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Ammonia-Oligotrophic and Diazotrophic Heavy Metal-Resistant Serratia liquefaciens Strains from Pioneer Plants and Mine Tailings

  • Environmental Microbiology
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Abstract

Mine tailings are man-made environments characterized by low levels of organic carbon and assimilable nitrogen, as well as moderate concentrations of heavy metals. For the introduction of nitrogen into these environments, a key role is played by ammonia-oligotrophic/diazotrophic heavy metal-resistant guilds. In mine tailings from Zacatecas, Mexico, Serratia liquefaciens was the dominant heterotrophic culturable species isolated in N-free media from bulk mine tailings as well as the rhizosphere, roots, and aerial parts of pioneer plants. S. liquefaciens strains proved to be a meta-population with high intraspecific genetic diversity and a potential to respond to these extreme conditions. The phenotypic and genotypic features of these strains reveal the potential adaptation of S. liquefaciens to oligotrophic and nitrogen-limited mine tailings with high concentrations of heavy metals. These features include ammonia-oligotrophic growth, nitrogen fixation, siderophore and indoleacetic acid production, phosphate solubilization, biofilm formation, moderate tolerance to heavy metals under conditions of diverse nitrogen availability, and the presence of zntA, amtB, and nifH genes. The acetylene reduction assay suggests low nitrogen-fixing activity. The nifH gene was harbored in a plasmid of ∼60 kb and probably was acquired by a horizontal gene transfer event from Klebsiella variicola.

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Acknowledgments

All the authors thank Bruce Allan Larsen for reviewing the English version of this manuscript, and Luc Dendooven (CINVESTAV, IPN) for supporting the GC analyses. L.Z.-M., L H.-S., and E.G.-C. thank CONACYT for graduate scholarships awarded and also PIFI/BEIFI-IPN for a scholarship complement. L.V.-T. and C.H.-R. are fellows of EDI-IPN, COFAA-IPN, and SNI-CONACYT, with grants 20131171, 20141333, 20150981, and 20161850 from SIP-IPN.

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  1. Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Prol. de Carpio y Plan de Ayala s/n. Col. Sto. Tomás, 11340, Mexico, D.F., Mexico

    Lily X. Zelaya-Molina, Luis M. Hernández-Soto, Jairo E. Guerra-Camacho, Lourdes Villa-Tanaca & César Hernández-Rodríguez

  2. Departamento de Ingeniería Bioquímica, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Prol. de Carpio y Plan de Ayala s/n. Col. Sto. Tomás, 11340, Mexico, D.F., Mexico

    Ricardo Monterrubio-López

  3. Departamento de Botánica, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Prol. de Carpio y Plan de Ayala s/n. Col. Sto. Tomás, 11340, Mexico, D.F., Mexico

    Alfredo Patiño-Siciliano

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  1. Lily X. Zelaya-Molina
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ESM 1

Figure S1. PCR-DGGE banding profiles of the V6-V8 region of the 16S rRNA gene from non-rhizospheric mine tailings. Lanes 1, 2 and 3: Gualterio old mill of three different strata of a mine-tailing profile 40 cm high. Lane 1 and 2 correspond to the first and second strata. Lane 4: San Pantaleon trademill sample. Lane 5: San Martin drying lagoon sample. T: Bands identified as Thiobacillus sp.. S: Bands identified as Serratia liquefaciens. Th: Thermosporothrix hazakensis, Ub: uncultured bacterium (PDF 475 kb)

ESM 2

Figure S2. Maximum likelihood phylogenetic tree of the V6-V8 region of the 16S rRNA gene of S. liquefaciens sequences, constructed from DGGE-bands and haplotypes of the culturable strains. The Kimura 2-parameter substitution model was used. The numbers at the nodes indicate bootstrap values of 1000 replicates. Branch lengths are proportional to the number of substitutions per site (see scale bar). The sequence of Escherichia coli X80725 was used as outgroup. (PDF 15 kb)

ESM 3

Figure S3. DNA polymorphism example of some Serratia liquefaciens strains generated with RAPD-PCR. Fingerprintings were generated with primers a) ROTH A03 and b) MFG17. Strain in lane 1: 388, lane 2: 392, lane 3: 405, lane 4: 406, lane 5: 412, lane 6: 451, lane 7: 456, lane 8: 479, lane 9: 493, lane 10: 604, lane 11: 616, lane 12: 642. M: 1 kb DNA ladder. (PDF 28 kb)

ESM 4

Figure S4. Plasmidic DNAs from five Serratia liquefaciens strains. Lane 1: plasmids of Escherichia coli V517. Lanes 2-6: S. liquefaciens strains. Strain in lane 2: 450, lane 3: 661, lane 4: 406, lane 5: 219, lane 5: 47, and lane 6: 227. (PDF 44 kb)

ESM 5

Table S1. Conditions of biofilm formation of Serratia liquefaciens strains. (DOCX 17 kb)

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Zelaya-Molina, L.X., Hernández-Soto, L.M., Guerra-Camacho, J.E. et al. Ammonia-Oligotrophic and Diazotrophic Heavy Metal-Resistant Serratia liquefaciens Strains from Pioneer Plants and Mine Tailings. Microb Ecol 72, 324–346 (2016). https://doi.org/10.1007/s00248-016-0771-3

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