1887

Abstract

An extremely thermophilic, xylanolytic, spore-forming and strictly anaerobic bacterium, strain DTU01, was isolated from a continuously stirred tank reactor fed with xylose and household waste. Cells stained Gram-negative and were rod-shaped (0.5–2 µm in length). Spores were terminal with a diameter of approximately 0.5 µm. Optimal growth occurred at 70 °C and pH 7, with a maximum growth rate of 0.1 h. DNA G+C content was 34.2 mol%. Strain DTU01 could ferment arabinose, cellobiose, fructose, galactose, glucose, lactose, mannitol, mannose, melibiose, pectin, starch, sucrose, xylan, yeast extract and xylose, but not cellulose, Avicel, inositol, inulin, glycerol, rhamnose, acetate, lactate, ethanol, butanol or peptone. Ethanol was the major fermentation product and a maximum yield of 1.39 mol ethanol per mol xylose was achieved when sulfite was added to the cultivation medium. Thiosulfate, but not sulfate, nitrate or nitrite, could be used as electron acceptor. On the basis of 16S rRNA gene sequence similarity, strain DTU01 was shown to be closely related to A3, Ab9 and JT3-3, with 98–99 % similarity. Despite this, the physiological and phylogenetic differences (DNA G+C content, substrate utilization, electron acceptors, phylogenetic distance and isolation site) allow for the proposal of strain DTU01 as a representative of a novel species within the genus , for which the name sp. nov. is proposed, with the type strain DTU01 ( = DSM 25963 = KCTC 4529 = VKM B-2752 = CECT 8142).

