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Isolation of Paenibacillus tumbae sp. nov., from the tomb of the emperor Yang of the Sui dynasty, and emended description of the genus Paenibacillus

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Abstract

A novel strain, designated strain CSA42T, was isolated from the tomb of emperor Yang of Sui in Yangzhou, Jiangsu province, China. Strain CSA42T was observed to be Gram-stain positive, strictly aerobic, rod-shaped, spore-forming and motile. The optimum conditions for growth were found to be 30 °C, pH 8.0 and without NaCl. Phylogenetic analysis, based on 16S rRNA gene sequences, revealed strain CSA42T to be closely related to Paenibacillus larvae DSM 7030T (94.7%), Paenibacillus doosanensis CAU 1055T (94.4%) and Paenibacillus gansuensis B518T (94.2%). The major cellular fatty acids were identified as anteiso-C15:0, anteiso-C17:0 and iso-C16:0. MK-8 was found to be the only respiratory quinone. The polar lipids were found to be comprised of diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylglycerol and two aminophospholipids. The cell wall peptidoglycan was found to contain meso-diaminopimelic acid and ribose as the only whole cell sugar. The genomic G+C content of strain CSA42T was determined to be 47.6 mol%. The low DNA–DNA relatedness values between strain CSA42T and the reference strain P. larvae KACC 11540T and many phenotypic properties support the classification of strain CSA42T (=KACC 18941T =CCTCC AB 2016201T) as the type strain of a novel species of the genus Paenibacillus, for which the name Paenibacillus tumbae sp. nov. is proposed. An emended description of the genus Paenibacillus based on the new data is also given.

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References

  • Achouak W, Normand P, Heulin T (1999) Comparative phylogeny of rrs and nifH genes in the Bacillaceae. Int J Syst Bacteriol 49:961–967

    Article  CAS  PubMed  Google Scholar 

  • Ash C, Priest FG, Collins MD (1993) Molecular identification of rRNA group 3 bacilli (Ash, Farrow, Wallbanks and Collins) using a PCR probe test. Proposal for the creation of a new genus Paenibacillus. Antonie Van Leeuwenhoek 64:253–260

    Article  CAS  PubMed  Google Scholar 

  • Ash C, Priest FG, Collins MD (1994) Paenibacillus gen. nov. In Validation of the publication of new names and new combinations previously effectively published outside the IJSB. List no. 51. Int J Syst Bacteriol 44:852

    Article  Google Scholar 

  • Berge O, Guinebretiere MH, Achouak W, Normand P, Heulin T (2002) Paenibacillus graminis sp. nov. and Paenibacullus odorifer sp. nov., isolated from plant roots, soil and food. Int J Syst Evol Microbiol 52:607–616

    Article  CAS  PubMed  Google Scholar 

  • Cao Y, Chen F, Li Y, Wei S, Wang G (2015) Paenibacillus ferrarius sp. nov., isolated from iron mineral soil. Int J Syst Evol Microbiol 65:165–170

    Article  CAS  PubMed  Google Scholar 

  • Chung YR, Kim CH, Hwang I, Chun J (2000) Paenibacillus koreensis sp. nov., a new species that produces an iturin-like antifungal compound. Int J Syst Evol Microbiol 50:1495–1500

    Article  CAS  PubMed  Google Scholar 

  • Collins MD (1985) Isoprenoid quinone analysis in classification and identification. In: Goodfellow M, Minnikin DE (eds) Chemical methods in bacterial systematics. Academic Press, London, pp 267–287

    Google Scholar 

  • De Ley J, Cattoir H, Reynaerts 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. Evolution 39:783–791

    Article  Google Scholar 

  • Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416

    Article  Google Scholar 

  • Gordon RE, Barnett DA, Handerhan JE, Pang CH-N (1974) Nocardia coeliaca, Nocardia autotrophica, and the nocardin strain. Int J Syst Bacteriol 24:54–63

    Article  Google Scholar 

  • Guo GN, Zhou X, Chen ZL, Yang ZW, Li XD, Li YH (2016a) Paenibacillus marchantiophytorum sp. nov., isolated from the liverwort Herbertus sendtneri. Int J Syst Evol Microbiol 66:755–761

    Article  CAS  Google Scholar 

  • Guo X, Zhou S, Wang Y-W, Wang H-M, Kong D-L, Zhu J, Dong W-W, He M-X, Zhao B-Q, Hu G-Q, Ruan Z-Y (2016b) Paenibacillus salinicaeni sp. nov., isolated from saline silt sample. Antonie Van Leeuwenhoek 109:721–728

