1887

Abstract

A novel thermophilic, chemoheterotrophic, Gram-negative-staining, multicellular filamentous bacterium, designated strain 110S, was isolated from an iron-rich coastal hydrothermal field in Japan. The isolate is facultatively aerobic and chemoheterotrophic. Phylogenetic analysis using 16S rRNA gene sequences nested strain 110S in a novel class-level clone cluster of the phylum ‘ ’. The isolate grows by dissimilatory iron- and nitrate-reduction under anaerobic conditions, which is the first report of these abilities in the phylum ‘ ’. The organism is capable of growth with oxygen, ferric iron and nitrate as a possible electron acceptor, has a wide range of growth temperatures, and tolerates higher NaCl concentrations for growth compared to the other isolates in the phylum. Using phenotypic and phylogenetic data, strain 110S ( = JCM 17282 = NBRC 107679 = DSM 23922 = KCTC 23289 = ATCC BAA-2145) is proposed as the type strain of a novel species in a new genus, gen. nov., sp. nov. In addition, as strain 110S apparently constitutes a new class of the phylum ‘ ’ with other related uncultivated clone sequences, we propose classis nov. and the subordinate taxa ord. nov. and fam. nov.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.046532-0
2013-08-01
2020-01-23
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/63/8/2992.html?itemId=/content/journal/ijsem/10.1099/ijs.0.046532-0&mimeType=html&fmt=ahah

References

  1. Balch W. E. , Fox G. E. , Magrum L. J. , Woese C. R. , Wolfe R. S. . ( 1979; ). Methanogens: reevaluation of a unique biological group. . Microbiol Rev 43:, 260–296.[PubMed]
    [Google Scholar]
  2. Björnsson L. , Hugenholtz P. , Tyson G. W. , Blackall L. L. . ( 2002; ). Filamentous Chloroflexi (green non-sulfur bacteria) are abundant in wastewater treatment processes with biological nutrient removal. . Microbiology 148:, 2309–2318.[PubMed]
    [Google Scholar]
  3. Botero L. M. , Brown K. B. , Brumefield S. , Burr M. , Castenholz R. W. , Young M. , McDermott T. R. . ( 2004; ). Thermobaculum terrenum gen. nov., sp. nov.: a non-phototrophic gram-positive thermophile representing an environmental clone group related to the Chloroflexi (green non-sulfur bacteria) and Thermomicrobia . . Arch Microbiol 181:, 269–277. [CrossRef] [PubMed]
    [Google Scholar]
  4. Cavaletti L. , Monciardini P. , Bamonte R. , Schumann P. , Rohde M. , Sosio M. , Donadio S. . ( 2006; ). New lineage of filamentous, spore-forming, gram-positive bacteria from soil. . Appl Environ Microbiol 72:, 4360–4369. [CrossRef] [PubMed]
    [Google Scholar]
  5. Davis K. E. , Sangwan P. , Janssen P. H. . ( 2011; ). Acidobacteria, Rubrobacteridae and Chloroflexi are abundant among very slow-growing and mini-colony-forming soil bacteria. . Environ Microbiol 13:, 798–805. [CrossRef] [PubMed]
    [Google Scholar]
  6. DeLong E. F. . ( 1992; ). Archaea in coastal marine environments. . Proc Natl Acad Sci U S A 89:, 5685–5689. [CrossRef] [PubMed]
    [Google Scholar]
  7. Garrity G. M. , Holt J. G. . ( 2001a; ). Phylum BVI. Chloroflexi phy. nov. . In Bergey's Manual of Systematic Bacteriology, , 2nd edn., vol. 1, pp. 427–446. Edited by Boone D. R. , Castenholtz R. W. , Garrity G. M. . . New York:: Springer;. [CrossRef]
