1887

Abstract

The -demethylation of phenyl methyl ethers under anaerobic conditions is a metabolic feature of acetogens and spp. Desulfitobacteria as well as most acetogens are Gram-positive bacteria with a low GC content and belong to the phylum . The consumption of the phenyl methyl ether syringate was studied in enrichment cultures originating from five different topsoils. spp. were detected in all topsoils via quantitative PCR. Desulfitobacteria could be enriched using the -demethylation of syringate as a growth-selective process. The enrichment was significantly favoured by an external electron acceptor such as 3-chloro-4-hydroxyphenylacetate or thiosulfate. Upon cultivation in the presence of syringate and thiosulfate, which naturally occur in soil, a maximum number of 16S rRNA gene copies of spp. was reached within the first three subcultivation steps and accounted for 3–10 % of the total microbial community depending on the soil type. Afterwards, a loss of gene copies was observed. Community analyses revealed that , , and were the main phyla in the initial soil samples. Upon addition of syringate and thiosulfate as growth substrates, these phyla were rapidly outcompeted by , which were under-represented in soil. The main genera identified were , , , and , which might be responsible for outcompeting the desulfitobacteria. Most of these organisms belong to the acetogens, which have previously been described to demethylate phenyl methyl ethers. The shift of the native community structure to almost exclusively supports the participation of members of this phylum in environmental demethylation processes.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000218
2016-02-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/162/2/224.html?itemId=/content/journal/micro/10.1099/mic.0.000218&mimeType=html&fmt=ahah

References

  1. Allen T. D., Caldwell M. E., Lawson P. A., Huhnke R. L., Tanner R. S. 2010; Alkalibaculum bacchi gen. nov., sp. nov., a CO-oxidizing, ethanol-producing acetogen isolated from livestock-impacted soil. Int J Syst Evol Microbiol 60:2483–2489 [View Article][PubMed]
    [Google Scholar]
  2. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410 [View Article][PubMed]
    [Google Scholar]
  3. Bache R., Pfennig N. 1981; Selective isolation of Acetobacterium woodii on methoxylated aromatic acids and determination of growth yields. Arch Microbiol 130:255–261 [View Article]
    [Google Scholar]
  4. Bouchard B., Beaudet R., Villemur R., McSween G., Lépine F., Bisaillon J.-G. 1996; Isolation and characterization of Desulfitobacterium frappieri sp. nov., an anaerobic bacterium which reductively dechlorinates pentachlorophenol to 3-chlorophenol. Int J Syst Bacteriol 46:1010–1015 [View Article][PubMed]
    [Google Scholar]
  5. Bradford M. M. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254 [View Article][PubMed]
    [Google Scholar]
  6. Breitenstein A., Saano A., Salkinoja-Salonen M., Andreesen J. R., Lechner U. 2001; Analysis of a 2,4,6-trichlorophenol-dehalogenating enrichment culture and isolation of the dehalogenating member Desulfitobacterium frappieri strain TCP-A. Arch Microbiol 175:133–142 [View Article][PubMed]
    [Google Scholar]
  7. Chen C.-L., Chang H.-M., Kirk T. K. 1982; Aromatic acids produced during degradation of lignin in spruce wood by Phanerochaete chrysosporium . Holzforschung 36:3–9 [View Article]
    [Google Scholar]
  8. Chen C.-L., Chang H.-M., Kirk T. K. 1983; Carboxylic acids produced through oxidative cleavage of aromatic rings during degradation of lignin in spruce wood by Phanerochaete chrysosporium . J Wood Chem Technol 3:35–57 [View Article]
