1887

Abstract

Understanding the molecular underpinnings of manganese oxidation in SS1 has been hampered by the lack of a genetic system. In this report, we describe the development of a genetic system for SS1. The antibiotic sensitivity was characterized, and a procedure for transformation with exogenous DNA via conjugation was developed and optimized, resulting in a maximum transfer frequency of 5.2×10 and a typical transfer frequency of the order of 1×10 transconjugants per donor. Genetic manipulation of SS1 was demonstrated by disrupting via chromosomal integration with a plasmid containing a R6Kγ origin of replication through homologous recombination. This resulted in resistance to 5-fluoroorotidine, which was abolished by complementation with an ectopically expressed copy of cloned into pBBR1MCS. This system is expected to be amenable to a systematic genetic analysis of SS1, including those genes responsible for manganese oxidation.

Funding
This study was supported by the:
  • , NSF , (Award EAR-031 1767)
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2014-11-01
2021-03-08
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References

  1. Adams L. F., Ghiorse W. C. ( 1986). Physiology and ultrastructure of Leptothrix discophora SS-1. Arch Microbiol 145:126–135 [CrossRef]
    [Google Scholar]
  2. Adams L. F., Ghiorse W. C. ( 1987). Characterization of extracellular Mn2+-oxidizing activity and isolation of an Mn2+-oxidizing protein from Leptothrix discophora SS-1. J Bacteriol 169:1279–1285[PubMed]
    [Google Scholar]
  3. Adelberg E. A., Pittard J. ( 1965). Chromosome transfer in bacterial conjugation. Bacteriol Rev 29:161–172[PubMed]
    [Google Scholar]
  4. Aminov R. I. ( 2011). Horizontal gene exchange in environmental microbiota. Front Microbiol 2:158 [CrossRef][PubMed]
    [Google Scholar]
  5. Anderson C. R., Johnson H. A., Caputo N., Davis R. E., Torpey J. W., Tebo B. M. ( 2009). Mn(II) oxidation is catalyzed by heme peroxidases in “Aurantimonas manganoxydans” strain SI85-9A1 and Erythrobacter sp. strain SD-21. Appl Environ Microbiol 75:4130–4138 [CrossRef][PubMed]
    [Google Scholar]
  6. Bitan-Banin G., Ortenberg R., Mevarech M. ( 2003). Development of a gene knockout system for the halophilic archaeon Haloferax volcanii by use of the pyrE gene. J Bacteriol 185:772–778 [CrossRef][PubMed]
    [Google Scholar]
  7. Brouwers G.-J. ( 1999). Molecular genetic aspects of microbial manganese oxidation: a geophysiological study Leiden University; Leiden, the Netherlands:
    [Google Scholar]
  8. Butterfield C. N., Soldatova A. V., Lee S. W., Spiro T. G., Tebo B. M. ( 2013). Mn(II,III) oxidation and MnO2 mineralization by an expressed bacterial multicopper oxidase. Proc Natl Acad Sci U S A 110:11731–11735 [CrossRef][PubMed]
    [Google Scholar]
  9. Chen I., Christie P. J., Dubnau D. ( 2005). The ins and outs of DNA transfer in bacteria. Science 310:1456–1460 [CrossRef][PubMed]
    [Google Scholar]
  10. Coppi M. V., Leang C., Sandler S. J., Lovley D. R. ( 2001). Development of a genetic system for Geobacter sulfurreducens. Appl Environ Microbiol 67:3180–3187 [CrossRef][PubMed]
    [Google Scholar]
  11. Dahlberg C., Bergström M., Hermansson M. ( 1998). In situ detection of high levels of horizontal plasmid transfer in marine bacterial communities. Appl Environ Microbiol 64:2670–2675[PubMed]
    [Google Scholar]
  12. Dominguez W., O’Sullivan D. J. ( 2013). Developing an efficient and reproducible conjugation-based gene transfer system for bifidobacteria. Microbiology 159:328–338 [CrossRef][PubMed]
    [Google Scholar]
  13. El Gheriany I. A. ( 2010). Manganese oxidation by Leptothrix discophora SS1 PhD dissertation. Cornell University. Ithaca, NY, USA;
    [Google Scholar]
  14. Fernandez-Astorga A., Muela A., Cisterna R., Iriberri J., Barcina I. ( 1992). Biotic and abiotic factors affecting plasmid transfer in Escherichia coli strains. Appl Environ Microbiol 58:392–398[PubMed]
    [Google Scholar]
  15. Francis C. A., Tebo B. M. ( 2002). Enzymatic manganese(II) oxidation by metabolically dormant spores of diverse Bacillus species. Appl Environ Microbiol 68:874–880 [CrossRef][PubMed]
    [Google Scholar]
  16. Galvão T. C., de Lorenzo V. ( 2005). Adaptation of the yeast URA3 selection system to gram-negative bacteria and generation of a ΔbetCDE Pseudomonas putida strain. Appl Environ Microbiol 71:883–892 [CrossRef][PubMed]
    [Google Scholar]
