Differential contribution of nitrifying prokaryotes to groundwater nitrification

Markus Krüger; Narendrakumar Chaudhari; Bo Thamdrup; Will A. Overholt; Laura A. Bristow; Martin Taubert; Kirsten Küsel; Nico Jehmlich; Martin von Bergen; Martina Herrmann

doi:10.1038/s41396-023-01471-4

Differential contribution of nitrifying prokaryotes to groundwater nitrification

Markus Krüger, Narendrakumar Chaudhari, Bo Thamdrup, Will A. Overholt, Laura A. Bristow, Martin Taubert, Kirsten Küsel, Nico Jehmlich, Martin von Bergen, Martina Herrmann^*

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Abstract

The ecophysiology of complete ammonia-oxidizing bacteria (CMX) of the genus Nitrospira and their widespread occurrence in groundwater suggests that CMX bacteria have a competitive advantage over ammonia-oxidizing bacteria (AOB) and archaea (AOA) in these environments. However, the specific contribution of their activity to nitrification processes has remained unclear. We aimed to disentangle the contribution of CMX, AOA and AOB to nitrification and to identify the environmental drivers of their niche differentiation at different levels of ammonium and oxygen in oligotrophic carbonate rock aquifers. CMX ammonia monooxygenase sub-unit A (amoA) genes accounted on average for 16 to 75% of the total groundwater amoA genes detected. Nitrification rates were positively correlated to CMX clade A associated phylotypes and AOB affiliated with Nitrosomonas ureae. Short-term incubations amended with the nitrification inhibitors allylthiourea and chlorate suggested that AOB contributed a large fraction to overall ammonia oxidation, while metaproteomics analysis confirmed an active role of CMX in both ammonia and nitrite oxidation. Ecophysiological niche differentiation of CMX clades A and B, AOB and AOA was linked to their requirements for ammonium, oxygen tolerance, and metabolic versatility. Our results demonstrate that despite numerical predominance of CMX, the first step of nitrification in oligotrophic groundwater appears to be primarily governed by AOB. Higher growth yields at lower ammonia turnover rates and energy derived from nitrite oxidation most likely enable CMX to maintain consistently high populations. [Figure not available: see fulltext.]

Originalsprog	Engelsk
Tidsskrift	ISME Journal
Vol/bind	17
Udgave nummer	10
Sider (fra-til)	1601-1611
ISSN	1751-7362
DOI	https://doi.org/10.1038/s41396-023-01471-4
Status	Udgivet - okt. 2023

Bibliografisk note

Funding Information:
This study was part of the Collaborative Research Centre 1076 AquaDiva (CRC AquaDiva) of the Friedrich Schiller University Jena, funded by the Deutsche Forschungsgemeinschaft under project number 218627073. Climate chambers to conduct experiments under controlled temperature conditions and the infrastructure for high-throughput sequencing were financially supported by the Thüringer Ministerium für Wirtschaft, Wissenschaft und Digitale Gesellschaft (TMWWDG; project B 715-09075 and project 2016 FGI 0024 “BIODIV”). Martin Taubert gratefully acknowledges funding by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany´s Excellence Strategy – EXC 2051 – Project-ID 390713860. Open Access funding enabled and organized by Projekt DEAL.

Publisher Copyright:
© 2023, The Author(s).

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10.1038/s41396-023-01471-4Licens: CC BY

Open Access VersionForlagets udgivne version, 3,55 MBLicens: CC BY

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Tjek adgangen til materialet i Syddansk Universitetsbiblioteks søgemaskine

Citationsformater

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title = "Differential contribution of nitrifying prokaryotes to groundwater nitrification",

abstract = "The ecophysiology of complete ammonia-oxidizing bacteria (CMX) of the genus Nitrospira and their widespread occurrence in groundwater suggests that CMX bacteria have a competitive advantage over ammonia-oxidizing bacteria (AOB) and archaea (AOA) in these environments. However, the specific contribution of their activity to nitrification processes has remained unclear. We aimed to disentangle the contribution of CMX, AOA and AOB to nitrification and to identify the environmental drivers of their niche differentiation at different levels of ammonium and oxygen in oligotrophic carbonate rock aquifers. CMX ammonia monooxygenase sub-unit A (amoA) genes accounted on average for 16 to 75% of the total groundwater amoA genes detected. Nitrification rates were positively correlated to CMX clade A associated phylotypes and AOB affiliated with Nitrosomonas ureae. Short-term incubations amended with the nitrification inhibitors allylthiourea and chlorate suggested that AOB contributed a large fraction to overall ammonia oxidation, while metaproteomics analysis confirmed an active role of CMX in both ammonia and nitrite oxidation. Ecophysiological niche differentiation of CMX clades A and B, AOB and AOA was linked to their requirements for ammonium, oxygen tolerance, and metabolic versatility. Our results demonstrate that despite numerical predominance of CMX, the first step of nitrification in oligotrophic groundwater appears to be primarily governed by AOB. Higher growth yields at lower ammonia turnover rates and energy derived from nitrite oxidation most likely enable CMX to maintain consistently high populations. [Figure not available: see fulltext.]",

author = "Markus Kr{\"u}ger and Narendrakumar Chaudhari and Bo Thamdrup and Overholt, {Will A.} and Bristow, {Laura A.} and Martin Taubert and Kirsten K{\"u}sel and Nico Jehmlich and {von Bergen}, Martin and Martina Herrmann",

note = "Funding Information: This study was part of the Collaborative Research Centre 1076 AquaDiva (CRC AquaDiva) of the Friedrich Schiller University Jena, funded by the Deutsche Forschungsgemeinschaft under project number 218627073. Climate chambers to conduct experiments under controlled temperature conditions and the infrastructure for high-throughput sequencing were financially supported by the Th{\"u}ringer Ministerium f{\"u}r Wirtschaft, Wissenschaft und Digitale Gesellschaft (TMWWDG; project B 715-09075 and project 2016 FGI 0024 “BIODIV”). Martin Taubert gratefully acknowledges funding by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany´s Excellence Strategy – EXC 2051 – Project-ID 390713860. Open Access funding enabled and organized by Projekt DEAL. Publisher Copyright: {\textcopyright} 2023, The Author(s).",