    [Google Scholar]
  9. Colombo C., Palumbo G., He J. Y., Pinton R., Cesco S. 2014; Review on iron availability in soil: interaction of Fe minerals, plants, and microbes. J Soils Sediments 14:538–548 [View Article]
    [Google Scholar]
  10. Cypionka H., Pfennig N. 1986; Growth yields of Desulfotomaculum orientis with hydrogen in chemostat culture. Arch Microbiol 143:396–399 [View Article]
    [Google Scholar]
  11. Daniel S. L., Keith E. S., Yang H., Lin Y. S., Drake H. L. 1991; Utilization of methoxylated aromatic compounds by the acetogen Clostridium thermoaceticum: expression and specificity of the co-dependent O-demethylating activity. Biochem Biophys Res Commun 180:416–422 [View Article][PubMed]
    [Google Scholar]
  12. Drake H. L., Küsel K., Matthies C. 2006; Acetogenic prokaryotes. Prokaryotes 2:354–420 [View Article]
    [Google Scholar]
  13. Drzyzga O., Gerritse J., Dijk J. A., Elissen H., Gottschal J. C. 2001; Coexistence of a sulphate-reducing Desulfovibrio species and the dehalorespiring Desulfitobacterium frappieri TCE1 in defined chemostat cultures grown with various combinations of sulfate and tetrachloroethene. Environ Microbiol 3:92–99 [View Article][PubMed]
    [Google Scholar]
  14. Edgar R. C., Haas B. J., Clemente J. C., Quince C., Knight R. 2011; uchime improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200 [View Article][PubMed]
    [Google Scholar]
  15. Garcia S. L., Jangid K., Whitman W. B., Das K. C. 2011; Transition of microbial communities during the adaption to anaerobic digestion of carrot waste. Bioresour Technol 102:7249–7256 [View Article][PubMed]
    [Google Scholar]
  16. Gebauer G., Rehder H., Wollenweber B. 1988; Nitrate, nitrate reduction and organic nitrogen in plants from different ecological taxonomic groups. Oecologica 75:371–385 [View Article]
    [Google Scholar]
  17. Grbić-Galić D. 1986; O-Demethylation, dehydroxylation, ring-reduction and cleavage of aromatic substrates by Enterobacteriaceae under anaerobic conditions. J Appl Bacteriol 61:491–497 [View Article][PubMed]
    [Google Scholar]
  18. Hanselmann K. W., Kaiser J. P., Wenk M., Schön R., Bachofen R. 1995; Growth on methanol and conversion of methoxylated aromatic substrates by Desulfotomaculum orientis in the presence and absence of sulfate. Microbiol Res 150:387–401 [View Article]
    [Google Scholar]
  19. Hartmann M., Niklaus P. A., Zimmermann S., Schmutz S., Kremer J., Abarenkov K., Lüscher P., Widmer F., Frey B. 2014; Resistance and resilience of the forest soil microbiome to logging-associated compaction. ISME J 8:226–244 [View Article][PubMed]
    [Google Scholar]
  20. Higuchi T. 1990; Lignin biochemistry: biosynthesis and biodegradation. Wood Sci Technol 24:23–63 [View Article]
    [Google Scholar]
  21. Janssen P. H. 2006; Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728 [View Article][PubMed]
    [Google Scholar]
  22. Karn S. K., Balda S. 2013; Bioremediation 2,4,6,-trichlorophenol (2,4,6-TCP) by Shigella sp. S2 isolated from industrial dumpsite. Bioremediat J 17:71–78 [View Article]
    [Google Scholar]
  23. Klindworth A., Pruesse E., Schweer T., Peplies J., Quast C., Horn M., Glöckner F. O. 2013; Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1 [View Article][PubMed]
    [Google Scholar]
  24. Kögel I. 1986; Estimation and decomposition pattern of the lignin component in forest humus layers. Soil Biol Biochem 18:589–594 [View Article]
    [Google Scholar]