    [Google Scholar]
  8. Garrity G. M. , Holt J. G. . ( 2001b; ). Phylum BVII. Thermomicrobia phy. nov. . In Bergey's Manual of Systematic Bacteriology, , 2nd edn., vol. 1, pp. 447–450. Edited by Boone D. R. , Castenholtz R. W. , Garrity G. M. . . New York:: Springer;. [CrossRef]
    [Google Scholar]
  9. Grégoire P. , Bohli M. , Cayol J.-L. , Joseph M. , Guasco S. , Dubourg K. , Cambar J. , Michotey V. , Bonin P. . & other authors ( 2011a; ). Caldilinea tarbellica sp. nov., a filamentous, thermophilic, anaerobic bacterium isolated from a deep hot aquifer in the Aquitaine Basin. . Int J Syst Evol Microbiol 61:, 1436–1441. [CrossRef] [PubMed]
    [Google Scholar]
  10. Grégoire P. , Fardeau M. L. , Joseph M. , Guasco S. , Hamaide F. , Biasutti S. , Michotey V. , Bonin P. , Ollivier B. . ( 2011b; ). Isolation and characterization of Thermanaerothrix daxensis gen. nov., sp. nov., a thermophilic anaerobic bacterium pertaining to the phylum “Chloroflexi”, isolated from a deep hot aquifer in the Aquitaine Basin. . Syst Appl Microbiol 34:, 494–497. [CrossRef] [PubMed]
    [Google Scholar]
  11. Gupta R. S. , Chander P. , George S. . ( 2013a; ). Phylogenetic framework and molecular signatures for the class Chloroflexi and its different clades; proposal for division of the class Chloroflexi class. nov. into the suborder Chloroflexineae subord. nov., consisting of the emended family Oscillochloridaceae and the family Chloroflexaceae fam. nov., and the suborder Roseiflexineae subord. nov., containing the family Roseiflexaceae fam. nov.. Antonie van Leeuwenhoek 103:, 99–119. [CrossRef] [PubMed]
    [Google Scholar]
  12. Gupta R. , Chander P. , George S. . ( 2013b; ). Erratum to: Phylogenetic framework and molecular signatures for the class Chloroflexi and its different clades; proposal for division of the class Chloroflexi class. nov. into the suborder Chloroflexineae subord. nov., consisting of the emended family Oscillochloridaceae and the family Chloroflexaceae fam. nov., and the suborder Roseiflexineae subord. nov., containing the family Roseiflexaceae fam. nov.. Antonie van Leeuwenhoek 103:, 261. [CrossRef]
    [Google Scholar]
  13. Hanada S. , Hiraishi A. , Shimada K. , Matsuura K. . ( 1995; ). Chloroflexus aggregans sp. nov., a filamentous phototrophic bacterium which forms dense cell aggregates by active gliding movement. . Int J Syst Bacteriol 45:, 676–681. [CrossRef] [PubMed]
    [Google Scholar]
  14. Hanada S. , Takaichi S. , Matsuura K. , Nakamura K. . ( 2002; ). Roseiflexus castenholzii gen. nov., sp. nov., a thermophilic, filamentous, photosynthetic bacterium that lacks chlorosomes. . Int J Syst Evol Microbiol 52:, 187–193.[PubMed] [CrossRef]
    [Google Scholar]
  15. Holt J. G. , Lewin R. A. . ( 1968; ). Herpetosiphon aurantiacus gen. et sp. n., a new filamentous gliding organism. . J Bacteriol 95:, 2407–2408.[PubMed]
    [Google Scholar]
  16. Huelsenbeck J. P. , Ronquist F. . ( 2001; ). mrbayes: Bayesian inference of phylogenetic trees. . Bioinformatics 17:, 754–755. [CrossRef] [PubMed]
    [Google Scholar]
  17. Hugenholtz P. , Stackebrandt E. . ( 2004; ). Reclassification of Sphaerobacter thermophilus from the subclass Sphaerobacteridae in the phylum Actinobacteria to the class Thermomicrobia (emended description) in the phylum Chloroflexi (emended description). . Int J Syst Evol Microbiol 54:, 2049–2051. [CrossRef] [PubMed]