    Article  CAS  PubMed  Google Scholar 

  • Huang Z, Dai W, Zhou Z, Wang G, Lin G, Yan X, Zhao F (2016) Paenibacillus terreus sp. nov., isolated from forest soil. Int J Syst Evol Microbiol 66:243–247

    Article  CAS  PubMed  Google Scholar 

  • Jin H-J, Lv J, Chen S-F (2011) Paenibacillus sophorae sp. nov., a nitrogen-fixing species isolated from the rhizosphere of Sophora japonica. Int J Syst Evol Microbiol 61:767–771

    Article  CAS  PubMed  Google Scholar 

  • Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, 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 

  • Kim J-H, Kang H, Kim W (2014a) Paenibacillus doosanensis sp. nov., isolated from soil. Int J Syst Evol Microbiol 64:1271–1277

    Article  CAS  PubMed  Google Scholar 

  • Kim M, Oh HS, Park SC, Chun J (2014b) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–351

    Article  CAS  PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Kämpfer P, Falsen E, Lodders N, Martin K, Kassmannhuber J, Busse H-J (2012) Paenibacillus chartarius sp. nov., isolated from a paper mill. Int J Syst Evol Microbiol 62:1342–1347

    Article  PubMed  Google Scholar 

  • Lee SD (2016) Paenibacillus cavernae sp. nov., isolated from soil of a natural cave. Int J Syst Evol Microbiol 66:598–603

    Article  CAS  Google Scholar 

  • Lee JC, Kim CJ, Yoon KH (2011) Paenibacillus telluris sp. nov., a novel phosphate-solubilizing bacterium isolated from soil. J Microbiol 49:617–621

    Article  PubMed  Google Scholar 

  • Lee HW, Roh SW, Yim KJ, Shin NR, Lee J, Whon TW, Kim JY, Hyun DW, Kim D, Bae JW (2013) Paenibacillus marinisediminis sp. nov., a bacterium isolated from marine sediment. J Microbiol 51:312–317

    Article  CAS  PubMed  Google Scholar 

  • Li J, Lu Q, Liu T, Zhou S, Yang G, Zhao Y (2014) Paenibacillus guangzhouensis sp. nov., an Fe(III)- and humus-reducing bacterium from a forest soil. Int J Syst Evol Microbiol 64:3891–3896

    Article  PubMed  Google Scholar 

  • Lim J-M, Jeon CO, Lee J-C, Xu L-H, Jiang C-L, Kim C-J (2006) Paenibacillus gansuensis sp. nov., isolated from desert soil of Gansu province in China. Int J Syst Evol Microbiol 56:2131–2134

    Article  CAS  PubMed  Google Scholar 

  • Logan NA, Berge O, Bishop AH, Busse H-J, De Vos P, Fritze D, Heyndrickx M, Kämpfer P, Rabinovitch L, Salkinoja-Salonen MS, Seldin L, Ventosa A (2009) Proposed minimal standards for describing new taxa of aerobic, endospore-forming bacteria. Int J Syst Evol Microbiol 59:2114–2121

    Article  CAS  PubMed  Google Scholar 

  • Ma Y-C, Chen S-F (2008) Paenibacillus forsythia sp. nov., a nitrogen-fixing species isolated from rhizosphere soil of Forsythia mira. Int J Syst Evol Microbiol 58:319–323

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Zhang J, Chen S (2007) Paenibacillus zanthoxyli sp. nov., a novel nitrogen-fixing species isolated from the rhizosphere of Zanthoxylum simulans. Int J Syst Evol Microbiol 57:873–877

    Article  CAS  PubMed  Google Scholar 

  • Mesbah M, Premachandran U, Whitman WB (1989) Precise measurement of the G+C content of deoxyribonucleic acid by high performance liquid chromatography. Int J Syst Bacteriol 39:159–167

    Article  CAS  Google Scholar 

  • Mishra AK, Lagier J-C, Rivet R, Raoult D, Fournier P-E (2012) Non-contiguous finished genome sequence and description of Paenibacillus senegalensis sp. nov. Stand Genomic Sci 7:70–81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moon J, Kim J (2014) Isolation of Paenibacillus pinesoli sp. nov. from forest soil in Gyeonggi-Do, Korea. J Microbiol 52:273–277