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.045211-0
2013-07-01
2019-10-21
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/63/7/2396.html?itemId=/content/journal/ijsem/10.1099/ijs.0.045211-0&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J.. ( 1997;). Gapped blast and psi-blast: a new generation of protein database search programs. . Nucleic Acids Res 25:, 3389–3402. [CrossRef][PubMed]
    [Google Scholar]
  2. Angelidaki I., Petersen S. P., Ahring B. K.. ( 1990;). Effects of lipids on thermophilic anaerobic digestion and reduction of lipid inhibition upon addition of bentonite. . Appl Microbiol Biotechnol 33:, 469–472. [CrossRef][PubMed]
    [Google Scholar]
  3. Balk M., Heilig H. G. H. J., van Eekert M. H. A., Stams A. J. M., Rijpstra I. C., Sinninghe-Damsté J. S., de Vos W. M., Kengen S. W. M.. ( 2009;). Isolation and characterization of a new CO-utilizing strain, Thermoanaerobacter thermohydrosulfuricus subsp. carboxydovorans, isolated from a geothermal spring in Turkey. . Extremophiles 13:, 885–894. [CrossRef][PubMed]
    [Google Scholar]
  4. Bligh E. G., Dyer W. J.. ( 1959;). A rapid method of total lipid extraction and purification. . Can J Biochem Physiol 37:, 911–917. [CrossRef][PubMed]
    [Google Scholar]
  5. Buera M. D. P., Chirife J., Resnik S. L., Lozano R. D.. ( 1987;). Nonenzymatic browning in liquid model systems of high water activity: kinetics of color changes due to caramelization of various single sugars. . J Food Sci 52:, 1059–1062. [CrossRef]
    [Google Scholar]
  6. Carlier J.-P., Bonne I., Bedora-Faure M.. ( 2006;). Isolation from canned foods of a novel Thermoanaerobacter species phylogenetically related to Thermoanaerobacter mathranii (Larsen 1997): emendation of the species description and proposal of Thermoanaerobacter mathranii subsp. alimentarius subsp. nov.. Anaerobe 12:, 153–159. [CrossRef][PubMed]
    [Google Scholar]
  7. Chun J., Lee J.-H., Jung Y., Kim M., Kim S., Kim B. K., Lim Y.-W.. ( 2007;). EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. . Int J Syst Evol Microbiol 57:, 2259–2261. [CrossRef][PubMed]
    [Google Scholar]
  8. Collins M. D., Jones D.. ( 1981;). Distribution of isoprenoid quinone structural types in bacteria and their taxonomic implication. . Microbiol Rev 45:, 316–354.[PubMed]
    [Google Scholar]
  9. Collins M. D., Lawson P. A., Willems A., Cordoba J. J., Fernandez-Garayzabal J., Garcia P., Cai J., Hippe H., Farrow J. A. E.. ( 1994;). The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. . Int J Syst Bacteriol 44:, 812–826. [CrossRef][PubMed]
    [Google Scholar]
  10. Crespo C. F., Pozzo T., Karlsson E. N., Alvarez M. T., Mattiasson B.. ( 2012;). Caloramator boliviensis sp. nov., a thermophilic, ethanol-producing bacterium isolated from a hot spring. . Int J Syst Evol Microbiol 62:, 1679–1686. [CrossRef][PubMed]
    [Google Scholar]
  11. da Costa M. S., Albuquerque L., Nobre M. F., Wait R.. ( 2011;). The identification of polar lipids in prokaryotes. . Methods Microbiol, 38:, pp. 165–181. [CrossRef]
    [Google Scholar]
  12. Fardeau M.-L., Bonilla Salinas M., L’Haridon S., Jeanthon C., Verhé F., Cayol J.-L., Patel B. K. C., Garcia J.-L., Ollivier B.. ( 2004;). Isolation from oil reservoirs of novel thermophilic anaerobes phylogenetically related to Thermoanaerobacter subterraneus: reassignment of T. subterraneus, Thermoanaerobacter yonseiensis, Thermoanaerobacter tengcongensis and Carboxydibrachium pacificum to Caldanaerobacter subterraneus gen. nov., sp. nov., comb. nov. as four novel subspecies. . Int J Syst Evol Microbiol 54:, 467–474. [CrossRef][PubMed]
    [Google Scholar]
  13. Felsenstein J.. ( 1985;). Confidence limits on phylogenies: An approach using the bootstrap. . Evolution 39:, 783–791. [CrossRef]
    [Google Scholar]
