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Characterization of precipitates formed by H2S-producing, Cu-resistant Firmicute isolates of Tissierella from human gut and Desulfosporosinus from mine waste

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Abstract

The purpose of this study was to characterize precipitates formed in anaerobic, H2S-producing cultures of two Tissierella isolates and Desulfosporosinus strain DB. The cultures were grown in Cu-containing media as part of a larger study of Cu resistance in anaerobic sulfidogens. The Tissierella strains produced H2S from peptone. Desulfosporosinus formed H2S from peptone or through dissimilatory sulfate reduction with lactate. Tissierella cultures precipitated iron phosphate, vivianite, but no crystalline phases or Cu sulfides were detected. Multiple Cu sulfides, including chalcopyrite and covellite, were detected in Desulfosporosinus cultures but vivianite was not formed. Ion microprobe spectra and electron microscopic examination showed major variation in the elemental composition and morphological differences depending on incubation conditions. Extended incubation time for at least 1–2 months increased the crystallinity of the precipitates. The results highlight biogeochemical differences in sulfide and phosphate precipitates between the two major groups of Firmicutes although they may share the same habitat including the human intestinal tract.

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References

  • Beerens H, Romond C (1977) Sulfate-reducing anaerobic bacteria in human feces. Am J Clin Nutr 30:1770–1776

    PubMed  CAS  Google Scholar 

  • Collins MD, Shah HN (1986) Reclassification of Bacteroides praeacutus Tissier (Holdeman and Moore) in a new genus, Tissierella, as Tissierella praeacuta comb. nov. Int J Syst Bacteriol 36:461–463

    Article  CAS  Google Scholar 

  • Cowper M, Rickard D (1989) Mechanism of chalcopyrite formation from iron monosulphides in aqueous solutions (<100 °C, pH 2–4.5). Chem Geol 78:325–341

    Article  CAS  Google Scholar 

  • DeLong EF (1992) Archaea in costal marine environments. Proc Natl Acad Sci USA 89:5685–5689

    Article  PubMed  CAS  Google Scholar 

  • Dosman CF, Drmic IE, Brian JA, Senthilselvan A, Harfond M, Smith R, Roberts SW (2006) Ferritin as an indicator of suspected iron deficiency in children with autism disorder: prevalence of low serum ferritin concentration. Dev Med Child Neurol 48:1006–1011

    Article  Google Scholar 

  • Farrow JAE, Lawson PA, Hippe H, Gauglitz U, Collins MD (1995) Phylogenetic evidence that the gram-negative nonsporulating bacterium Tissierella (Bacteroides) praeacuta is a member of the Clostridium subphylum of the gram-positive bacteria and description of Tissierella creatinini sp. nov. Int J Syst Bacteriol 45:436–440

    Article  PubMed  CAS  Google Scholar 

  • Finegold SM, Downes J, Summanen PH (2012) Microbiology of regressive autism. Anaerobe 18:260–262

    Article  PubMed  CAS  Google Scholar 

  • Fredrickson JK, Zachara JM, Kennedy DW, Dong H, Onstott TC, Hinman NW, Li S (1998) Biogenic iron mineralization accompanying the dissimilatory reduction of hydrous ferric oxide by a groundwater bacterium. Geochim Cosmochim Acta 62:3239–3257

    Article  CAS  Google Scholar 

  • Gibson GR, Macfarlane GT (1988) Chemostat enrichment of sulphate-reducing bacteria from the large gut. Lett Appl Microbiol 7:127–133

    Article  CAS  Google Scholar 

  • Glasauer S, Weidler PG, Langley S, Beveridge TJ (2003) Controls on Fe reduction and mineral formation by a subsurface bacterium. Geochim Cosmochim Acta 67:1277–1288

    Article  CAS  Google Scholar 

  • Gramp GP, Sasaki K, Bigham JM, Karnachuk OV, Tuovinen OH (2006) Formation of covellite (CuS) under biological sulfate-reducing conditions. Geomicrobiol J 23:613–619

