1887

Abstract

Several strictly anaerobic bacteria that are Gram-stain-positive have the ability to use uric acid as the sole source of carbon and energy. The phylogeny of three such species, , , and , members of the cluster XII that ferment purines, but not most amino acids or carbohydrates, has been re-examined, taking advantage of their recently sequenced genomes. Phylogenetic analyses, based on 16S rRNA gene sequences, protein sequences of RpoB and GyrB, and on a concatenated alignment of 50 ribosomal proteins, revealed tight clustering of and showed consistent association with and , but differed from these two in terms of the genome size, G+C content of its chromosomal DNA and its inability to form spores. We propose reassigning and to the novel genus as gen. nov. comb. nov. (the type species of the genus) and comb. nov., respectively. is proposed to be reclassified as gen. nov. comb. nov. Furthermore, based on the phylogenetic data and similar metabolic properties, we propose assigning genera and to the novel family Metagenomic sequencing data indicate the widespread distibution of organisms falling within the radiation of the proposed family in terrestrial and aquatic habitats from upstate New York to Antarctica, most likely due to their ability to metabolize avian-produced uric acid.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.002008
2017-08-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/67/8/2711.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.002008&mimeType=html&fmt=ahah

References

  1. Ludwig W, Schleifer K-H, Whitman WB. Revised road map to the phylum Firmicutes. In De Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W et al. (editors) Bergey's Manual of Systematic Bacteriology, 2nd ed. vol. 3 The Firmicutes New York: Springer; 2009 pp. 1–24
    [Google Scholar]
  2. Rainey FA, Hollen BJ, Small A. Genus I. Clostridium. In De Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W et al. (editors) Bergey's Manual of Systematic Bacteriology 2nd ed, vol. 3, The Firmicutes New York: Springer; 2009 pp. 738–828
    [Google Scholar]
  3. Parte AC. LPSN - list of prokaryotic names with standing in nomenclature. Nucleic Acids Res 2014; 42:D613–D616 [View Article][PubMed]
    [Google Scholar]
  4. Collins MD, Lawson PA, Willems A, Cordoba JJ, Fernandez-Garayzabal J et al. The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol 1994; 44:812–826 [View Article][PubMed]
    [Google Scholar]
  5. Marchandin H, Teyssier C, Campos J, Jean-Pierre H, Roger F et al. Negativicoccus succinicivorans gen. nov., sp. nov., isolated from human clinical samples, emended description of the family Veillonellaceae and description of Negativicutes classis nov., Selenomonadales ord. nov. and Acidaminococcaceae fam. nov. in the bacterial phylum Firmicutes. Int J Syst Evol Microbiol 2010; 60:1271–1279 [View Article][PubMed]
    [Google Scholar]
  6. Ludwig W, Schleifer K-H, Whitman WB. Taxonomic outline of the phylum Firmicutes. In De Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W et al. (editors) Bergey's Manual of Systematic Bacteriology, 2nd ed. vol. 3 The Firmicutes New York: Springer; 2009 pp. 15–17
    [Google Scholar]
  7. Lawson PA, Rainey FA. Proposal to restrict the genus Clostridium (Prazmowski) to Clostridium butyricum and related species. Int J Syst Evol Microbiol 2015; 66:1009–1016 [View Article][PubMed]
    [Google Scholar]
  8. Farrow JA, Lawson PA, Hippe H, Gauglitz U, Collins MD. 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 1995; 45:436–440 [View Article][PubMed]
    [Google Scholar]
