Niche Differentiation of Bacterial Versus Archaeal Soil Nitrifiers Induced by Ammonium Inhibition Along a Management Gradient

Soil nitrification, mediated mainly by ammonia oxidizing archaea (AOA) and bacteria (AOB), converts ammonium (NH4+) to nitrite (NO2−) and thence nitrate (NO3−). To better understand ecological differences between AOA and AOB, we investigated the nitrification kinetics of AOA and AOB under eight repl...

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Main Authors: Di Liang, Yang Ouyang, Lisa Tiemann, G. Philip Robertson
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-11-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2020.568588/full
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author Di Liang
Di Liang
Yang Ouyang
Lisa Tiemann
G. Philip Robertson
G. Philip Robertson
author_facet Di Liang
Di Liang
Yang Ouyang
Lisa Tiemann
G. Philip Robertson
G. Philip Robertson
author_sort Di Liang
collection DOAJ
description Soil nitrification, mediated mainly by ammonia oxidizing archaea (AOA) and bacteria (AOB), converts ammonium (NH4+) to nitrite (NO2−) and thence nitrate (NO3−). To better understand ecological differences between AOA and AOB, we investigated the nitrification kinetics of AOA and AOB under eight replicated cropped and unmanaged ecosystems (including two fertilized natural systems) along a long-term management intensity gradient in the upper U.S. Midwest. For five of eight ecosystems, AOB but not AOA exhibited Haldane kinetics (inhibited by high NH4+ additions), especially in perennial and successional systems. In contrast, AOA predominantly exhibited Michaelis-Menten kinetics, suggesting greater resistance to high nitrogen inputs than AOB. These responses suggest the potential for NH4+-induced niche differentiation between AOA and AOB. Additionally, long-term fertilization significantly enhanced maximum nitrification rates (Vmax) in the early successional systems for both AOA and AOB, but not in the deciduous forest systems. This was likely due to pH suppression of nitrification in the acidic forest soils, corroborated by a positive correlation of Vmax with soil pH but not with amoA gene abundance. Results also demonstrated that soil nitrification potentials were relatively stable, as there were no seasonal differences. Overall, results suggest that (1) NH4+ inhibition of AOB but not AOA could be another factor contributing to niche differentiation between AOA and AOB in soil, and (2) nitrification by both AOA and AOB can be significantly promoted by long-term nitrogen inputs.
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spelling doaj.art-2b194d92c191433c9e6fd0eca58160f72022-12-22T01:17:40ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-11-011110.3389/fmicb.2020.568588568588Niche Differentiation of Bacterial Versus Archaeal Soil Nitrifiers Induced by Ammonium Inhibition Along a Management GradientDi Liang0Di Liang1Yang Ouyang2Lisa Tiemann3G. Philip Robertson4G. Philip Robertson5Department of Plant, Soil and Microbial Sciences and Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI, United StatesW. K. Kellogg Biological Station, Michigan State University, Hickory Corners, MI, United StatesDepartment of Plant, Soil and Microbial Sciences and Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI, United StatesDepartment of Plant, Soil and Microbial Sciences and Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI, United StatesDepartment of Plant, Soil and Microbial Sciences and Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI, United StatesW. K. Kellogg Biological Station, Michigan State University, Hickory Corners, MI, United StatesSoil nitrification, mediated mainly by ammonia oxidizing archaea (AOA) and bacteria (AOB), converts ammonium (NH4+) to nitrite (NO2−) and thence nitrate (NO3−). To better understand ecological differences between AOA and AOB, we investigated the nitrification kinetics of AOA and AOB under eight replicated cropped and unmanaged ecosystems (including two fertilized natural systems) along a long-term management intensity gradient in the upper U.S. Midwest. For five of eight ecosystems, AOB but not AOA exhibited Haldane kinetics (inhibited by high NH4+ additions), especially in perennial and successional systems. In contrast, AOA predominantly exhibited Michaelis-Menten kinetics, suggesting greater resistance to high nitrogen inputs than AOB. These responses suggest the potential for NH4+-induced niche differentiation between AOA and AOB. Additionally, long-term fertilization significantly enhanced maximum nitrification rates (Vmax) in the early successional systems for both AOA and AOB, but not in the deciduous forest systems. This was likely due to pH suppression of nitrification in the acidic forest soils, corroborated by a positive correlation of Vmax with soil pH but not with amoA gene abundance. Results also demonstrated that soil nitrification potentials were relatively stable, as there were no seasonal differences. Overall, results suggest that (1) NH4+ inhibition of AOB but not AOA could be another factor contributing to niche differentiation between AOA and AOB in soil, and (2) nitrification by both AOA and AOB can be significantly promoted by long-term nitrogen inputs.https://www.frontiersin.org/articles/10.3389/fmicb.2020.568588/fullniche differentiationlong-termmanagement gradientammonia oxidizing archaeaammonia oxidizing bacteriaresistance
spellingShingle Di Liang
Di Liang
Yang Ouyang
Lisa Tiemann
G. Philip Robertson
G. Philip Robertson
Niche Differentiation of Bacterial Versus Archaeal Soil Nitrifiers Induced by Ammonium Inhibition Along a Management Gradient
Frontiers in Microbiology
niche differentiation
long-term
management gradient
ammonia oxidizing archaea
ammonia oxidizing bacteria
resistance
title Niche Differentiation of Bacterial Versus Archaeal Soil Nitrifiers Induced by Ammonium Inhibition Along a Management Gradient
title_full Niche Differentiation of Bacterial Versus Archaeal Soil Nitrifiers Induced by Ammonium Inhibition Along a Management Gradient
title_fullStr Niche Differentiation of Bacterial Versus Archaeal Soil Nitrifiers Induced by Ammonium Inhibition Along a Management Gradient
title_full_unstemmed Niche Differentiation of Bacterial Versus Archaeal Soil Nitrifiers Induced by Ammonium Inhibition Along a Management Gradient
title_short Niche Differentiation of Bacterial Versus Archaeal Soil Nitrifiers Induced by Ammonium Inhibition Along a Management Gradient
title_sort niche differentiation of bacterial versus archaeal soil nitrifiers induced by ammonium inhibition along a management gradient
topic niche differentiation
long-term
management gradient
ammonia oxidizing archaea
ammonia oxidizing bacteria
resistance
url https://www.frontiersin.org/articles/10.3389/fmicb.2020.568588/full
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