  14. Goris J., Konstantinidis K. T., Klappenbach J. A., Coenye T., Vandamme P., Tiedje J. M.. ( 2007;). DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. . Int J Syst Evol Microbiol 57:, 81–91. [CrossRef][PubMed]
    [Google Scholar]
  15. Hill E. G., Patton A. R.. ( 1947;). The Maillard reaction in microbiological assay. . Science 105:, 481–482. [CrossRef][PubMed]
    [Google Scholar]
  16. Hungate R. E.. ( 1969;). A roll tube method for cultivation of strict anaerobes. . Methods Microbiol 1:, 117–132. [CrossRef]
    [Google Scholar]
  17. Jin F., Yamasato K., Toda K.. ( 1988;). Clostridium thermocopriae sp. nov., a cellulolytic thermophile from animal feces, compost, soil, and a hot spring in Japan. . Int J Syst Bacteriol 38:, 279–281. [CrossRef]
    [Google Scholar]
  18. Jukes H. T., Cantor C. R.. ( 1969;). Evolution of protein molecules. . In Mammalian Protein Metabolism, vol. 3, pp. 21–132. Edited by Munro H. N... New York:: Academic Press;.
    [Google Scholar]
  19. Jung S., Zeikus J. G., Hollingsworth R. I.. ( 1994;). A new family of very long chain α,ω-dicarboxylic acids is a major structural fatty acyl component of the membrane lipids of Thermoanaerobacter ethanolicus 39E. . J Lipid Res 35:, 1057–1065.[PubMed]
    [Google Scholar]
  20. Kim B. C., Grote R., Lee D. W., Antranikian G., Pyun Y. R.. ( 2001;). Thermoanaerobacter yonseiensis sp. nov., a novel extremely thermophilic, xylose-utilizing bacterium that grows at up to 85 degrees C. . Int J Syst Evol Microbiol 51:, 1539–1548.[PubMed]
    [Google Scholar]
  21. Kongjan P., Min B., Angelidaki I.. ( 2009;). Biohydrogen production from xylose at extreme thermophilic temperatures (70 °C) by mixed culture fermentation. . Water Res 43:, 1414–1424. [CrossRef][PubMed]
    [Google Scholar]
  22. Konstantinidis K. T., Tiedje J. M.. ( 2005;). Genomic insights that advance the species definition for prokaryotes. . Proc Natl Acad Sci U S A 102:, 2567–2572. [CrossRef][PubMed]
    [Google Scholar]
  23. Kozianowski G., Canganella F., Rainey F. A., Hippe H., Antranikian G.. ( 1997;). Purification and characterization of thermostable pectate-lyases from a newly isolated thermophilic bacterium, Thermoanaerobacter italicus sp. nov.. Extremophiles 1:, 171–182. [CrossRef][PubMed]
    [Google Scholar]
  24. Kuykendall L. D., Roy M. A., O’Neill J. J., Devine T. E.. ( 1988;). Fatty acids, antibiotic resistance, and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum. . Int J Syst Bacteriol 38:, 358–361. [CrossRef]
    [Google Scholar]
  25. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A.. & other authors ( 2007;). clustal w and clustal_x version 2.0. . Bioinformatics 23:, 2947–2948. [CrossRef][PubMed]
    [Google Scholar]
  26. Larsen L., Nielsen P., Ahring B. K.. ( 1997;). Thermoanaerobacter mathranii sp. nov., an ethanol-producing, extremely thermophilic anaerobic bacterium from a hot spring in Iceland. . Arch Microbiol 168:, 114–119. [CrossRef][PubMed]
    [Google Scholar]
  27. Lechevalier H., Lechevalier M. P.. ( 1988;). Chemotaxonomic use of lipids - an overview. . In Microbial lipids, vol. 1, pp. 869–902. Edited by Ratledge C., Wilkinson S. G... London:: Academic Press;.
    [Google Scholar]
  28. Lee Y.-E., Jain M. K., Lee C., Zeikus J. G.. ( 1993;). Taxonomic distinction of saccharolytic thermophilic anaerobes: description of Thermoanaerobacterium xylanolyticum gen. nov., sp. nov., and Thermoanaerobacterium saccharolyticum gen. nov., sp. nov.; reclassification of Thermoanaerobium brockii, Clostridium thermosulfurogenes, and Clostridium thermohydrosulfuricum E100–69 as Thermoanaerobacter brockii comb. nov., Thermoanaerobacterium thermosulfurigenes comb. nov., and Thermoanaerobacter thermohydrosulfuricus comb. nov., respectively; and transfer of Clostridium thermohydrosulfuricum 39E to Thermoanaerobacter ethanolicus. . Int J Syst Bacteriol 43:, 41–51. [CrossRef]