  25. Kozich J. J., Westcott S. L., Baxter N. T., Highlander S. K., Schloss P. D. 2013; Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120 [View Article][PubMed]
    [Google Scholar]
  26. Kreher S., Schilhabel A., Diekert G. 2008; Enzymes involved in the anoxic utilization of phenyl methyl ethers by Desulfitobacterium hafniense DCB2 and Desulfitobacterium hafniense PCE-S. Arch Microbiol 190:489–495 [View Article][PubMed]
    [Google Scholar]
  27. Lanthier M., Villemur R., Lépine F., Bisaillon J., Beaudet R. 2001; Geographic distribution of Desulfitobacterium frappieri PCP-1 and Desulfitobacterium spp. in soils from the province of Quebec, Canada. FEMS Microbiol Ecol 36:185–191 [View Article][PubMed]
    [Google Scholar]
  28. Lanthier M., Juteau P., Lépine F., Beaudet R., Villemur R. 2005; Desulfitobacterium hafniense is present in a high proportion within the biofilms of a high-performance pentachlorophenol-degrading, methanogenic fixed-film reactor. Appl Environ Microbiol 71:1058–1065 [View Article][PubMed]
    [Google Scholar]
  29. Liesack W., Bak F., Kreft J.-U., Stackebrandt E. 1994; Holophaga foetida gen. nov., sp. nov., a new, homoacetogenic bacterium degrading methoxylated aromatic compounds. Arch Microbiol 162:85–90[PubMed]
    [Google Scholar]
  30. Mechichi T., Labat M., Garcia J. L., Thomas P., Patel B. K. 1999a; Sporobacterium olearium gen. nov., sp. nov., a new methanethiol-producing bacterium that degrades aromatic compounds, isolated from an olive mill wastewater treatment digester. Int J Syst Bacteriol 49:1741–1748 [View Article][PubMed]
    [Google Scholar]
  31. Mechichi T., Labat M., Patel B. K. C., Woo T. H. S., Thomas P., Garcia J. L. 1999b; Clostridium methoxybenzovorans sp. nov., a new aromatic O-demethylating homoacetogen from an olive mill wastewater treatment digester. Int J Syst Bacteriol 49:1201–1209 [View Article][PubMed]
    [Google Scholar]
  32. Mingo F. S., Studenik S., Diekert G. 2014; Conversion of phenyl methyl ethers by Desulfitobacterium spp. and screening for the genes involved. FEMS Microbiol Ecol 90:783–790 [View Article][PubMed]
    [Google Scholar]
  33. Muyzer G., de Waal E. C., Uitterlinden A. G. 1993; Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700[PubMed]
    [Google Scholar]
  34. Neumann A., Engelmann T., Schmitz R., Greiser Y., Orthaus A., Diekert G. 2004; Phenyl methyl ethers: novel electron donors for respiratory growth of Desulfitobacterium hafniense and Desulfitobacterium sp. strain PCE-S. Arch Microbiol 181:245–249 [View Article][PubMed]
    [Google Scholar]
  35. Niggemyer A., Spring S., Stackebrandt E., Rosenzweig R. F. 2001; Isolation and characterization of a novel As(V)-reducing bacterium: implications for arsenic mobilization and the genus Desulfitobacterium . Appl Environ Microbiol 67:5568–5580 [View Article][PubMed]
    [Google Scholar]
  36. Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., Peplies J., Glöckner F. O., ribosomal R. N. A. 2013; The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:(D1)D590–D596[PubMed] [CrossRef]
    [Google Scholar]
  37. Quentin K.-E., Pachmayr F. 1964; [Determination of thiosulfate in the sulfur-containing mineral waters]. Fresenius Z Anal Chem 200:250–256 (in German) [View Article]
    [Google Scholar]
  38. Rouzeau-Szynalski K., Maillard J., Holliger C. 2011; Frequent concomitant presence of Desulfitobacterium spp. and Dehalococcoides spp. in chloroethene-dechlorinating microbial communities. Appl Microbiol Biotechnol 90:361–368 [View Article][PubMed]
    [Google Scholar]