  9. Yutin N, Galperin MY. A genomic update on clostridial phylogeny: Gram-negative spore formers and other misplaced clostridia. Environ Microbiol 2013; 15:2341–2641 [View Article][PubMed]
    [Google Scholar]
  10. Bae JW, Park JR, Chang YH, Rhee SK, Kim BC et al. Clostridium hastiforme is a later synonym of Tissierella praeacuta. Int J Syst Evol Microbiol 2004; 54:947–949 [View Article][PubMed]
    [Google Scholar]
  11. Johnson CN, Whitehead TR, Cotta MA, Rhoades RE, Lawson PA et al. Peptoniphilus stercorisuis sp. nov., isolated from a swine manure storage tank and description of Peptoniphilaceae fam. nov. Int J Syst Evol Microbiol 2014; 64:3538–3545 [View Article][PubMed]
    [Google Scholar]
  12. Alauzet C, Marchandin H, Courtin P, Mory F, Lemée L et al. Multilocus analysis reveals diversity in the genus Tissierella: description of Tissierella carlieri sp. nov. in the new class Tissierellia classis nov. Syst Appl Microbiol 2014; 37:23–34 [View Article][PubMed]
    [Google Scholar]
  13. Federhen S. Type material in the NCBI taxonomy database. Nucleic Acids Res 2015; 43:D1086–D1098 [View Article][PubMed]
    [Google Scholar]
  14. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22:4673–4680 [View Article][PubMed]
    [Google Scholar]
  15. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article][PubMed]
    [Google Scholar]
  16. Durre P, Andersch W, Andreesen JR. Isolation and characterization of an Adenine-Utilizing, anaerobic sporeformer, Clostridium purinolyticum sp. nov. Int J Syst Bacteriol 1981; 31:184–194 [View Article]
    [Google Scholar]
  17. Dürre P, Andreesen JR. Purine and glycine metabolism by purinolytic clostridia. J Bacteriol 1983; 154:192–199[PubMed]
    [Google Scholar]
  18. Hartwich K, Poehlein A, Daniel R. The purine-utilizing bacterium Clostridium acidurici 9a: a genome-guided metabolic reconsideration. PLoS One 2012; 7:e51662 [View Article][PubMed]
    [Google Scholar]
  19. Harms C, Schleicher A, Collins MD, Andreesen JR. Tissierella creatinophila sp. nov., a gram-positive, anaerobic, non-spore-forming, creatinine-fermenting organism. Int J Syst Bacteriol 1998; 48:983–993 [View Article][PubMed]
    [Google Scholar]
  20. Parshina SN, Kleerebezem R, Sanz JL, Lettinga G, Nozhevnikova AN et al. Soehngenia saccharolytica gen. nov., sp. nov. and Clostridium amygdalinum sp. nov., two novel anaerobic, benzaldehyde-converting bacteria. Int J Syst Evol Microbiol 2003; 53:1791–1799 [View Article][PubMed]
    [Google Scholar]
  21. Rezgui R, Maaroufi A, Fardeau ML, Ben Ali Gam Z, Cayol JL et al. Anaerosalibacter bizertensis gen. nov., sp. nov., a halotolerant bacterium isolated from sludge. Int J Syst Evol Microbiol 2012; 62:2469–2474 [View Article][PubMed]
    [Google Scholar]
  22. Yutin N, Puigbò P, Koonin EV, Wolf YI. Phylogenomics of prokaryotic ribosomal proteins. PLoS One 2012; 7:e36972 [View Article][PubMed]
    [Google Scholar]
  23. Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W et al. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 2014; 12:635–645 [View Article][PubMed]
    [Google Scholar]
  24. Qin QL, Xie BB, Zhang XY, Chen XL, Zhou BC et al. A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 2014; 196:2210–2215 [View Article][PubMed]
    [Google Scholar]
  25. Wiegel J, Tanner R, Rainey FA. An introduction to the family Clostridiaceae. In Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E. (editors) The Prokaryotes : Bacteria: Firmicutes, Cyanobacteria vol. 4 2006 pp. 654–678
    [Google Scholar]
  26. Galperin MY, Mekhedov SL, Puigbo P, Smirnov S, Wolf YI et al. Genomic determinants of sporulation in Bacilli and Clostridia: towards the minimal set of sporulation-specific genes. Environ Microbiol 2012; 14:2870–2890 [View Article][PubMed]
