Skip to main content
SpringerLink
Log in

Bacillus bingmayongensis sp. nov., isolated from the pit soil of Emperor Qin’s Terra-cotta warriors in China

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

An Erratum to this article was published on 21 March 2014

Abstract

A Bacillus-like isolate, strain FJAT-13831T, isolated from the No. 1 pit soil of Emperor Qin’s Terra-cotta Warriors in Xi’an City, China, was studied to determine its taxonomic status. Dominant fatty acids of this organism included iso-C15:0, iso-C17:0, C16:0, iso-C13:0, anteiso-C15:0, and iso-C17:1ω5c. Comparative 16S rRNA gene sequence analysis confirmed the affiliation of this isolate to the genus Bacillus and indicated that it was closely related to Bacillus pseudomycoides DSM 12442T (99.72 % similarity). A phylogenetic analysis of the gyrB gene sequence similarities exhibited independent clustering of the isolate FJAT-13831T and showed 93.8 % (<95 %) sequence similarity with its closest phylogenetic neighbour B. pseudomycoides DSM 12442T. Separate standing of the strain FJAT-13831T was supported by a whole genome-based phylogenetic analysis with an average nucleotide identity value of 91.47 (<95 %) between isolate FJAT-13831T and B. pseudomycoides DSM 12442T and was consistent with the results of DNA–DNA hybridization (69.1 % relatedness). These findings support the conclusion that the isolate FJAT-13831T represents a novel species, for which the name Bacillus bingmayongensis sp. nov. is proposed. The type strain is FJAT-13831T (= CGMCC 1.12043T = DSM 25427T).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Ahmed I, Yokota A, Yamazoe A, Fujiwara T (2007) Proposal of Lysinibacillus boronitolerans gen. nov. sp. nov., and transfer of B. fusiformis to L. fusiformis comb. nov. and Bacillus sphaericus to L. sphaericus comb. nov. Int J Syst Evol Microbiol 57:1117–1125

    Article  CAS  PubMed  Google Scholar 

  • Atlas RM (1993) Handbook of microbiological media, 2nd edn. In: Parks LC (ed). CRC Press, Boca Raton

  • Baik KS, Lim CH, Park SC, Kim EM, Rhee MS, Seong CN (2010) Bacillus rigui sp. nov., isolated from wetland fresh water. Int J Syst Evol Microbiol 60:2204–2209

    Article  CAS  PubMed  Google Scholar 

  • Bhandari V, Ahmod NZ, Shah HN, Gupta RS (2013) Molecular signatures for Bacillus species: demarcation of the B. subtilis and B. cereus clades in molecular terms and proposal to limit the placement of new species into the genus Bacillus. Int J Syst Evol Microbiol 63:2712–2726

    Article  CAS  PubMed  Google Scholar 

  • Chen YG, Hao DF, Chen QH, Zhang YQ, Liu JB, He JW, Tang SK, Li WJ (2011) Bacillus hunanensis sp. nov., a slightly halophilic bacterium isolated from non-saline forest soil. Antonie Van Leeuwenhoek 99:481–488

    Article  PubMed  Google Scholar 

  • Cohn F (1872) Untersuchungen über Bacterien. Beitrage zur Biologie der Pflanzen 1:127–244

    Google Scholar 

  • De Ley J, Cattoir H, Cattoir R, Reynaert A (1970) The quantitative measurement of DNA hybridization from renaturation rates. Eur J Biochem 12:133–142

    Article  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evol 40:783–791

    Article  Google Scholar 

  • Gatson JW, Benz BF, Chandrasekaran C, Satomi M, Venkateswaran K, Hart ME (2006) Bacillus tequilensis sp. nov., isolated from a 2000-year-old Mexican shaft-tomb, is closely related to B. subtilis. Int J Syst Evol Microbiol 56:1475–1484

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez JM, Saiz-Jimenez C (2005) A simple fluorimetric method for the estimation of DNA–DNA relatedness between closely related microorganisms by thermal denaturation temperatures. Extremophiles 9:75–79

    Article  CAS  PubMed  Google Scholar 

  • Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91

    Article  CAS  PubMed  Google Scholar 

  • Gregersen T (1978) Rapid method for distinction of Gram–negative from Gram–positive bacteria. Eur J Appl Microbiol Biotechnol 5:123–127

    Article  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comp Appl Biosci 3:8275–8282

    Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism, vol 3. Academic Press, New York, pp 21–132

    Chapter  Google Scholar 

  • Jung MY, Kim JS, Paek WK, Lim J, Lee H, Kim PI, Ma JY, Kim W, Chang YH (2011) Bacillus manliponensis sp. nov., a new member of the B. cereus group isolated from foreshore tidal flat sediment. J Microbiol 49:1027–1032

    Article  PubMed  Google Scholar 

  • Kämpfer P, Blasczyk K, Auling G (1994) Characterization of Aeromonas genomic species by using quinone, polyamine, and fatty acid patterns. Can J Microbiol 40:844–850