    [Google Scholar]
  29. Lee S., Kang S., Kim J. N., Jung S.. ( 2002;). Structural analyses of the novel phosphoglycolipids containing the unusual very long bifunctional acyl chain, α,ω-13,16-dimethyloctacosanedioate in Thermoanaerobacter ethanolicus. . Bull Korean Chem Soc 23:, 1778–1784. [CrossRef]
    [Google Scholar]
  30. Lin C. C., Casida L. E.. ( 1984;). GELRITE as a gelling agent in media for the growth of thermophilic microorganisms. . Appl Environ Microbiol 47:, 427–429.[PubMed]
    [Google Scholar]
  31. Liu D., Zeng R. J., Angelidaki I.. ( 2008;). Effects of pH and hydraulic retention time on hydrogen production versus methanogenesis during anaerobic fermentation of organic household solid waste under extreme-thermophilic temperature (70 °C). . Biotechnol Bioeng 100:, 1108–1114. [CrossRef][PubMed]
    [Google Scholar]
  32. Macy J. M., Snellen J. E., Hungate R. E.. ( 1972;). Use of syringe methods for anaerobiosis. . Am J Clin Nutr 25:, 1318–1323.[PubMed]
    [Google Scholar]
  33. Miller L. T.. ( 1982;). Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxy acids. . J Clin Microbiol 16:, 584–586.[PubMed]
    [Google Scholar]
  34. Morotomi M., Nagai F., Watanabe Y.. ( 2012;). Description of Christensenella minuta gen. nov., sp. nov., isolated from human faeces that forms a distinct branch in the order Clostridiales, and proposal of Christensenellaceae fam. nov.. Int J Syst Evol Microbiol 62:, 144–149. [CrossRef][PubMed]
    [Google Scholar]
  35. Partanen P., Hultman J., Paulin L., Auvinen P., Romantschuk M.. ( 2010;). Bacterial diversity at different stages of the composting process. . BMC Microbiol 10:, 94–105. [CrossRef][PubMed]
    [Google Scholar]
  36. Pei A. Y., Oberdorf W. E., Nossa C. W., Agarwal A., Chokshi P., Gerz E. A., Jin Z., Lee P., Yang L.. & other authors ( 2010;). Diversity of 16S rRNA genes within individual prokaryotic genomes. . Appl Environ Microbiol 76:, 3886–3897. [CrossRef][PubMed]
    [Google Scholar]
  37. Pourcher A., Sutra L., Hébé I., Moguedet G., Bollet C., Simoneau P., Gardan L.. ( 2001;). Enumeration and characterization of cellulolytic bacteria from refuse of a landfill. . FEMS Microbiol Ecol 34:, 229–241. [CrossRef][PubMed]
    [Google Scholar]
  38. Rainey F. A., Ward N. L., Morgan H. W., Toalster R., Stackebrandt E.. ( 1993;). Phylogenetic analysis of anaerobic thermophilic bacteria: aid for their reclassification. . J Bacteriol 175:, 4772–4779.[PubMed]
    [Google Scholar]
  39. Richter M., Rosselló-Móra R.. ( 2009;). Shifting the genomic gold standard for the prokaryotic species definition. . Proc Natl Acad Sci U S A 106:, 19126–19131. [CrossRef][PubMed]
    [Google Scholar]
  40. Schaeffer A. B., Fulton M. D.. ( 1933;). A simplified method of staining endospores. . Science 77:, 194. [CrossRef][PubMed]
    [Google Scholar]
  41. Schumann P.. ( 2011;). Peptidoglycan structure. . Methods Microbiol, 38:, 101–129. [CrossRef]
    [Google Scholar]
  42. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S.. ( 2011;). mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. . Mol Biol Evol 28:, 2731–2739. [CrossRef][PubMed]
    [Google Scholar]
  43. Taylor M. P., Eley K. L., Martin S., Tuffin M. I., Burton S. G., Cowan D. A.. ( 2009;). Thermophilic ethanologenesis: future prospects for second-generation bioethanol production. . Trends Biotechnol 27:, 398–405. [CrossRef][PubMed]
    [Google Scholar]
  44. Tindall B.. ( 1990a;). Lipid composition of Halobacterium lacusprofundi. . FEMS Microbiol Lett 66:, 199–202. [CrossRef]
    [Google Scholar]
  45. Tindall B. J.. ( 1990b;). A comparative study of the lipid composition of Halobacterium saccharovorum from various sources. . Syst Appl Microbiol 13:, 128–130. [CrossRef]
    [Google Scholar]