    [Google Scholar]
  18. Jackson T. J. , Ramaley R. F. , Meinschein W. G. . ( 1973; ). Thermomicrobium, a new genus of extremely thermophilic bacteria. . Int J Syst Bacteriol 23:, 28–36. [CrossRef]
    [Google Scholar]
  19. Kale V. , Björnsdoóttir S. H. , Friðjónsson Ó. H. , Pétursdóttir S. K. , Ómarsdóttir S. , Hreggviðsson G. Ó. . ( 2013; ). Litorilinea aerophila gen. nov., sp. nov., an aerobic member of class Caldilineae, phylum Chloroflexi, isolated from an intertidal hot spring. . Int J Syst Evol Microbiol 63:, 1149–1154. [CrossRef] [PubMed]
    [Google Scholar]
  20. Kashefi K. , Holmes D. E. , Reysenbach A. L. , Lovley D. R. . ( 2002; ). Use of Fe(III) as an electron acceptor to recover previously uncultured hyperthermophiles: isolation and characterization of Geothermobacterium ferrireducens gen. nov., sp. nov.. Appl Environ Microbiol 68:, 1735–1742. [CrossRef] [PubMed]
    [Google Scholar]
  21. Keppen O. , Baulina O. , Kondratieva E. . ( 1994; ). Oscillochloris trichoides neotype strain DG-6. . Photosynth Res 41:, 29–33. [CrossRef]
    [Google Scholar]
  22. Keppen O. I. , Tourova T. P. , Kuznetsov B. B. , Ivanovsky R. N. , Gorlenko V. M. . ( 2000; ). Proposal of Oscillochloridaceae fam. nov. on the basis of a phylogenetic analysis of the filamentous anoxygenic phototrophic bacteria, and emended description of Oscillochloris and Oscillochloris trichoides in comparison with further new isolates. . Int J Syst Evol Microbiol 50:, 1529–1537. [CrossRef] [PubMed]
    [Google Scholar]
  23. Kormas K. A. , Tamaki H. , Hanada S. , Kamagata Y. . ( 2009; ). Apparent richness and community composition of Bacteria and Archaea in geothermal springs. . Aquat Microb Ecol 57:, 113–122. [CrossRef]
    [Google Scholar]
  24. Lauerer G. , Kristjansson J. K. , Langworthy T. A. , König H. , Stetter K. O. . ( 1986; ). Methanothermus sociabilis sp. nov., a second species within the Methanothermaceae growing at 97°C. . Syst Appl Microbiol 8:, 100–105. [CrossRef]
    [Google Scholar]
  25. Löffler F. E. , Yan J. , Ritalahti K. M. , Adrian L. , Edwards E. A. , Konstantinidis K. T. , Müller J. A. , Fullerton H. , Zinder S. H. , Spormann A. M. . ( 2013; ). Dehalococcoides mccartyi gen. nov., sp. nov., obligate organohalide-respiring anaerobic bacteria, relevant to halogen cycling and bioremediation, belong to a novel bacterial class, Dehalococcoidia classis nov., order Dehalococcoidales ord. nov. and family Dehalococcoidaceae fam. nov., within the phylum Chloroflexi . . Int J Syst Evol Microbiol 63:, 625–635. [CrossRef] [PubMed]
    [Google Scholar]
  26. Lovley D. R. , Phillips E. J. . ( 1986; ). Organic matter mineralization with reduction of ferric iron in anaerobic sediments. . Appl Environ Microbiol 51:, 683–689.[PubMed]
    [Google Scholar]
  27. Lovley D. R. , Phillips E. J. . ( 1987; ). Rapid assay for microbially reducible ferric iron in aquatic sediments. . Appl Environ Microbiol 53:, 1536–1540.[PubMed]
    [Google Scholar]
  28. Lovley D. R. , Phillips E. J. . ( 1988; ). Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. . Appl Environ Microbiol 54:, 1472–1480.[PubMed]