    [Google Scholar]
  27. Beuscher HU, Andreesen JR. Eubacterium angustum sp. nov., a Gram-positive anaerobic, non-sporeforming, obligate purine fermenting organism. Arch Microbiol 1984; 140:2–8 [View Article]
    [Google Scholar]
  28. Poehlein A, Galperin MY, Andreesen JR, Daniel R. Genome sequence of uric acid-fermenting Eubacterium angustum DSM 1989T (MK-1). Genome Announc 2017; 5:e01439-16 [View Article][PubMed]
    [Google Scholar]
  29. Barker HA, Beck JV. Clostridium acidi-uridi and Clostridium cylindrosporum, organisms fermenting uric acid and some other purines. J Bacteriol 1942; 43:291–304[PubMed]
    [Google Scholar]
  30. Harris JK, Caporaso JG, Walker JJ, Spear JR, Gold NJ et al. Phylogenetic stratigraphy in the Guerrero Negro hypersaline microbial mat. ISME J 2013; 7:50–60 [View Article][PubMed]
    [Google Scholar]
  31. Isenbarger TA, Finney M, Rios-Velazquez C, Handelsman J, Ruvkun G. Miniprimer PCR, a new lens for viewing the microbial world. Appl Environ Microbiol 2008; 74:840–849 [CrossRef]
    [Google Scholar]
  32. Meyer KM, Macalady JL, Fulton JM, Kump LR, Schaperdoth I et al. Carotenoid biomarkers as an imperfect reflection of the anoxygenic phototrophic community in meromictic Fayetteville Green Lake. Geobiology 2011; 9:321–329 [View Article][PubMed]
    [Google Scholar]
  33. Li J, Li F, Yu S, Qin S, Wang G. Impacts of mariculture on the diversity of bacterial communities within intertidal sediments in the Northeast of China. Microb Ecol 2013; 66:861–870 [View Article][PubMed]
    [Google Scholar]
  34. Aislabie J, Jordan S, Ayton J, Klassen JL, Barker GM et al. Bacterial diversity associated with ornithogenic soil of the Ross Sea region, Antarctica. Can J Microbiol 2009; 55:21–36 [View Article][PubMed]
    [Google Scholar]
  35. Kim OS, Chae N, Lim HS, Cho A, Kim JH et al. Bacterial diversity in ornithogenic soils compared to mineral soils on King George Island, Antarctica. J Microbiol 2012; 50:1081–1085 [View Article][PubMed]
    [Google Scholar]
  36. Banks JC, Cary SC, Hogg ID. The phylogeography of Adelie penguin faecal flora. Environ Microbiol 2009; 11:577–588 [View Article][PubMed]
    [Google Scholar]
  37. Tkavc R, Ausec L, Oren A, Gunde-Cimerman N. Bacteria associated with Artemia spp. along the salinity gradient of the solar salterns at Eilat (Israel). FEMS Microbiol Ecol 2011; 77:310–321 [View Article][PubMed]
    [Google Scholar]
  38. Oikonomou G, Machado VS, Santisteban C, Schukken YH, Bicalho RC. Microbial diversity of bovine mastitic milk as described by pyrosequencing of metagenomic 16s rDNA. PLoS One 2012; 7:e47671 [View Article][PubMed]
    [Google Scholar]
  39. Garcia SL, Jangid K, Whitman WB, das KC. Transition of microbial communities during the adaption to anaerobic digestion of carrot waste. Bioresour Technol 2011; 102:7249–7256 [View Article][PubMed]
    [Google Scholar]
  40. Smith AM, Sharma D, Lappin-Scott H, Burton S, Huber DH. Microbial community structure of a pilot-scale thermophilic anaerobic digester treating poultry litter. Appl Microbiol Biotechnol 2014; 98:2321–2334 [View Article][PubMed]
    [Google Scholar]
  41. Yilmaz P, Parfrey LW, Yarza P, Gerken J, Pruesse E et al. The SILVA and "All-species Living Tree Project (LTP)" taxonomic frameworks. Nucleic Acids Res 2014; 42:D643–D648 [View Article][PubMed]
    [Google Scholar]
  42. Barker HA, Peterson WH. The nutritional requirements of Clostridium acidi-urici. J Bacteriol 1944; 47:307–308[PubMed]
    [Google Scholar]