    Article  PubMed  Google Scholar 

  • Kaneda T (1977) Fatty acids of the genus Bacillus: an example of branched-chain preference. Bacteriol Rev 41:391–418

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kim OS, Cho YJ, Lee K, Yoon SH, Na H, Kim M, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon–e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721

    Article  CAS  PubMed  Google Scholar 

  • Konstantinidis KT, Tiedje JM (2005a) Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci USA 102:2567–2572

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Konstantinidis KT, Tiedje JM (2005b) Towards a genome based taxonomy for prokaryotes. J Bacteriol 187:6258–6264

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • La Duc MT, Satomi M, Agata N, Venkateswaran K (2004a) gyrB as a phylogenetic discriminator for members of the Bacillus anthracis-cereus-thuringiensis group. J Microbiol Methods 56:383–394

    Article  PubMed  Google Scholar 

  • La Duc MT, Satomi M, Venkateswaran K (2004b) Bacillus odysseyi sp. nov., a round-spore-forming Bacillus isolated from the Mars Odyssey spacecraft. Int J Syst Evol Microbiol 54:195–201

    Article  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Liu B, Liu GH, Lin NQ, Tang JY (2012a) Bacillus identification and phylogenetic analysis, isolated from the 1st pit soil of Emperor Qin’s Terracotta Warrior. Fujian J Agric Sci 27:563–573

    Google Scholar 

  • Liu GH, Liu B, Lin NQ, Tang WQ, Tang JY, Lin YZ (2012b) Genome sequence of the aerobic bacterium Bacillus sp. strain FJAT-13831. J Bacteriol 194:6633

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Logan NA, Berkeley RCW (1984) Identification of Bacillus strains using the API system. J Gen Microbiol 130:1871–1882

    CAS  PubMed  Google Scholar 

  • Nazina TN, Lebedeva EV, Poltaraus AB, Tourova TP, Grigoryan AA, Sokolova DSH, Lysenko AM, Osipov GA (2004) Geobacillus gargensis sp. nov., a novel thermophile from a hot spring, and the reclassification of Bacillus vulcani as Geobacillus vulcani comb. nov. Int J Syst Evol Microbiol 54:2019–2024

    Article  CAS  PubMed  Google Scholar 

  • Owen RJ, Hill LR (1979) The estimation of base compositions, base pairing and genome size of bacterial deoxyribonucleic acids. In: Skinner FA, Lovelock DW (eds) Identification methods for microbiologists (Society for Applied Bacteriology Technical Series no. 14), 2nd edn. Academic Press, London, pp 277–296

    Google Scholar 

  • Priest FG (1993) Systematics and ecology of Bacillus. In: Sonenshein AL, Hoch JA, Losick R (eds) Bacillus subtilis and other Gram-positive bacteria—Biochemistry, physiology, and molecular genetics. ASM press, American Society for Microbiology, Washington. ISBN 1-55581-053-5

  • Priest FG, Goodfellow M, Todd C (1988) A numerical classification of the genus Bacillus. J Gen Microbiol 134:1847–1882

    CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sambrook J, Fritschi EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. In: Klement S, Rudolf K, Sands D (eds) Methods in phytobacteriology. Akademiai Kiado, Budapest, pp 199–204

    Google Scholar 

  • Satomi M, Kimura B, Hamada T, Harayama S, Fujii T (2002) Phylogenetic study of the genus Oceanospirillum based on 16S rRNA and gyrB genes: emended description of the genus Oceanospirillum, description of Pseudospirillum gen. nov., Oceanobacter gen. nov. and Terasakiella gen. nov. and transfer of Oceanospirillum jannaschii and Pseudomonas stanieri to Marinobacterium as Marinobacterium jannaschii comb. nov. and Marinobacterium stanieri comb. nov. Int J Syst Evol Microbiol 52:739–747

    Article  CAS  PubMed  Google Scholar 

  • Satomi M, Oikawa H, Yano Y (2003) Shewanella marinintestina sp. nov., Shewanella schlegeliana sp. nov. and Shewanella sairae sp. nov., novel eicosapentaenoic acid-producing marine bacteria isolated from sea-animal intestines. Int J Syst Evol Microbiol 53:491–499

    Article  CAS  PubMed  Google Scholar 

  • Satomi M, Kimura B, Hayashi M, Okuzumi M, Fujii T (2004) Marinospirillum insulare sp. nov., a novel halophilic helical bacterium isolated from kusaya gravy. Int J Syst Evol Microbiol 54:163–167

    Article  CAS  PubMed  Google Scholar 

  • Satomi M, La Duc MT, Venkateswaran K (2006) Bacillus safensis sp. nov., isolated from spacecraft and assembly facility surfaces. Int J Syst Evol Microbiol 56:1735–1740