  46. Tindall B. J., Sikorski J., Smibert R. A., Krieg N. R.. ( 2007;). Phenotypic characterization and the principles of comparative systematics. . In Methods for General and Molecular Microbiology, , 3rd edn., pp. 330–393. Edited by Reddy C. A., Beveridge T. J., Breznak J. A., Marzluf G., Schmidt T. M., Snyder L. R... Washington, DC:: American Society for Microbiology;.
    [Google Scholar]
  47. Tomás A. F., Karakashev D., Angelidaki I.. ( 2011;). Effect of xylose and nutrients concentration on ethanol production by a newly isolated extreme thermophilic bacterium. . Water Sci Technol 64:, 341–347. [CrossRef][PubMed]
    [Google Scholar]
  48. Verbeke T. J., Dumonceaux T. J., Wushke S., Cicek N., Levin D. B., Sparling R.. ( 2011a;). Isolates of Thermoanaerobacter thermohydrosulfuricus from decaying wood compost display genetic and phenotypic microdiversity. . FEMS Microbiol Ecol 78:, 473–487. [CrossRef][PubMed]
    [Google Scholar]
  49. Verbeke T. J., Sparling R., Hill J. E., Links M. G., Levin D., Dumonceaux T. J.. ( 2011b;). Predicting relatedness of bacterial genomes using the chaperonin-60 universal target (cpn60 UT): application to Thermoanaerobacter species. . Syst Appl Microbiol 34:, 171–179. [CrossRef][PubMed]
    [Google Scholar]
  50. Westlake K., Archer D. B., Boone D. R.. ( 1995;). Diversity of cellulolytic bacteria in landfill. . J Appl Microbiol 79:, 73–78. [CrossRef]
    [Google Scholar]
  51. Wiegel J. W., Ljungdahl L. G.. ( 1981;). Thermoanaerobacter ethanolicus gen. nov., spec. nov., a new, extreme thermophilic, anaerobic bacterium. . Arch Microbiol 1979:, 343–348. [CrossRef]
    [Google Scholar]
  52. Yabe S., Aiba Y., Sakai Y., Hazaka M., Yokota A.. ( 2011;). Thermasporomyces composti gen. nov., sp. nov., a thermophilic actinomycete isolated from compost. . Int J Syst Evol Microbiol 61:, 86–90. [CrossRef][PubMed]
    [Google Scholar]
  53. Yamamoto K., Murakami R., Takamura Y.. ( 1998;). Isoprenoid quinone, cellular fatty acid composition and diaminopimelic acid isomers of newly classified thermophilic anaerobic Gram-positive bacteria. . FEMS Microbiol Lett 161:, 351–358. [CrossRef]
    [Google Scholar]
  54. Yassin A. F., Spröer C., Hupfer H., Siering C., Klenk H.-P.. ( 2009;). Nocardiopsis potens sp. nov., isolated from household waste. . Int J Syst Evol Microbiol 59:, 2729–2733. [CrossRef][PubMed]
    [Google Scholar]
  55. Yokoyama H., Wagner I. D., Wiegel J.. ( 2010;). Caldicoprobacter oshimai gen. nov., sp. nov., an anaerobic, xylanolytic, extremely thermophilic bacterium isolated from sheep faeces, and proposal of Caldicoprobacteraceae fam. nov.. Int J Syst Evol Microbiol 60:, 67–71. [CrossRef][PubMed]
    [Google Scholar]
  56. Zeigler D. R.. ( 2003;). Gene sequences useful for predicting relatedness of whole genomes in bacteria. . Int J Syst Evol Microbiol 53:, 1893–1900. [CrossRef][PubMed]
    [Google Scholar]
  57. Zhang Z., Schwartz S., Wagner L., Miller W.. ( 2000;). A greedy algorithm for aligning DNA sequences. . J Comput Biol 7:, 203–214. [CrossRef][PubMed]
    [Google Scholar]
  58. Zhao C., O-Thong S., Karakashev D., Angelidaki I., Lu W., Wang H.. ( 2009;). High yield simultaneous hydrogen and ethanol production under extreme-thermophilic (70°C) mixed culture environment. . Int J Hydrogen Energy 34:, 5657–5665. [CrossRef]
    [Google Scholar]
  59. Zhao C., Karakashev D., Lu W., Wang H., Angelidaki I.. ( 2010;). Xylose fermentation to biofuels (hydrogen and ethanol) by extreme thermophilic (70°C) mixed culture. . Int J Hydrogen Energy 35:, 3415–3422. [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijs.0.045211-0
Loading
/content/journal/ijsem/10.1099/ijs.0.045211-0
Loading

Data & Media loading...

Supplements

Supplementary material 

PDF

Supplementary material 

PDF

Most Cited This Month

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