Denitrifier Abundance in a No-Till Wheat Cropping System
title_short Mining the Drilosphere: Bacterial Communities and Denitrifier Abundance in a No-Till Wheat Cropping System
title_sort mining the drilosphere bacterial communities and denitrifier abundance in a no till wheat cropping system
topic earthworms
soil
microbiome
next-generation sequencing
direct seed
Pacific Northwest
url https://www.frontiersin.org/article/10.3389/fmicb.2019.01339/full
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