  17. Ghiorse W. C. ( 1984). Biology of iron- and manganese-depositing bacteria. Annu Rev Microbiol 38:515–550 [CrossRef][PubMed]
    [Google Scholar]
  18. Hao L., Liu X., Wang H., Lin J., Pang X., Lin J. ( 2012). Detection and validation of a small broad-host-range plasmid pBBR1MCS-2 for use in genetic manipulation of the extremely acidophilic Acidithiobacillus sp.. J Microbiol Methods 90:309–314 [CrossRef][PubMed]
    [Google Scholar]
  19. Haugaard L. E., West T. P. ( 2002). Pyrimidine biosynthesis in Pseudomonas oleovorans. J Appl Microbiol 92:517–525 [CrossRef][PubMed]
    [Google Scholar]
  20. Isaac J. H., Holloway B. W. ( 1968).Pseudomonas aeruginosaJ Bacteriol96 [CrossRef][PubMed]
  21. Kalogeraki V. S., Winans S. C. ( 1997). Suicide plasmids containing promoterless reporter genes can simultaneously disrupt and create fusions to target genes of diverse bacteria. Gene 188:69–75 [CrossRef][PubMed]
    [Google Scholar]
  22. Kaniga K., Delor I., Cornelis G. R. ( 1991). A wide-host-range suicide vector for improving reverse genetics in gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica. Gene 109:137–141 [CrossRef][PubMed]
    [Google Scholar]
  23. Kolter R., Helsinki D. R. ( 1979). Regulation of initiation of DNA replication. Annu Rev Genet 13:355–391 [CrossRef][PubMed]
    [Google Scholar]
  24. Kovach M. E., Elzer P. H., Hill D. S., Robertson G. T., Farris M. A., Roop R. M. II, Peterson K. M. ( 1995). Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175–176 [CrossRef][PubMed]
    [Google Scholar]
  25. Lampkowska J., Feld L., Monaghan A., Toomey N., Schjørring S., Jacobsen B., van der Voet H., Andersen S. R., Bolton D., Aarts H. ( 2008). A standardized conjugation protocol to asses antibiotic resistance transfer between lactococcal species. Int J Food Microbiol 127:172–175 [CrossRef][PubMed]
    [Google Scholar]
  26. Nealson K. H., Tebo B. M., Rosson R. A. ( 1988). Occurrence and mechanisms of microbial oxidation of manganese. Adv Appl Microbiol 33:279–318 [CrossRef]
    [Google Scholar]
  27. Ridge J. P., Lin M., Larsen E. I., Fegan M., McEwan A. G., Sly L. I. ( 2007). A multicopper oxidase is essential for manganese oxidation and laccase-like activity in Pedomicrobium sp. ACM 3067. Environ Microbiol 9:944–953 [CrossRef][PubMed]
    [Google Scholar]
  28. Schneider J. C., Jenings A. F., Mun D. M., McGovern P. M., Chew L. C. ( 2005). Auxotrophic markers pyrF and proC can replace antibiotic markers on protein production plasmids in high-cell-density Pseudomonas fluorescens fermentation. Biotechnol Prog 21:343–348 [CrossRef][PubMed]
    [Google Scholar]
  29. Schultheiss D., Schüler D. ( 2003). Development of a genetic system for Magnetospirillum gryphiswaldense. Arch Microbiol 179:89–94[PubMed]
    [Google Scholar]
  30. Siering P. L. ( 1996). Application of molecular approaches to investigate the role of microorganisms in manganese cycling in wetland environments PhD dissertation. Cornell University. Ithaca, NY, USA;
    [Google Scholar]
  31. Su J., Bao P., Bai T., Deng L., Wu H., Liu F., He J. ( 2013). CotA, a multicopper oxidase from Bacillus pumilus WH4, exhibits manganese-oxidase activity. PLoS ONE 8:e60573 [CrossRef][PubMed]
    [Google Scholar]
  32. Szostková M., Horáková D. ( 1998). The effect of plasmid DNA sizes and other factors on electrotransformation of Escherichia coli JM109. Bioelectrochem Bioenerg 47:319–323 [CrossRef]
    [Google Scholar]
  33. Takeno S., Sakuradani E., Murata S., Inohara-Ochiai M., Kawashima H., Ashikari T., Shimizu S. ( 2004). Cloning and sequencing of the ura3 and ura5 genes, and isolation and characterization of uracil auxotrophs of the fungus Mortierella alpina 1S-4. Biosci Biotechnol Biochem 68:277–285 [CrossRef][PubMed]
    [Google Scholar]
  34. Tebo B. M., Ghiorse W. C., van Waasbergen L. G., Siering P. L., Caspi R. ( 1997). Bacterially mediated mineral formation; insights into manganese(II) oxidation from molecular genetic and biochemical studies. Rev Mineral Geochem 35:225–266
    [Google Scholar]
  35. Thia-Toong T.-L., Roovers M., Durbecq V., Gigot D., Glansdorff N., Charlier D. ( 2002). Genes of de novo pyrimidine biosynthesis from the hyperthermoacidophilic crenarchaeote Sulfolobus acidocaldarius: novel organization in a bipolar operon. J Bacteriol 184:4430–4441 [CrossRef][PubMed]
    [Google Scholar]
  36. Willetts N., Wilkins B. ( 1984). Processing of plasmid DNA during bacterial conjugation. Microbiol Rev 48:24–41[PubMed]
    [Google Scholar]
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