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Globally Abundant “Candidatus Udaeobacter” Benefits from Release of Antibiotics in Soil and Potentially Performs Trace Gas Scavenging

Verrucomicrobia affiliated with “Candidatus Udaeobacter” belong to the most abundant soil bacteria worldwide. Although the synthesis of antibiotics presumably evolved in soil, and environmental pollution with antimicrobials increases, the impact of these complex molecules on “Ca. Udaeobacter” remain...

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Autores principales: Willms, Inka M., Rudolph, Anina Y., Göschel, Isabell, Bolz, Simon H., Schneider, Dominik, Penone, Caterina, Poehlein, Anja, Schöning, Ingo, Nacke, Heiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7343977/
https://www.ncbi.nlm.nih.gov/pubmed/32641424
http://dx.doi.org/10.1128/mSphere.00186-20
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author Willms, Inka M.
Rudolph, Anina Y.
Göschel, Isabell
Bolz, Simon H.
Schneider, Dominik
Penone, Caterina
Poehlein, Anja
Schöning, Ingo
Nacke, Heiko
author_facet Willms, Inka M.
Rudolph, Anina Y.
Göschel, Isabell
Bolz, Simon H.
Schneider, Dominik
Penone, Caterina
Poehlein, Anja
Schöning, Ingo
Nacke, Heiko
author_sort Willms, Inka M.
collection PubMed
description Verrucomicrobia affiliated with “Candidatus Udaeobacter” belong to the most abundant soil bacteria worldwide. Although the synthesis of antibiotics presumably evolved in soil, and environmental pollution with antimicrobials increases, the impact of these complex molecules on “Ca. Udaeobacter” remains to be elucidated. In this study, we demonstrate that “Ca. Udaeobacter” representatives residing in grassland as well as forest soil ecosystems show multidrug resistance and even take advantage of antibiotics release. Soils treated with up to six different antibiotics exhibited a higher “Ca. Udaeobacter” abundance than corresponding controls after 3, 8, and 20 days of incubation. In this context, we provide evidence that “Ca. Udaeobacter” representatives may utilize nutrients which are released due to antibiotic-driven lysis of other soil microbes and thereby reduce energetically expensive synthesis of required biomolecules. Moreover, genomic analysis revealed the presence of genes conferring resistance to multiple classes of antibiotics and indicated that “Ca. Udaeobacter” representatives most likely oxidize the trace gas H(2) to generate energy. This energy might be required for long-term persistence in terrestrial habitats, as already suggested for other dominant soil bacteria. Our study illustrates, for the first time, that globally abundant “Ca. Udaeobacter” benefits from release of antibiotics, which confers advantages over other soil bacteria and represents a so-far overlooked fundamental lifestyle feature of this poorly characterized verrucomicrobial genus. Furthermore, our study suggests that “Ca. Udaeobacter” representatives can utilize H(2) as an alternative electron donor. IMPORTANCE Soil bacteria have been investigated for more than a century, but one of the most dominant terrestrial groups on Earth, “Candidatus Udaeobacter,” remains elusive and largely unexplored. Its natural habitat is considered a major reservoir of antibiotics, which directly or indirectly impact phylogenetically diverse microorganisms. Here, we found that “Ca. Udaeobacter” representatives exhibit multidrug resistance and not only evade harmful effects of antimicrobials but even benefit from antibiotic pressure in soil. Therefore, “Ca. Udaeobacter” evidently affects the composition of soil resistomes worldwide and might represent a winner of rising environmental pollution with antimicrobials. In addition, our study indicates that “Ca. Udaeobacter” representatives utilize H(2) and thereby contribute to global hydrogen cycling. The here-reported findings provide insights into elementary lifestyle features of “Ca. Udaeobacter,” potentially contributing to its successful global dissemination.
