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. 2024 Jan 8;18(1):wrae204.
doi: 10.1093/ismejo/wrae204.

Nitrate-dependent antimony oxidase in an uncultured Symbiobacteriaceae member

Liying Wang  1 , Zhipeng Yin  1 , Wei Yan  1 , Jialong Hao  2 , Fei Tian  3 , Jianbo Shi  1   4   5
Affiliations

Nitrate-dependent antimony oxidase in an uncultured Symbiobacteriaceae member

Liying Wang et al. ISME J. .

Abstract

Autotrophic antimony (Sb) oxidation coupled to nitrate reduction plays an important role in the transformation and detoxification of Sb. However, the specific oxidase involved in this process has yet to be identified. Herein, we enriched the microbiota capable of nitrate-dependent Sb(III) oxidation and identified a new Sb(III) oxidase in an uncultured member of Symbiobacteriaceae. Incubation experiments demonstrated that nitrate-dependent Sb(III) oxidation occurred in the microcosm supplemented with Sb(III) and nitrate. Both the 16S rRNA gene and metagenomic analyses indicated that a species within Symbiobacteriaceae played a crucial role in this process. Furthermore, carbon-13 isotope labeling with carbon dioxide-fixing Rhodopseudomonas palustris in combination with nanoscale secondary ion mass spectrometry revealed that a newly characterized oxidase from the dimethylsulfoxide reductase family, designated as NaoABC, was responsible for autotrophic Sb(III) oxidation coupled with nitrate reduction. The NaoABC complex functions in conjunction with the nitrate reductase NarGHI, forming a redox loop that transfers electrons from Sb(III) to nitrate, thereby generating the energy necessary for autotrophic growth. This research offers new insights into the understanding of how microbes link Sb and nitrogen biogeochemical cycles in the environment.

Keywords: Symbiobacteriaceae; antimony oxidase; nitrate-dependent Sb(III) oxidation.

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Conflict of interest statement

None declared.

Figures

Figure 1
Figure 1
The detection of microbial Sb(III) oxidation coupled to NO3− reduction. Time-dependent concentration of dissolved Sb(III) (A), Sb(V) (B), NO3− (C), and NO2− (D) in the microcosm of soil + Sb(III), soil + NO3−, soil + Sb(III) + NO3−, negative control soil, soil + Sb(III) + NO3− + azide, and soil. The percentage of N products (E), NO was calculated by deducing those of NO2−, N2O, N2, and NH4+. Time-dependent concentration of dissolved Fe(II) (F), labile Fe(III) (G), and the amount of abiotic Sb(III) oxidation by labile Fe(III) as measured by adding 1 mM Sb(III) to the precipitates obtained from respective soil microcosm (H). Correlation analysis between soluble NO3− and Sb(V) in soil + Sb(III) + NO3− incubation (I). Error bars represent the standard deviations of means of triplicates.
Figure 2
Figure 2
Identification of functional microbes for nitrate-dependent Sb(III) oxidation by LEfSe analysis. Comparative analysis of the differential abundance microbes at the species level among microcosms of soil, soil + NO3−, soil + Sb(III), and soil + Sb(III) + NO3−. The term “unclassified” refers to microbial strains that have not yet been definitively assigned to a particular species in the database.
Figure 3
Figure 3
Counts of genes responsible for Sb, N, and C metabolism detected in the metagenome-assembled genomes from the microcosm of soil + Sb(III) + NO3−. The genes narG, napA, nasA, nirK, nirS, norB, and nosZ are responsible for denitrification; nirB, nrfA, and nrfB for the dissimilatory nitrate reduction to ammonium (DNRA). The genes korA, korB, porA, and porB are responsible for the reductive citrate cycle (rTCA cycle); atoB, ppcA, abfD, ppsA, mcr, and ppc for the 3-hydroxypropionate/4-hydroxybutyrate (3-HP/4-HB cycle); cbbL and cbbM for the Calvin cycle (Calvin); and acsA and acsB for the reductive acetyl-CoA pathway (Wood–Ljungdahl). “WL” refers to Wood–Ljungdahl. The genes arsR, arsB/acr3, arsA, and arsH are responsible for Sb(III) resistance; aioAB and naoABC for Sb(III) oxidation.
Figure 4
Figure 4
Functional genes for nitrate-dependent Sb(III) oxidation in uncultured Symbiobacteriaceae. Organization of nao and nar clusters possibly functioned as coupling Sb(III) oxidation with nitrate reduction (A). nao1 and nao2 cluster encoding Sb(III) oxidase, and nar for nitrate reductase. ORF represents the open reading frame which is annotated as hypothetical protein. Phylogenetic affiliation of the Mo-bioMGD unit NaoA (B), and Fe-S units NaoB and NaoC (C) in the unrooted trees constructed using representative sequences of the catalytic subunit, and iron–sulfur subunit of the DMSOR members. Aio, arsenite oxidase; Fdn, formate dehydrogenase; nap, periplasmic nitrate reductase; YnfF/Dms, dimethyl sulfoxide reductase; Bis, biotinsulfoxide reductase; tor, trimethylamineoxide reductase; Ser, selenate reductase; Nar, membrane-associated nitrate reductase; Arr, arsenate respiratory reductase; Psr, polysulfide reductase; Arx, arsenite oxidase; Frd, fumarate reductase; Anr, antimony reductase. Values in parentheses represent the number of sequences used. Scale bar represents the amino acid change on the branch of the length unit.
Figure 5
Figure 5
Autotrophic oxidation of Sb(III) in recombinant R. palustris enhanced by IPTG. The amount of Sb(III) oxidation (A), cell number monitored over time (B), 13C incorporation by the isotope ratio mass spectrometry analysis (C), nano-SIMS images of 13C (D, F, and H) and 12C14N (as indicator of biomass) (E, G, and I) in the incubation with Sb(III) and nitrate (autotrophic condition), and images of 13C (J, L, and N) and 12C14N (K, M, and O) in the incubation with only nitrate (control condition). IPTG-control stands for R. palustris-pCE2TA, IPTG-Nao1 for R. palustris-pCE2TA-nao1, and IPTG-Nao2 for R. palustris-pCE2TA-nao2 induced by IPTG. Error bars represent the standard deviations of means of triplicates. Scale bars, 2 μm. Vertical scale bars on the right indicate 13C or 12C14N atom percent. Asterisks indicate IPTG-Nao1 and IPTG-Nao2 significantly differ from IPTG-control (***P < .001).
Figure 6
Figure 6
Schematic diagram for the enzymatic mechanism of nitrate-dependent Sb(III) oxidation in uncultured Symbiobacteriaceae species. Sb(III) donates electrons and is oxidized by the NaoABC complex. Subsequently, these electrons are transferred to the quinone pool. Finally, the reduced quinols convey the electrons to the membrane-bound nitrate reductase complex NarGHI, where nitrate is reduced. In this Nao-quinol-Nar chain, the transfer of electrons from Sb(III) to nitrate is coupled with the generation of a proton motive force across the cytoplasmic membrane.
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