    Article  CAS  Google Scholar 

  • Gramp J, Bigham JM, Sasaki K, Tuovinen OH (2007) Formation of Ni- and Zn-sulfides in cultures of sulfate-reducing bacteria. Geomicrobiol J 24:609–614

    Article  CAS  Google Scholar 

  • Harms C, Schleicher A, Collins MD, Andereesen JR (1998) Tissierella creatinophila sp. nov., a Gram-positive, anaerobic, non-spore-forming, creatinine-fermenting organism. Int J Syst Evol Microbiol 48:983–993

    CAS  Google Scholar 

  • Helz GR, Horzempa LM (1983) EDTA as a kinetic inhibitor of copper (II) sulfide precipitation. Water Res 17:167–172

    Article  CAS  Google Scholar 

  • Jorand F, Appenzeller BMR, Abdelmoula M, Refait P, Block J-C, Genin J-MR (2000) Assessment of vivianite formation in Shewanella putrefaciens culture. Environ Technol 21:1001–1005

    CAS  Google Scholar 

  • Kabil O, Banerjee R (2010) Redox biochemistry of hydrogen sulfide. J Biol Chem 285:21903–21907

    Article  PubMed  CAS  Google Scholar 

  • Karnachuk OV, Sasaki K, Gerasimchuk AL, Sukhanova O, Ivasenko DA, Kaksonen AH, Puhakka JA, Tuovinen OH (2008) Precipitation of Cu-sulfides by copper-tolerant Desulfovibrio isolates. Geomicrobiol J 25:219–227

    Article  CAS  Google Scholar 

  • Karnachuk OV, Gerasimchuk AL, Banks D, Frengstad B, Stykon GA, Tikhonova ZL, Kaksonen A, Puhakka J, Yanenko AS, Pimenov NV (2009) Bacteria of the sulfur cycle in the sediments of gold mine tailings, Kuznetsk Basin, Russia. Microbiology 78:483–491

    Article  CAS  Google Scholar 

  • Labrenz M, Banfield JF (2004) Sulfate-reducing bacteria-dominated biofilms that precipitate ZnS in a subsurface circumneutral-pH mine drainage system. Microb Ecol 47:205–217

    PubMed  CAS  Google Scholar 

  • Labrenz M, Druschel GK, Thomsen-Ebert T, Gilbert B, Welch SA, Kemmer KM, Logan GA, Summons RE, De Stasio G, Bond PL, Lai B, Kelly SD, Banfield JF (2000) Formation of sphalerite (ZnS) deposits in natural biofilms of sulfate-reducing bacteria. Science 290:1744–1747

    Article  PubMed  CAS  Google Scholar 

  • Latif A, Heinz P, Cook R (2002) Iron deficiency in autism and Asperger syndrome. Autism 6:103–114

    Article  PubMed  CAS  Google Scholar 

  • Ludwig W, Schleifer K-H, Whitman WB (2009) Revised road map to the phylum Firmicutes. In: Vos P, Garrity G, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer K-H, Whitman WB (eds) The Firmicutes. Bergey’s manual of systematic bacteriology, 2nd edn. Springer, New York, pp 1–13

    Google Scholar 

  • Macfarlane GT, Cummings JH, Macfarlane S (2007) Sulphate-reducing bacteria and the human large intestine. In: Barton LL, Hamilton WA (eds) Sulphate-reducing bacteria. Environmental and engineered systems. Cambridge University Press, Cambridge, pp 503–523

    Chapter  Google Scholar 

  • Matocha CJ, Karathanasis AD, Rakshit S, Wagner KM (2005) Reduction of copper(II) by iron(II). J Environ Qual 34:1539–1546

    Article  PubMed  CAS  Google Scholar 

  • Moore WEC, Johnson JL, Holdeman LV (1976) Emendation of Bacteroidaceae and Butyrivibrio and descriptions of Desulfomonas gen. nov. and ten new species of the genera Desulfomonas, Butyrivibrio, Eubacterium, and Ruminococcus. Int J Syst Bacteriol 26:238–252

