ABSTRACT
Members of the verrucomicrobial clade 'Candidatus Udaeobacter' rank among the most dominant bacterial phylotypes in soil. Nevertheless, despite this global prevalence, in-depth analyses with respect to pH preferences of 'Ca. Udaeobacter' representatives are still lacking. Here, we utilized a recently designed primer pair, specifically targeting 'Ca. Udaeobacter', to investigate links between soil pH and the abundance as well as phylotype composition of this largely unexplored verrucomicrobial clade. Based on 150 forest and 150 grassland soils, comprising a broad pH range, we determined the highest total abundance of 'Ca. Udaeobacter' in strongly acidic soil (pH, ~5.1) and, noteworthy, in ultra-acidic soil (pH < 3.5) and at a pH ≥ 7, its abundance drastically declined. When we analysed the six most dominant amplicon sequence variants affiliated with 'Ca. Udaeobacter' separately, their abundances peaked within a pH range of approximately 4.7-5.2, and only in one case at slightly acidic soil pH (pH, 6.1). Our study benefits from a combination of quantitative real-time PCR and high-throughput amplicon sequencing, enabling for the first time a highly specific abundance analysis of representatives affiliated with 'Ca. Udaeobacter', which revealed that this globally abundant verrucomicrobial clade shows preferences for acidic soil.
Subject(s)
Soil Microbiology , Soil , Bacteria , Forests , Hydrogen-Ion Concentration , Soil/chemistryABSTRACT
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.