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doi = "10.1038/s41396-023-01471-4",

language = "English",

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T1 - Differential contribution of nitrifying prokaryotes to groundwater nitrification

AU - Krüger, Markus

AU - Chaudhari, Narendrakumar

AU - Thamdrup, Bo

AU - Overholt, Will A.

AU - Bristow, Laura A.

AU - Taubert, Martin

AU - Küsel, Kirsten

AU - Jehmlich, Nico

AU - von Bergen, Martin

AU - Herrmann, Martina

N1 - Funding Information: This study was part of the Collaborative Research Centre 1076 AquaDiva (CRC AquaDiva) of the Friedrich Schiller University Jena, funded by the Deutsche Forschungsgemeinschaft under project number 218627073. Climate chambers to conduct experiments under controlled temperature conditions and the infrastructure for high-throughput sequencing were financially supported by the Thüringer Ministerium für Wirtschaft, Wissenschaft und Digitale Gesellschaft (TMWWDG; project B 715-09075 and project 2016 FGI 0024 “BIODIV”). Martin Taubert gratefully acknowledges funding by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany´s Excellence Strategy – EXC 2051 – Project-ID 390713860. Open Access funding enabled and organized by Projekt DEAL. Publisher Copyright: © 2023, The Author(s).

PY - 2023/10

Y1 - 2023/10

N2 - The ecophysiology of complete ammonia-oxidizing bacteria (CMX) of the genus Nitrospira and their widespread occurrence in groundwater suggests that CMX bacteria have a competitive advantage over ammonia-oxidizing bacteria (AOB) and archaea (AOA) in these environments. However, the specific contribution of their activity to nitrification processes has remained unclear. We aimed to disentangle the contribution of CMX, AOA and AOB to nitrification and to identify the environmental drivers of their niche differentiation at different levels of ammonium and oxygen in oligotrophic carbonate rock aquifers. CMX ammonia monooxygenase sub-unit A (amoA) genes accounted on average for 16 to 75% of the total groundwater amoA genes detected. Nitrification rates were positively correlated to CMX clade A associated phylotypes and AOB affiliated with Nitrosomonas ureae. Short-term incubations amended with the nitrification inhibitors allylthiourea and chlorate suggested that AOB contributed a large fraction to overall ammonia oxidation, while metaproteomics analysis confirmed an active role of CMX in both ammonia and nitrite oxidation. Ecophysiological niche differentiation of CMX clades A and B, AOB and AOA was linked to their requirements for ammonium, oxygen tolerance, and metabolic versatility. Our results demonstrate that despite numerical predominance of CMX, the first step of nitrification in oligotrophic groundwater appears to be primarily governed by AOB. Higher growth yields at lower ammonia turnover rates and energy derived from nitrite oxidation most likely enable CMX to maintain consistently high populations. [Figure not available: see fulltext.]

AB - The ecophysiology of complete ammonia-oxidizing bacteria (CMX) of the genus Nitrospira and their widespread occurrence in groundwater suggests that CMX bacteria have a competitive advantage over ammonia-oxidizing bacteria (AOB) and archaea (AOA) in these environments. However, the specific contribution of their activity to nitrification processes has remained unclear. We aimed to disentangle the contribution of CMX, AOA and AOB to nitrification and to identify the environmental drivers of their niche differentiation at different levels of ammonium and oxygen in oligotrophic carbonate rock aquifers. CMX ammonia monooxygenase sub-unit A (amoA) genes accounted on average for 16 to 75% of the total groundwater amoA genes detected. Nitrification rates were positively correlated to CMX clade A associated phylotypes and AOB affiliated with Nitrosomonas ureae. Short-term incubations amended with the nitrification inhibitors allylthiourea and chlorate suggested that AOB contributed a large fraction to overall ammonia oxidation, while metaproteomics analysis confirmed an active role of CMX in both ammonia and nitrite oxidation. Ecophysiological niche differentiation of CMX clades A and B, AOB and AOA was linked to their requirements for ammonium, oxygen tolerance, and metabolic versatility. Our results demonstrate that despite numerical predominance of CMX, the first step of nitrification in oligotrophic groundwater appears to be primarily governed by AOB. Higher growth yields at lower ammonia turnover rates and energy derived from nitrite oxidation most likely enable CMX to maintain consistently high populations. [Figure not available: see fulltext.]

U2 - 10.1038/s41396-023-01471-4

DO - 10.1038/s41396-023-01471-4

M3 - Journal article

C2 - 37422599

AN - SCOPUS:85164190278

SN - 1751-7362

VL - 17

SP - 1601

EP - 1611

JO - ISME Journal

JF - ISME Journal

IS - 10

ER -

Differential contribution of nitrifying prokaryotes to groundwater nitrification

Abstract

Bibliografisk note

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