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Cited by 13Antibiotic Resistance in BacteriaPharmaceutical and Antibiotic Environmental ImpactsAnaerobic Digestion and Biogas Production

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Antibiotic-Resistant Desulfovibrio Produces H2S from Supplements for Animal Farming

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Karnachuk, Olga V., Beletsky, Alexey V., Rakitin, Andrey L., Ikkert, Olga P., Avakyan, Marat R., Zyusman, Viacheslav S., Napilov, Andrei, Mardanov, Andrey V., Ravin, Nikolai V.·2023·Microorganisms
DOI 10.3390/microorganisms11040838PMC PMC10146906
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Abstract

Sulphate-reducing bacteria, primarily Desulfovibrio, are responsible for the active generation of H2S in swine production waste. The model species for sulphate reduction studies, Desulfovibrio vulgaris strain L2, was previously isolated from swine manure characterized by high rates of dissimilatory sulphate reduction. The source of electron acceptors in low-sulphate swine waste for the high rate of H2S formation remains uncertain. Here, we demonstrate the ability of the L2 strain to use common animal farming supplements including L-lysine-sulphate, gypsum and gypsum plasterboards as electron acceptors for H2S production. Genome sequencing of strain L2 revealed the presence of two megaplasmids and predicted resistance to various antimicrobials and mercury, which was confirmed in physiological experiments. Most of antibiotic resistance genes (ARG) are carried by two class 1 integrons located on the chromosome and on the plasmid pDsulf-L2-2. These ARGs, predicted to confer resistance to beta-lactams, aminoglycosides, lincosamides, sulphonamides, chloramphenicol and tetracycline, were probably laterally acquired from various Gammaproteobacteria and Firmicutes. Resistance to mercury is likely enabled by two mer operons also located on the chromosome and on pDsulf-L2-2 and acquired via horizontal gene transfer. The second megaplasmid, pDsulf-L2-1, encoded nitrogenase, catalase and type III secretion system suggesting close contact of the strain with intestinal cells in the swine gut. The location of ARGs on mobile elements allows us to consider D. vulgaris strain L2 as a possible vector transferring antimicrobials resistance determinants between the gut microbiote and microbial communities in environmental biotopes.

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Figure 1 X-ray diffraction patterns of (A) gypsum and (B) gypsum plasterboard. The diagnostic peaks for gypsum CaSO4 2H2O (●) are indicated. Letter code: Ab = albite, NaAlSi3O8. The vertical bar shows the scale of relative counts.
Figure 1 X-ray diffraction patterns of (A) gypsum and (B) gypsum plasterboard. The diagnostic peaks for gypsum CaSO4 2H2O (●) are indicated. Letter code: Ab = albite, NaAlSi3O8. The vertical bar shows the scale of relative counts.CC BY · PubMed Central
Figure 2 (A,B) TEM micrographs of ultrathin layers of strain L2 and (C) Phylogenetic position of D. vulgaris strain L2 inferred using neighbor-joining inference on the 120 concatenated single copy marker proteins. The optimal tree is shown. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1000 replicates) are shown next to the branches. The tree is drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic tree. The evolutionary distances were computed using the Poisson correction method and are in the units of the number of amino acid substitutions per site. All ambiguous positions were removed for each sequence pair (pairwise deletion option). There was a total of 5040 positions in the final dataset. Evolutionary analyses were conducted in MEGA11.
Figure 2 (A,B) TEM micrographs of ultrathin layers of strain L2 and (C) Phylogenetic position of D. vulgaris strain L2 inferred using neighbor-joining inference on the 120 concatenated single copy marker proteins. The optimal tree is shown. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1000 replicates) are shown next to the branches. The tree is drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic tree. The evolutionary distances were computed using the Poisson correction method and are in the units of the number of amino acid substitutions per site. All ambiguous positions were removed for each sequence pair (pairwise deletion option). There was a total of 5040 positions in the final dataset. Evolutionary analyses were conducted in MEGA11.CC BY · PubMed Central
Figure 3 (A) Growth of strain L2 with Na2SO4, gypsum (CaSO4 2H2O), gypsum plasterboard and L-lysine sulphate (2(C6H14N2O2). H2SO4) as the sole electron acceptor and (B) H2S production during growth with Na2SO4, gypsum (CaSO4. 2H2O), gypsum plasterboard and L-lysine sulphate (2(C6H14N2O2). H2SO4): ▲ Na2SO4 (triangles); ♦ gypsum (diamonds); ○ gypsum plasterboard (circles); □ L-lysine sulphate (squares).
Figure 3 (A) Growth of strain L2 with Na2SO4, gypsum (CaSO4 2H2O), gypsum plasterboard and L-lysine sulphate (2(C6H14N2O2). H2SO4) as the sole electron acceptor and (B) H2S production during growth with Na2SO4, gypsum (CaSO4. 2H2O), gypsum plasterboard and L-lysine sulphate (2(C6H14N2O2). H2SO4): ▲ Na2SO4 (triangles); ♦ gypsum (diamonds); ○ gypsum plasterboard (circles); □ L-lysine sulphate (squares).CC BY · PubMed Central
Figure 4 Integrons carrying antibiotic resistance genes on the chromosome and plasmid pDsulf-L2-2. Genes are represented by arrows. Transposase genes are shown by gray arrows; black arrows indicate genes encoding the conjugate transfer protein and the hypothetical protein. Gray areas highlight regions of sequence identity (>99%) between the plasmid and the chromosome.
Figure 4 Integrons carrying antibiotic resistance genes on the chromosome and plasmid pDsulf-L2-2. Genes are represented by arrows. Transposase genes are shown by gray arrows; black arrows indicate genes encoding the conjugate transfer protein and the hypothetical protein. Gray areas highlight regions of sequence identity (>99%) between the plasmid and the chromosome.CC BY · PubMed Central

