Globally Abundant “<italic toggle="yes">Candidatus</italic> Udaeobacter” Benefits from Release of Antibiotics in Soil and Potentially Performs Trace Gas Scavenging

ABSTRACT 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. Udaeobacte...

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Autores principales:	Inka M. Willms, Anina Y. Rudolph, Isabell Göschel, Simon H. Bolz, Dominik Schneider, Caterina Penone, Anja Poehlein, Ingo Schöning, Heiko Nacke
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Candidatus Udaeobacter soil antibiotics antibiotic resistance Verrucomicrobia Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b22b90cb7fbf4c74856426aec6ec752d
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spelling	oai:doaj.org-article:b22b90cb7fbf4c74856426aec6ec752d2021-11-15T15:30:51ZGlobally Abundant “<italic toggle="yes">Candidatus</italic> Udaeobacter” Benefits from Release of Antibiotics in Soil and Potentially Performs Trace Gas Scavenging10.1128/mSphere.00186-202379-5042https://doaj.org/article/b22b90cb7fbf4c74856426aec6ec752d2020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00186-20https://doaj.org/toc/2379-5042ABSTRACT 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 H2 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 H2 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 H2 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.Inka M. WillmsAnina Y. RudolphIsabell GöschelSimon H. BolzDominik SchneiderCaterina PenoneAnja PoehleinIngo SchöningHeiko NackeAmerican Society for MicrobiologyarticleCandidatus Udaeobactersoilantibioticsantibiotic resistanceVerrucomicrobiaMicrobiologyQR1-502ENmSphere, Vol 5, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Candidatus Udaeobacter soil antibiotics antibiotic resistance Verrucomicrobia Microbiology QR1-502
spellingShingle	Candidatus Udaeobacter soil antibiotics antibiotic resistance Verrucomicrobia Microbiology QR1-502 Inka M. Willms Anina Y. Rudolph Isabell Göschel Simon H. Bolz Dominik Schneider Caterina Penone Anja Poehlein Ingo Schöning Heiko Nacke Globally Abundant “<italic toggle="yes">Candidatus</italic> Udaeobacter” Benefits from Release of Antibiotics in Soil and Potentially Performs Trace Gas Scavenging
description	ABSTRACT 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 H2 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 H2 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 H2 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.
format	article
author	Inka M. Willms Anina Y. Rudolph Isabell Göschel Simon H. Bolz Dominik Schneider Caterina Penone Anja Poehlein Ingo Schöning Heiko Nacke
author_facet	Inka M. Willms Anina Y. Rudolph Isabell Göschel Simon H. Bolz Dominik Schneider Caterina Penone Anja Poehlein Ingo Schöning Heiko Nacke
author_sort	Inka M. Willms
title	Globally Abundant “<italic toggle="yes">Candidatus</italic> Udaeobacter” Benefits from Release of Antibiotics in Soil and Potentially Performs Trace Gas Scavenging
title_short	Globally Abundant “<italic toggle="yes">Candidatus</italic> Udaeobacter” Benefits from Release of Antibiotics in Soil and Potentially Performs Trace Gas Scavenging
title_full	Globally Abundant “<italic toggle="yes">Candidatus</italic> Udaeobacter” Benefits from Release of Antibiotics in Soil and Potentially Performs Trace Gas Scavenging
title_fullStr	Globally Abundant “<italic toggle="yes">Candidatus</italic> Udaeobacter” Benefits from Release of Antibiotics in Soil and Potentially Performs Trace Gas Scavenging
title_full_unstemmed	Globally Abundant “<italic toggle="yes">Candidatus</italic> Udaeobacter” Benefits from Release of Antibiotics in Soil and Potentially Performs Trace Gas Scavenging
title_sort	globally abundant “<italic toggle="yes">candidatus</italic> udaeobacter” benefits from release of antibiotics in soil and potentially performs trace gas scavenging
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/b22b90cb7fbf4c74856426aec6ec752d
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Globally Abundant “<italic toggle="yes">Candidatus</italic> Udaeobacter” Benefits from Release of Antibiotics in Soil and Potentially Performs Trace Gas Scavenging

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