    Article  CAS  PubMed  Google Scholar 

  • Schleifer KH, Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36:407–477

    CAS  PubMed Central  PubMed  Google Scholar 

  • Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, pp 607–654

    Google Scholar 

  • Sorokin A, Candelon B, Guilloux K, Galleron N, Wackerow-Kouzova N, Ehrlich SD, Bourguet D, Sanchis V (2006) Multiple-locus sequence typing analysis of B. cereus and B. thuringiensis reveals separate clustering and a distinct population structure of psychrotrophic strains. Appl Environ Microbiol 72:1569–1578

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–155

    Google Scholar 

  • Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA–DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849

    Article  CAS  Google Scholar 

  • Stackebrandt E, Liesack W (1993) Nucleic acids and classification. In: Goodfellow M, O’Donnell AG (eds) Handbook of new bacterial systematics. Academic Press, London, pp 152–189

    Google Scholar 

  • Takami H (2007) Genomic diversity of Bacillus-related species. Nova Science Publisher, New York. ISBN 978-1-–60456–396–2

  • Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56(4):564–577

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. PNAS 101:11030–11035

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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(10):2731–2739

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vanlaere E, Baldwin A, Gevers D, Henry D, De Brandt E, LiPuma JJ, Mahenthiralingam E, Speert DP, Dowson C, Vandamme P (2009) Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminans sp. nov. and Burkholderia lata sp. nov. Int J Syst Evol Microbiol 59:102–111

    Article  CAS  PubMed  Google Scholar 

  • Venkateswaran K, Dohmoto N, Harayama S (1998) Cloning and nucleotide sequence of the gyrB gene of Vibrio parahaemolyticus and its application in detection of this pathogen in shrimp. Appl Environ Microbiol 64:681–687

    CAS  PubMed Central  PubMed  Google Scholar 

  • Venkateswaran K, Moser DP, Dollhopf ME, Lies DP, Saffarini DA, MacGregor BJ, Ringelberg DB, White DC, Nishijima M (1999) Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov. Int J Syst Bacteriol 49:705–724

    Article  CAS  PubMed  Google Scholar 

  • Wang LT, Lee FL, Tai CJ, Kasai H (2007) Comparison of gyrB gene sequences, 16S rRNA gene sequences and DNA–DNA hybridization in the B. subtilis group. Int J Syst Bacteriol 57:1846–1850

    Article  CAS  Google Scholar 

  • Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE (1987) International committee on systematic bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37: 463–464

    Google Scholar 

  • Yamamoto S, Harayama S (1995) PCR amplification and direct sequencing of gyrB gene with universal primers and their application to the detection and taxonomic analysis of Pseudomonas putida strains. Appl Environ Microbiol 61:1104–1109

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang L, Wu GL, Wang Y, Dai J, Fang CX (2011) Bacillus deserti sp. nov., a novel bacterium isolated from the desert of Xinjiang, China. Antonie Van Leeuwenhoek 99:221–229

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to Dr. Jean P. Euzeby (Society for Systematic and Veterinary Bacteriology, France) for his advice on nomenclatural queries and Dr. Peter Schumann (DSMZ, Germany) for his contribution to the analysis of the cell wall composition of the strain FJAT-13831T. This work was supported by the National fund projects (31370059), by the National Key Project of Fundamental Scientific Research (“973” Program, No. 2011CB111607), by the project of Agriculture Science & Technology Achievement Transformation (No. 2010GB2C400220), by the program of International Science & Technology Cooperation (No. 2012DFA31120), by Agro-scientific Research in the Public Interest (No. 201303094), and by the national “948” project (No. 2011-G25) from the Chinese Ministry of Agriculture.

Author information

Authors and Affiliations

  1. Agricultural Bio-Resource Institute, Fujian Academy of Agricultural Sciences, Fuzhou, 350003, Fujian, People’s Republic of China

    Bo Liu, Guo-Hong Liu, Gui-Ping Hu, Jian-Yang Tang & Ying-Zhi Lin

  2. Fujian Agricultural and Forest University, Fuzhou, 350002, Fujian, People’s Republic of China

    Gui-Ping Hu, Nai-Quan Lin & Wei-Qi Tang

  3. Institut fuer Nutzpflanzenwissenschaften und Ressourcenschutz (INRES), Phytomedizin-Entomologie und Pflanzenschutz, Universitaet Bonn, Nussallee 9, 53115, Bonn, Germany

    Sengonca Cetin

Authors
  1. Bo Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guo-Hong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gui-Ping Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sengonca Cetin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nai-Quan Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jian-Yang Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Wei-Qi Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ying-Zhi Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bo Liu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 548 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, B., Liu, GH., Hu, GP. et al. Bacillus bingmayongensis sp. nov., isolated from the pit soil of Emperor Qin’s Terra-cotta warriors in China. Antonie van Leeuwenhoek 105, 501–510 (2014). https://doi.org/10.1007/s10482-013-0102-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-013-0102-3

Keywords

Search

Navigation