  43. Poehlein A, Bengelsdorf FR, Schiel-Bengelsdorf B, Daniel R, Dürre P. Draft genome sequence of purine-degrading Gottschalkia purinilyticum (formerly Clostridium purinilyticum) WA1 (DSM 1384). Genome Announc 2015; 3:e0108801015 [View Article][PubMed]
    [Google Scholar]
  44. Wade WG. Genus I. Eubacterium. In De Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W et al. (editors) Bergey's Manual of Systematic Bacteriology, 2nd ed. vol. 3 The Firmicutes New York: Springer; 2009 pp. 865–891
    [Google Scholar]
  45. Lawson PA, Citron DM, Tyrrell KL, Finegold SM. Reclassification of Clostridium difficile as Clostridioides difficile (Hall and O'Toole 1935) Prévot 1938. Anaerobe 2016; 40:95–99 [View Article][PubMed]
    [Google Scholar]
  46. Galperin MY, Brover V, Tolstoy I, Yutin N. Phylogenomic analysis of the family Peptostreptococcaceae (Clostridium cluster XI) and proposal for reclassification of Clostridium litorale (Fendrich et al. 1991) and Eubacterium acidaminophilum (Zindel et al. 1989) as Peptoclostridium litorale gen. nov. comb. nov. and Peptoclostridium acidaminophilum comb. nov. Int J Syst Evol Microbiol 2016; 66:5506–5513 [View Article][PubMed]
    [Google Scholar]
  47. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 1993; 10:512–526[PubMed]
    [Google Scholar]
  48. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article][PubMed]
    [Google Scholar]
  49. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article][PubMed]
    [Google Scholar]
  50. Anisimova M, Gil M, Dufayard JF, Dessimoz C, Gascuel O. Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes. Syst Biol 2011; 60:685–699 [View Article][PubMed]
    [Google Scholar]
  51. Collins MD, Shah HN. Reclassification of Bacteroides praeacutus Tissier (Holdeman and Moore) in a new genus, Tissierella, as Tissierella praeacuta comb. nov. Int J Syst Bacteriol 1986; 36:461–463 [View Article]
    [Google Scholar]
  52. Dione N, Sankar SA, Lagier JC, Khelaifia S, Michele C et al. Genome sequence and description of Anaerosalibacter massiliensis sp. nov. New Microbes New Infect 2016; 10:66–76 [View Article][PubMed]
    [Google Scholar]
  53. Schnurer A, Schink B, Svensson BH. Clostridium ultunense sp. nov., a mesophilic bacterium oxidizing acetate in syntrophic association with a hydrogenotrophic methanogenic bacterium. Int J Syst Bacteriol 1996; 46:1145–1152 [View Article][PubMed]
    [Google Scholar]
  54. Wei Y, Zhou H, Zhang L, Zhang J, Wang Y et al. Draft genome sequence of Clostridium ultunense strain BS (DSMZ 10521), recovered from a mixed culture. Genome Announc 2014; 2:e01269-13 [View Article][PubMed]
    [Google Scholar]
  55. Schiefer-Ullrich H, Wagner R, Dürre P, Andreesen JR. Comparative studies on physiology and taxonomy of obligately purinolytic clostridia. Arch Microbiol 1984; 138:345–353 [View Article][PubMed]
    [Google Scholar]
  56. Andreesen JR, Zindel U, Durre P. Clostridium cylindrosporum (ex Barker and Beck 1942) nom. rev. Int J Syst Bacteriol 1985; 35:206–208 [View Article]
    [Google Scholar]
  57. Poehlein A, Montoya Solano JD, Bengelsdorf FR, Schiel-Bengelsdorf B, Daniel R et al. Draft genome sequence of purine-degrading Clostridium cylindrosporum HC-1 (DSM 605). Genome Announc 2015; 3:e00917-15 [View Article][PubMed]
    [Google Scholar]
  58. Sasser M. Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids, MIDI Technical Note 101. Newark, DE: MIDI Inc; 2001
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.002008
Loading
/content/journal/ijsem/10.1099/ijsem.0.002008
Loading

Data & Media loading...

Supplements

Supplementary File 1

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