    Article  Google Scholar 

  • Nriagu JO (1972) Stability of vivianite and ion-pair formation in the system Fe3(PO4)2–H3PO4–H2O. Geochim Cosmochim Acta 36:459–470

    Article  CAS  Google Scholar 

  • Pankhania IP, Moosavi AN, Hamilton WA (1986) Utilization of cathodic hydrogen by Desulfovibrio vulgaris (Hildenborough). J Gen Microbiol 132:3357–3365

    CAS  Google Scholar 

  • Pekala M, Asael D, Butler IB, Matthews A, Rickard D (2011) Experimental study of Cu isotope fractionation during the reaction of aqueous Cu(II) with Fe(II) sulphides at temperatures between 40 and 200 °C. Chem Geol 289:31–38

    Article  CAS  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    Article  PubMed  CAS  Google Scholar 

  • Rickard D, Cowper M (1994) Kinetics and mechanism of chalcopyrite formation from Fe(II) disulphide in aqueous solution (<200 °C). Geochim Cosmochim Acta 58:3795–3802

    Article  CAS  Google Scholar 

  • Rickard D, Luther GW III (2007) Chemistry of iron sulfides. Chem Rev 107:514–562

    Article  PubMed  CAS  Google Scholar 

  • Roberts WMB (1963) The low temperature synthesis in aqueous solution of chalcopyrite and bornite. Econ Geol 58:52–61

    Article  CAS  Google Scholar 

  • Shatalin K, Shatalina E, Mironov A, Nudler E (2011) H2S: universal defense against antibiotics in bacteria. Science 334:986–990

    Article  PubMed  CAS  Google Scholar 

  • Shea D, Helz GR (1987) Kinetics of inhibited crystal growth: precipitation of CuS from solutions containing chelated copper(II). J Colloid Interface Sci 116:373–383

    Article  CAS  Google Scholar 

  • Thiennimitr P, Winter SE, Winter MG, Xavier MN, Tolstikov V, Huseby DL, Sterzenbach T, Tsolis RM, Roth JR, Baumler AJ (2011) Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc Natl Acad Sci USA 108:17480–17485

    Article  PubMed  CAS  Google Scholar 

  • Undeen AH, Vávra J (1997) Research methods for entomopathogenic protozoa. In: Lacey LA (ed) Manual of techniques in insect pathology. Academic Press, San Diego, pp 117–151

    Chapter  Google Scholar 

  • Walker CA, Rimstidt JD (1986) Rates of reaction of covellite and blaubleibender covellite with ferric iron at pH 2.0. Can Mineral 24:35–44

    Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S Ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    PubMed  CAS  Google Scholar 

  • Widdel FF, Bak R (1992) Gram-negative mesophilic sulfate-reducing bacteria. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-H (eds) The prokaryotes: a handbook on the biology of bacteria: ecophysiology, isolation, identification, applications, 2nd edn. Springer, Berlin, pp 3352–3378

    Google Scholar 

  • Winter SE, Thiennimitr P, Winter MG, Butler BP, Huseby DL, Crawford RW, Russel JM, Bevins CL, Adams LG, Tsolis RM, Roth JR, Baumler AJ (2010) Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467:426–429

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Anna Kozlova, Yuri Lopushniak and Andrei Miller for skillful technical assistance in SEM/EDS, XRD, and TEM analyses. This study was supported by the Russian Ministry of Education and Science (Contract number 11.519.11.2011), the Russian Fund for Basic Research (RFBR 11-04-98076-r_sibir_a) to OVK, and the Russian President Grant MK-3489.2011.4 to AG.

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Correspondence to Olga V. Karnachuk.

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Ikkert, O.P., Gerasimchuk, A.L., Bukhtiyarova, P.A. et al. Characterization of precipitates formed by H2S-producing, Cu-resistant Firmicute isolates of Tissierella from human gut and Desulfosporosinus from mine waste. Antonie van Leeuwenhoek 103, 1221–1234 (2013). https://doi.org/10.1007/s10482-013-9900-x

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  • DOI: https://doi.org/10.1007/s10482-013-9900-x

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