    [Google Scholar]
  29. Lysnes K. , Thorseth I. H. , Steinsbu B. O. , Øvreås L. , Torsvik T. , Pedersen R. B. . ( 2004; ). Microbial community diversity in seafloor basalt from the Arctic spreading ridges. . FEMS Microbiol Ecol 50:, 213–230. [CrossRef] [PubMed]
    [Google Scholar]
  30. Meyer-Dombard D. A. R. , Amend J. P. , Osburn M. R. . ( 2012; ). Microbial diversity and potential for arsenic and iron biogeochemical cycling at an arsenic rich, shallow-sea hydrothermal vent (Tutum Bay, Papua New Guinea). . Chem Geol. [CrossRef]
    [Google Scholar]
  31. Moe W. M. , Yan J. , Nobre M. F. , da Costa M. S. , Rainey F. A. . ( 2009; ). Dehalogenimonas lykanthroporepellens gen. nov., sp. nov., a reductively dehalogenating bacterium isolated from chlorinated solvent-contaminated groundwater. . Int J Syst Evol Microbiol 59:, 2692–2697. [CrossRef] [PubMed]
    [Google Scholar]
  32. Nishijima M. , Araki-Sakai M. , Sano H. . ( 1997; ). Identification of isoprenoid quinones by frit-FAB liquid chromatography–mass spectrometry for the chemotaxonomy of microorganisms. . J Microbiol Methods 28:, 113–122. [CrossRef]
    [Google Scholar]
  33. Pierson B. K. , Castenholz R. W. . ( 1974; ). A phototrophic gliding filamentous bacterium of hot springs, Chloroflexus aurantiacus, gen. and sp. nov.. Arch Microbiol 100:, 5–24. [CrossRef] [PubMed]
    [Google Scholar]
  34. Podosokorskaya O. A. , Bonch-Osmolovskaya E. A. , Novikov A. A. , Kolganova T. V. , Kublanov I. V. . ( 2013; ). Ornatilinea apprima gen. nov., sp. nov., a novel cellulolytic representative of class Anaerolineae . . Int J Syst Evol Microbiol 63:, 86–92.[PubMed] [CrossRef]
    [Google Scholar]
  35. Porter K. G. , Feig Y. S. . ( 1980; ). The use of DAPI for identifying and counting aquatic microflora. . Limnol Oceanogr 25:, 943–948. [CrossRef]
    [Google Scholar]
  36. Reysenbach A. L. , Liu Y. , Banta A. B. , Beveridge T. J. , Kirshtein J. D. , Schouten S. , Tivey M. K. , Von Damm K. L. , Voytek M. A. . ( 2006; ). A ubiquitous thermoacidophilic archaeon from deep-sea hydrothermal vents. . Nature 442:, 444–447. [CrossRef] [PubMed]
    [Google Scholar]
  37. Roeselers G. , Norris T. B. , Castenholz R. W. , Rysgaard S. , Glud R. N. , Kühl M. , Muyzer G. . ( 2007; ). Diversity of phototrophic bacteria in microbial mats from Arctic hot springs (Greenland). . Environ Microbiol 9:, 26–38. [CrossRef] [PubMed]
    [Google Scholar]
  38. Sako Y. , Takai K. , Ishida Y. , Uchida A. , Katayama Y. . ( 1996; ). Rhodothermus obamensis sp. nov., a modern lineage of extremely thermophilic marine bacteria. . Int J Syst Bacteriol 46:, 1099–1104. [CrossRef] [PubMed]
    [Google Scholar]
  39. Schmitt S. , Deines P. , Behnam F. , Wagner M. , Taylor M. W. . ( 2011; ). Chloroflexi bacteria are more diverse, abundant, and similar in high than in low microbial abundance sponges. . FEMS Microbiol Ecol 78:, 497–510. [CrossRef] [PubMed]
    [Google Scholar]
  40. Sekiguchi Y. , Yamada T. , Hanada S. , Ohashi A. , Harada H. , Kamagata Y. . ( 2003; ). Anaerolinea thermophila gen. nov., sp. nov. and Caldilinea aerophila gen. nov., sp. nov., novel filamentous thermophiles that represent a previously uncultured lineage of the domain Bacteria at the subphylum level. . Int J Syst Evol Microbiol 53:, 1843–1851. [CrossRef] [PubMed]
