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Globally Abundant "Candidatus 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 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.

SUBMITTER: Willms IM

PROVIDER: S-EPMC7343977 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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

Willms Inka M IM Rudolph Anina Y AY Göschel Isabell I Bolz Simon H SH Schneider Dominik D Penone Caterina C Poehlein Anja A Schöning Ingo I Nacke Heiko H

mSphere 20200708 4

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 an ...[more]

PMID: 32641424

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Project description:The ability of "Candidatus Accumulibacter phosphatis" to grow and remove phosphorus from wastewater under cycling anaerobic and aerobic conditions has also been investigated as a metabolism that could lead to simultaneous removal of nitrogen and phosphorus by a single organism. However, although phosphorus removal under cyclic anaerobic and anoxic conditions has been demonstrated, clarifying the role of "Ca. Accumulibacter phosphatis" in this process has been challenging, since (i) experimental research describes contradictory findings, (ii) none of the published "Ca. Accumulibacter phosphatis" genomes show the existence of a complete respiratory pathway for denitrification, and (iii) some genomes lacking a complete respiratory pathway have genes for assimilatory nitrate reduction. In this study, we used an integrated omics analysis to elucidate the physiology of a "Ca. Accumulibacter phosphatis" strain enriched in a reactor operated under cyclic anaerobic and microaerobic conditions. The reactor's performance suggested the ability of the enriched "Ca. Accumulibacter phosphatis" strain (clade IC) to simultaneously use oxygen and nitrate as electron acceptors under microaerobic conditions. A draft genome of this organism was assembled from metagenomic reads ("Ca. Accumulibacter phosphatis" UW-LDO-IC) and used as a reference to examine transcript abundance throughout one reactor cycle. The genome of UW-LDO-IC revealed the presence of a full pathway for respiratory denitrification. The observed transcript abundance patterns showed evidence of coregulation of the denitrifying genes along with a cbb3 cytochrome, which has been characterized as having high affinity for oxygen. Furthermore, we identified an FNR-like binding motif upstream of the coregulated genes, suggesting transcription-level regulation of both denitrifying and respiratory pathways in UW-LDO-IC. Taking the results together, the omics analysis provides strong evidence that "Ca. Accumulibacter phosphatis" UW-LDO-IC uses oxygen and nitrate simultaneously as electron acceptors under microaerobic conditions. IMPORTANCE "Candidatus Accumulibacter phosphatis" is widely found in full-scale wastewater treatment plants, where it has been identified as the key organism for biological removal of phosphorus. Since aeration can account for 50% of the energy use during wastewater treatment, microaerobic conditions for wastewater treatment have emerged as a cost-effective alternative to conventional biological nutrient removal processes. Our report provides strong genomics-based evidence not only that "Ca. Accumulibacter phosphatis" is the main organism contributing to phosphorus removal under microaerobic conditions but also that this organism simultaneously respires nitrate and oxygen in this environment, consequently removing nitrogen and phosphorus from the wastewater. Such activity could be harnessed in innovative designs for cost-effective and energy-efficient optimization of wastewater treatment systems.

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Dataset Information

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

Publications

Globally Abundant "<i>Candidatus</i> Udaeobacter" Benefits from Release of Antibiotics in Soil and Potentially Performs Trace Gas Scavenging.

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