Nutrient-Limited Enrichments of Nitrifiers From Soil Yield Consortia of Nitrosocosmicus-Affiliated AOA and Nitrospira-Affiliated NOB

The discovery of ammonia-oxidizing archaea (AOA) and complete ammonia-oxidizing (comammox) bacteria widespread in terrestrial ecosystems indicates an important role of these organisms in terrestrial nitrification. Recent evidence indicated a higher ammonia affinity of comammox bacteria than of terre...

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Main Authors: Jonathan Rodriguez, Seemanti Chakrabarti, Eunkyung Choi, Nisreen Shehadeh, Samantha Sierra-Martinez, Jun Zhao, Willm Martens-Habbena
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.671480/full
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spelling doaj-f911795bfbdd4566aba35d146c9571692021-07-12T09:40:02ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-07-011210.3389/fmicb.2021.671480671480Nutrient-Limited Enrichments of Nitrifiers From Soil Yield Consortia of Nitrosocosmicus-Affiliated AOA and Nitrospira-Affiliated NOBJonathan RodriguezSeemanti ChakrabartiEunkyung ChoiNisreen ShehadehSamantha Sierra-MartinezJun ZhaoWillm Martens-HabbenaThe discovery of ammonia-oxidizing archaea (AOA) and complete ammonia-oxidizing (comammox) bacteria widespread in terrestrial ecosystems indicates an important role of these organisms in terrestrial nitrification. Recent evidence indicated a higher ammonia affinity of comammox bacteria than of terrestrial AOA and ammonia-oxidizing bacteria (AOB), suggesting that comammox bacteria could potentially represent the most low-nutrient adapted nitrifiers in terrestrial systems. We hypothesized that a nutrient-limited enrichment strategy could exploit the differences in cellular kinetic properties and yield enrichments dominated by high affinity and high yield comammox bacteria. Using soil with a mixed community of AOA, AOB, and comammox Nitrospira, we compared performance of nutrient-limited chemostat enrichment with or without batch culture pre-enrichment in two different growth media without inhibitors or antibiotics. Monitoring of microbial community composition via 16S rRNA and amoA gene sequencing showed that batch enrichments were dominated by AOB, accompanied by low numbers of AOA and comammox Nitrospira. In contrast, nutrient-limited enrichment directly from soil, and nutrient-limited sub-cultivation of batch enrichments consistently yielded high enrichments of Nitrosocosmicus-affiliated AOA associated with multiple canonical nitrite-oxidizing Nitrospira strains, whereas AOB numbers dropped below 0.1% and comammox Nitrospira were lost completely. Our results reveal competitiveness of Nitrosocosmicus sp. under nutrient limitation, and a likely more complex or demanding ecological niche of soil comammox Nitrospira than simulated in our nutrient-limited chemostat experiments.https://www.frontiersin.org/articles/10.3389/fmicb.2021.671480/fullnitrificationcompetitionnutrient limitationammonia-oxidizing bacteriaammonia-oxidizing archaeacomammox
collection DOAJ
language English
format Article
sources DOAJ
author Jonathan Rodriguez
Seemanti Chakrabarti
Eunkyung Choi
Nisreen Shehadeh
Samantha Sierra-Martinez
Jun Zhao
Willm Martens-Habbena
spellingShingle Jonathan Rodriguez
Seemanti Chakrabarti
Eunkyung Choi
Nisreen Shehadeh
Samantha Sierra-Martinez
Jun Zhao
Willm Martens-Habbena
Nutrient-Limited Enrichments of Nitrifiers From Soil Yield Consortia of Nitrosocosmicus-Affiliated AOA and Nitrospira-Affiliated NOB
Frontiers in Microbiology
nitrification
competition
nutrient limitation
ammonia-oxidizing bacteria
ammonia-oxidizing archaea
comammox
author_facet Jonathan Rodriguez
Seemanti Chakrabarti
Eunkyung Choi
Nisreen Shehadeh
Samantha Sierra-Martinez
Jun Zhao
Willm Martens-Habbena
author_sort Jonathan Rodriguez
title Nutrient-Limited Enrichments of Nitrifiers From Soil Yield Consortia of Nitrosocosmicus-Affiliated AOA and Nitrospira-Affiliated NOB
title_short Nutrient-Limited Enrichments of Nitrifiers From Soil Yield Consortia of Nitrosocosmicus-Affiliated AOA and Nitrospira-Affiliated NOB
title_full Nutrient-Limited Enrichments of Nitrifiers From Soil Yield Consortia of Nitrosocosmicus-Affiliated AOA and Nitrospira-Affiliated NOB
title_fullStr Nutrient-Limited Enrichments of Nitrifiers From Soil Yield Consortia of Nitrosocosmicus-Affiliated AOA and Nitrospira-Affiliated NOB
title_full_unstemmed Nutrient-Limited Enrichments of Nitrifiers From Soil Yield Consortia of Nitrosocosmicus-Affiliated AOA and Nitrospira-Affiliated NOB
title_sort nutrient-limited enrichments of nitrifiers from soil yield consortia of nitrosocosmicus-affiliated aoa and nitrospira-affiliated nob
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2021-07-01
description The discovery of ammonia-oxidizing archaea (AOA) and complete ammonia-oxidizing (comammox) bacteria widespread in terrestrial ecosystems indicates an important role of these organisms in terrestrial nitrification. Recent evidence indicated a higher ammonia affinity of comammox bacteria than of terrestrial AOA and ammonia-oxidizing bacteria (AOB), suggesting that comammox bacteria could potentially represent the most low-nutrient adapted nitrifiers in terrestrial systems. We hypothesized that a nutrient-limited enrichment strategy could exploit the differences in cellular kinetic properties and yield enrichments dominated by high affinity and high yield comammox bacteria. Using soil with a mixed community of AOA, AOB, and comammox Nitrospira, we compared performance of nutrient-limited chemostat enrichment with or without batch culture pre-enrichment in two different growth media without inhibitors or antibiotics. Monitoring of microbial community composition via 16S rRNA and amoA gene sequencing showed that batch enrichments were dominated by AOB, accompanied by low numbers of AOA and comammox Nitrospira. In contrast, nutrient-limited enrichment directly from soil, and nutrient-limited sub-cultivation of batch enrichments consistently yielded high enrichments of Nitrosocosmicus-affiliated AOA associated with multiple canonical nitrite-oxidizing Nitrospira strains, whereas AOB numbers dropped below 0.1% and comammox Nitrospira were lost completely. Our results reveal competitiveness of Nitrosocosmicus sp. under nutrient limitation, and a likely more complex or demanding ecological niche of soil comammox Nitrospira than simulated in our nutrient-limited chemostat experiments.
topic nitrification
competition
nutrient limitation
ammonia-oxidizing bacteria
ammonia-oxidizing archaea
comammox
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.671480/full
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