    [Google Scholar]
  41. Seshadri R. , Adrian L. , Fouts D. E. , Eisen J. A. , Phillippy A. M. , Methe B. A. , Ward N. L. , Nelson W. C. , Deboy R. T. . & other authors ( 2005; ). Genome sequence of the PCE-dechlorinating bacterium Dehalococcoides ethenogenes . . Science 307:, 105–108. [CrossRef] [PubMed]
    [Google Scholar]
  42. Sievert S. M. , Brinkhoff T. , Muyzer G. , Ziebis W. , Kuever J. . ( 1999; ). Spatial heterogeneity of bacterial populations along an environmental gradient at a shallow submarine hydrothermal vent near Milos Island (Greece). . Appl Environ Microbiol 65:, 3834–3842.[PubMed]
    [Google Scholar]
  43. Slobodkin A. I. , Wiegel J. . ( 1997; ). Fe(III) as an electron acceptor for H2 oxidation in thermophilic anaerobic enrichment cultures from geothermal areas. . Extremophiles 1:, 106–109. [CrossRef] [PubMed]
    [Google Scholar]
  44. Slobodkin A. I. , Jeanthon C. , L’Haridon S. , Nazina T. , Miroshnichenko M. , Bonch-Osmolovskaya E. . ( 1999; ). Dissimilatory reduction of Fe(III) by thermophilic bacteria and archaea in deep subsurface petroleum reservoirs of western siberia. . Curr Microbiol 39:, 99–102. [CrossRef] [PubMed]
    [Google Scholar]
  45. Slobodkin A. I. , Campbell B. , Cary S. C. , Bonch-Osmolovskaya E. , Jeanthon C. . ( 2001; ). Evidence for the presence of thermophilic Fe(III)-reducing microorganisms in deep-sea hydrothermal vents at 13 degrees N (East Pacific Rise). . FEMS Microbiol Ecol 36:, 235–243.[PubMed]
    [Google Scholar]
  46. Slobodkina G. B. , Panteleeva A. N. , Sokolova T. G. , Bonch-Osmolovskaya E. A. , Slobodkin A. I. . ( 2012; ). Carboxydocella manganica sp. nov., a thermophilic, dissimilatory Mn(IV)- and Fe(III)-reducing bacterium from a Kamchatka hot spring. . Int J Syst Evol Microbiol 62:, 890–894. [CrossRef] [PubMed]
    [Google Scholar]
  47. Stamatakis A. . ( 2006; ). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. . Bioinformatics 22:, 2688–2690. [CrossRef] [PubMed]
    [Google Scholar]
  48. Stamatakis A. , Hoover P. , Rougemont J. . ( 2008; ). A rapid bootstrap algorithm for the RAxML Web servers. . Syst Biol 57:, 758–771. [CrossRef] [PubMed]
    [Google Scholar]
  49. Stookey L. L. . ( 1970; ). Ferrozine – a new spectrophotometric reagent for iron. . Anal chem 42:, 779–781. [CrossRef]
    [Google Scholar]
  50. Takai K. , Nakagawa S. , Sako Y. , Horikoshi K. . ( 2003; ). Balnearium lithotrophicum gen. nov., sp. nov., a novel thermophilic, strictly anaerobic, hydrogen-oxidizing chemolithoautotroph isolated from a black smoker chimney in the Suiyo Seamount hydrothermal system. . Int J Syst Evol Microbiol 53:, 1947–1954. [CrossRef] [PubMed]
    [Google Scholar]
  51. Teske A. , Hinrichs K. U. , Edgcomb V. , de Vera Gomez A. , Kysela D. , Sylva S. P. , Sogin M. L. , Jannasch H. W. . ( 2002; ). Microbial diversity of hydrothermal sediments in the Guaymas Basin: evidence for anaerobic methanotrophic communities. . Appl Environ Microbiol 68:, 1994–2007. [CrossRef] [PubMed]
    [Google Scholar]
  52. Trick I. , Lingens F. . ( 1984; ). Characterization of Herpetosiphon spec. —A gliding filamentous bacterium from bulking sludge. . Appl Microbiol Biotechnol 19:, 191–198. [CrossRef]