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spelling pubmed-73439772020-07-10 Globally Abundant “Candidatus Udaeobacter” Benefits from Release of Antibiotics in Soil and Potentially Performs Trace Gas Scavenging Willms, Inka M. Rudolph, Anina Y. Göschel, Isabell Bolz, Simon H. Schneider, Dominik Penone, Caterina Poehlein, Anja Schöning, Ingo Nacke, Heiko mSphere Research Article Verrucomicrobia affiliated with “Candidatus Udaeobacter” belong to the most abundant soil bacteria worldwide. Although the synthesis of antibiotics presumably evolved in soil, and environmental pollution with antimicrobials increases, the impact of these complex molecules on “Ca. Udaeobacter” remains to be elucidated. In this study, we demonstrate that “Ca. Udaeobacter” representatives residing in grassland as well as forest soil ecosystems show multidrug resistance and even take advantage of antibiotics release. Soils treated with up to six different antibiotics exhibited a higher “Ca. Udaeobacter” abundance than corresponding controls after 3, 8, and 20 days of incubation. In this context, we provide evidence that “Ca. Udaeobacter” representatives may utilize nutrients which are released due to antibiotic-driven lysis of other soil microbes and thereby reduce energetically expensive synthesis of required biomolecules. Moreover, genomic analysis revealed the presence of genes conferring resistance to multiple classes of antibiotics and indicated that “Ca. Udaeobacter” representatives most likely oxidize the trace gas H(2) to generate energy. This energy might be required for long-term persistence in terrestrial habitats, as already suggested for other dominant soil bacteria. Our study illustrates, for the first time, that globally abundant “Ca. Udaeobacter” benefits from release of antibiotics, which confers advantages over other soil bacteria and represents a so-far overlooked fundamental lifestyle feature of this poorly characterized verrucomicrobial genus. Furthermore, our study suggests that “Ca. Udaeobacter” representatives can utilize H(2) as an alternative electron donor. IMPORTANCE Soil bacteria have been investigated for more than a century, but one of the most dominant terrestrial groups on Earth, “Candidatus Udaeobacter,” remains elusive and largely unexplored. Its natural habitat is considered a major reservoir of antibiotics, which directly or indirectly impact phylogenetically diverse microorganisms. Here, we found that “Ca. Udaeobacter” representatives exhibit multidrug resistance and not only evade harmful effects of antimicrobials but even benefit from antibiotic pressure in soil. Therefore, “Ca. Udaeobacter” evidently affects the composition of soil resistomes worldwide and might represent a winner of rising environmental pollution with antimicrobials. In addition, our study indicates that “Ca. Udaeobacter” representatives utilize H(2) and thereby contribute to global hydrogen cycling. The here-reported findings provide insights into elementary lifestyle features of “Ca. Udaeobacter,” potentially contributing to its successful global dissemination. American Society for Microbiology 2020-07-08 /pmc/articles/PMC7343977/ /pubmed/32641424 http://dx.doi.org/10.1128/mSphere.00186-20 Text en Copyright © 2020 Willms et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Willms, Inka M.
Rudolph, Anina Y.
Göschel, Isabell
Bolz, Simon H.
Schneider, Dominik
Penone, Caterina
Poehlein, Anja
Schöning, Ingo
Nacke, Heiko
Globally Abundant “Candidatus Udaeobacter” Benefits from Release of Antibiotics in Soil and Potentially Performs Trace Gas Scavenging
title Globally Abundant “Candidatus Udaeobacter” Benefits from Release of Antibiotics in Soil and Potentially Performs Trace Gas Scavenging
title_full Globally Abundant “Candidatus Udaeobacter” Benefits from Release of Antibiotics in Soil and Potentially Performs Trace Gas Scavenging
title_fullStr Globally Abundant “Candidatus Udaeobacter” Benefits from Release of Antibiotics in Soil and Potentially Performs Trace Gas Scavenging
title_full_unstemmed Globally Abundant “Candidatus Udaeobacter” Benefits from Release of Antibiotics in Soil and Potentially Performs Trace Gas Scavenging
title_short Globally Abundant “Candidatus Udaeobacter” Benefits from Release of Antibiotics in Soil and Potentially Performs Trace Gas Scavenging
title_sort globally abundant “candidatus udaeobacter” benefits from release of antibiotics in soil and potentially performs trace gas scavenging
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7343977/
https://www.ncbi.nlm.nih.gov/pubmed/32641424
http://dx.doi.org/10.1128/mSphere.00186-20
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