  39. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  40. Sánchez-Andrea I., Rodríguez N., Amils R., Sanz J. L. 2011; Microbial diversity in anaerobic sediments at Rio Tinto, a naturally acidic environment with a high heavy metal content. Appl Environ Microbiol 77:6085–6093 [View Article][PubMed]
    [Google Scholar]
  41. Sánchez-Andrea I., Rojas-Ojeda P., Amils R., Sanz J. L. 2012; Screening of anaerobic activities in sediments of an acidic environment: Tinto River. Extremophiles 16:829–839 [View Article][PubMed]
    [Google Scholar]
  42. Schloss P. D., Westcott S. L., Ryabin T., Hall J. R., Hartmann M., Hollister E. B., Lesniewski R. A., Oakley B. B., Parks D. H., other authors. 2009; Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541 [View Article][PubMed]
    [Google Scholar]
  43. Schloss P. D., Gevers D., Westcott S. L. 2011; Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310 [View Article][PubMed]
    [Google Scholar]
  44. Sharma P. K., McCarty P. L. 1996; Isolation and characterization of a facultatively aerobic bacterium that reductively dehalogenates tetrachloroethene to cis-1,2-dichloroethene. Appl Environ Microbiol 62:761–765[PubMed]
    [Google Scholar]
  45. Smith C. J., Osborn A. M. 2009; Advantages and limitations of quantitative PCR (Q-PCR)-based approaches in microbial ecology. FEMS Microbiol Ecol 67:6–20 [View Article][PubMed]
    [Google Scholar]
  46. Starkey R. L. 1950; Relations of microorganisms to transformations of sulfur in soils. Soil Sci 70:55–65 [View Article]
    [Google Scholar]
  47. Stupperich E., Konle R. 1993; Corrinoid-dependent methyl transfer reactions are involved in methanol and 3,4-dimethoxybenzoate metabolism by Sporomusa ovata . Appl Environ Microbiol 59:3110–3116[PubMed]
    [Google Scholar]
  48. Traunecker J., Preuss A., Diekert G. 1991; Isolation and characterization of a methyl chloride utilizing, strictly anaerobic bacterium. Arch Microbiol 156:416–421 [View Article]
    [Google Scholar]
  49. Utkin I., Woese C., Wiegel J. 1994; Isolation and characterization of Desulfitobacterium dehalogenans gen. nov., sp. nov., an anaerobic bacterium which reductively dechlorinates chlorophenolic compounds. Int J Syst Bacteriol 44:612–619 [View Article][PubMed]
    [Google Scholar]
  50. Villemur R., Lanthier M., Beaudet R., Lépine F. 2006; The Desulfitobacterium genus. FEMS Microbiol Rev 30:706–733 [View Article][PubMed]
    [Google Scholar]
  51. Wang Q., Garrity G. M., Tiedje J. M., Cole J. R. 2007; Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267 [View Article][PubMed]
    [Google Scholar]
  52. Weisburg W. G., Barns S. M., Pelletier D. A., Lane D. J. 1991; 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703[PubMed]
    [Google Scholar]
  53. Whitehead D. C. 1964; Identification of p-hydroxybenzoic, vanillic, p-coumaric and ferulic acids in soils. Nature 202:417–418 [View Article][PubMed]
    [Google Scholar]
  54. Wind T., Conrad R. 1995; Sulfur compounds, potential turnover of sulfate and thiosulfate, and numbers of sulfate-reducing bacteria in planted and unplanted paddy soil. FEMS Microbiol Ecol 18:257–266 [View Article]
    [Google Scholar]
  55. Yoshida N., Asahi K., Sakakibara Y., Miyake K., Katayama A. 2007; Isolation and quantitative detection of tetrachloroethene (PCE)-dechlorinating bacteria in unsaturated subsurface soils contaminated with chloroethenes. J Biosci Bioeng 104:91–97 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000218
Loading
/content/journal/micro/10.1099/mic.0.000218
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error