    [Google Scholar]
  53. Vargas M. , Kashefi K. , Blunt-Harris E. L. , Lovley D. R. . ( 1998; ). Microbiological evidence for Fe(III) reduction on early Earth. . Nature 395:, 65–67. [CrossRef] [PubMed]
    [Google Scholar]
  54. Weber K. A. , Achenbach L. A. , Coates J. D. . ( 2006; ). Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. . Nat Rev Microbiol 4:, 752–764. [CrossRef] [PubMed]
    [Google Scholar]
  55. Wu D. , Raymond J. , Wu M. , Chatterji S. , Ren Q. , Graham J. E. , Bryant D. A. , Robb F. , Colman A. . & other authors ( 2009; ). Complete genome sequence of the aerobic CO-oxidizing thermophile Thermomicrobium roseum . . PLoS ONE 4:, e4207. [CrossRef] [PubMed]
    [Google Scholar]
  56. Yabe S. , Aiba Y. , Sakai Y. , Hazaka M. , Yokota A. . ( 2010; ). Thermosporothrix hazakensis gen. nov., sp. nov., isolated from compost, description of Thermosporotrichaceae fam. nov. within the class Ktedonobacteria Cavaletti et al. 2007 and emended description of the class Ktedonobacteria . . Int J Syst Evol Microbiol 60:, 1794–1801. [CrossRef] [PubMed]
    [Google Scholar]
  57. Yabe S. , Aiba Y. , Sakai Y. , Hazaka M. , Yokota A. . ( 2011; ). Thermogemmatispora onikobensis gen. nov., sp. nov. and Thermogemmatispora foliorum sp. nov., isolated from fallen leaves on geothermal soils, and description of Thermogemmatisporaceae fam. nov. and Thermogemmatisporales ord. nov. within the class Ktedonobacteria . . Int J Syst Evol Microbiol 61:, 903–910. [CrossRef] [PubMed]
    [Google Scholar]
  58. Yamada T. , Sekiguchi Y. , Hanada S. , Imachi H. , Ohashi A. , Harada H. , Kamagata Y. . ( 2006; ). Anaerolinea thermolimosa sp. nov., Levilinea saccharolytica gen. nov., sp. nov. and Leptolinea tardivitalis gen. nov., sp. nov., novel filamentous anaerobes, and description of the new classes Anaerolineae classis nov. and Caldilineae classis nov. in the bacterial phylum Chloroflexi . . Int J Syst Evol Microbiol 56:, 1331–1340. [CrossRef] [PubMed]
    [Google Scholar]
  59. Yamada T. , Imachi H. , Ohashi A. , Harada H. , Hanada S. , Kamagata Y. , Sekiguchi Y. . ( 2007; ). Bellilinea caldifistulae gen. nov., sp. nov. and Longilinea arvoryzae gen. nov., sp. nov., strictly anaerobic, filamentous bacteria of the phylum Chloroflexi isolated from methanogenic propionate-degrading consortia. . Int J Syst Evol Microbiol 57:, 2299–2306. [CrossRef] [PubMed]
    [Google Scholar]
  60. Yan J. , Rash B. A. , Rainey F. A. , Moe W. M. . ( 2009; ). Isolation of novel bacteria within the Chloroflexi capable of reductive dechlorination of 1,2,3-trichloropropane. . Environ Microbiol 11:, 833–843. [CrossRef] [PubMed]
    [Google Scholar]
  61. Yoneda Y. , Yoshida T. , Kawaichi S. , Daifuku T. , Takabe K. , Sako Y. . ( 2012; ). Carboxydothermus pertinax sp. nov., a thermophilic, hydrogenogenic, Fe(III)-reducing, sulfur-reducing carboxydotrophic bacterium from an acidic hot spring. . Int J Syst Evol Microbiol 62:, 1692–1697. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijs.0.046532-0
Loading
/content/journal/ijsem/10.1099/ijs.0.046532-0
Loading

Data & Media loading...

Supplements

Supplementary material 

PDF

Most cited articles

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