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Cited by

  • Current Concepts in Probiotic Safety and Efficacy

    Churin, A. A., Sokolyanskaya, L. O., Lukina, A. P., & Karnachuk, O. V. (2026) · Nutrients · doi:10.3390/nu18040696 · Cited by 31

    “The identification of mobile antimicrobial resistance genes and their potential impact on intestinal resistance also requires whole-genome sequencing and detailed characterization of antibiotic resistance genes [42,66–68].”
    Self-citation

See all 13

Metadata

Authors
Karnachuk, O. V., Beletsky, A. V., Rakitin, A. L., Ikkert, O. P., Avakyan, M. R., Zyusman, V. S., Napilov, A., Mardanov, A. V., & Ravin, N. V.
Affiliations
  • National Research Tomsk State University (RU)
  • Russian Academy of Sciences (RU)
Corresponding author
Karnachuk, Olga V.
ORCID
Venue
Microorganisms
Publisher
MDPI AG
Published
2023-03-25
Volume
11
Issue
4
Pages
838
ISSN
2076-2607 (ISSN-L)
DOI
10.3390/microorganisms11040838
PMC
PMC10146906
OpenAlex
W4361006555
Cited by
13
References
0
Citations by year
2026: 4 · 2025: 4 · 2024: 3 · 2023: 2
FWCI
1.11
Type
journal article
Language
en
Open access
Licence
Locations
  • Microorganisms (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Ministry of Science (Agreement № 075-15-2021-1401)
Topics
  • Health Sciences › Medicine › Microbiology (medical) › Antibiotic Resistance in Bacteria
  • Physical Sciences › Environmental Science › Pollution › Pharmaceutical and Antibiotic Environmental Impacts
  • Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Anaerobic Digestion and Biogas Production
Keywords
hydrogen sulfide production, sulfate-reducing bacteria, pig manure, antibiotic resistance genes, class 1 integron, megaplasmid, horizontal gene transfer, mercury resistance, mer operon, gypsum, beta-lactam resistance, aminoglycoside resistance, type III secretion system, nitrogenase, swine gut microbiota

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CoChat. (2026). Citation check: Antibiotic-Resistant Desulfovibrio Produces H2S from Supplements for Animal Farming. https://app.cochat.ai/papers/10.3390/microorganisms11040838
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Karnachuk, O. V., Beletsky, A. V., Rakitin, A. L., Ikkert, O. P., Avakyan, M. R., Zyusman, V. S., Napilov, A., Mardanov, A. V., & Ravin, N. V. (2023). Antibiotic-Resistant Desulfovibrio Produces H2S from Supplements for Animal Farming. Microorganisms. https://doi.org/10.3390/microorganisms11040838