    Article  CAS  PubMed  Google Scholar 

  • Rameshkumar N, Lang E, Tanaka N (2016) Description of Vogesella oryzae sp. nov., isolated from the rhizosphere of saline tolerant pokkali rice. Syst Appl Microbiol 39:20–24

    Article  CAS  PubMed  Google Scholar 

  • Rhuland LE, Work E, Denman RF, Hoare DS (1955) The behavior of the isomers of α, ε-diaminopimelic acid on paper chromatograms. J Am Chen Soc 77:4844–4846

    Article  CAS  Google Scholar 

  • Romanenko LA, Tanaka N, Svetashev VI, Kalinovskaya NI (2013) Paenibacillus profundus sp. nov., a deep sediment bacterium that produces isocoumarin and peptide antibiotics. Arch Microbiol 195:247–254

    Article  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 

  • Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. MIDI technical note 101. MIDI Inc, Newark

  • Shen P, Fan XR, Li GW (1999) Experiment of microbiology. Higher Education Press, Beijing

    Google Scholar 

  • Shida O, Takagi H, Kadowaki K, Nakamura LK, Komagata K (1997) Transfer of Bacillus alginolyticus, Bacillus chondroitinus, Bacillus curdlanolyticus, Bacillus glucanolyticus, Bacillus kobensis, and Bacillus thiaminolyticus to the genus Paenibacillus and emended description of the genus Paenibacillus. Int J Syst Bacteriol 47:289–298

    Article  CAS  PubMed  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 

  • Sukweenadhi J, Kim Y-J, Lee KJ, Koh S-C, Hoang V-A, Nguyen N-L, Yang D-C (2014) Paenibacillus yonginensis sp. nov., a potential plant growth promoting bacterium isolated from humus soil of Yongin forest. Antonie Van Leeuwenhoek 106:935–945

    Article  CAS  PubMed  Google Scholar 

  • Švec P, Vancanneyt M, Seman M, Snauwaert C, Lefebvre K, Sedláček I, Swings J (2005) Evaluation of (GTG)5-PCR for identification of Enterococcus spp. FEMS Microbiol Lett 247:59–63

    Article  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA 6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tindall BJ (1990a) A comparative study of the lipid composition of Halobacterium saccharovorum from various sources. Syst Appl Microbiol 13:128–130

    Article  CAS  Google Scholar 

  • Tindall BJ (1990b) Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol Lett 66:199–202

    Article  CAS  Google Scholar 

  • Van der Maarel MJEC, Veen A, Wijbenga DJ (2000) Paenibacillus granivorans sp. nov., a new Paenibacillus species which degrades native potato starch granules. Syst Appl Microbiol 23:344–348

    Article  PubMed  Google Scholar 

  • Wang L, Baek SH, Cui Y, Lee HG, Lee ST (2012) Paenibacillus sediminis sp. nov., a xylanolytic bacterium isolated from a tidal flat. Int J Syst Evol Microbiol 62:1284–1288

    Article  CAS  PubMed  Google Scholar 

  • Wang LY, Li J, Li QX, Chen SF (2013) Paenibacillus beijingensis sp. nov., a nitrogen-fixing species isolated from wheat rhizosphere soil. Antonie Van Leeuwenhoek 104:675–683

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Xiang W, Wang G, Wang Y, Yao R, Zhang F, Wang R, Wang D, Zheng S (2014) Paenibacillus selenii sp. nov., isolated from selenium mineral soil. Int J Syst Evol Microbiol 64:2662–2667

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Gao S, Wei D-Q, Yang L-L, Huang X, He J, Zhang Y-J, Tang S-K, Li W-J (2012) Paenibacillus thermophiles sp. nov., a novel bacterium isolated from a sediment of hot spring in Fujian Province, China. Antonie Van Leeuwenhoek 102:601–609

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Dr Soon-Wo Kwon, Korean Agricultural Culture Collection (KACC), for kindly providing strain Paenibacillus larvae KACC 11540T. The authors also thank the editor and reviewers for giving many suggestions to improve this manuscript. This work was supported by National Nature Science Foundation of China (41201251, 41101229 and 51478103).

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Correspondence to Fei Zhao or Yong-Hui Li.

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Huang, Z., Zhao, F. & Li, YH. Isolation of Paenibacillus tumbae sp. nov., from the tomb of the emperor Yang of the Sui dynasty, and emended description of the genus Paenibacillus . Antonie van Leeuwenhoek 110, 357–364 (2017). https://doi.org/10.1007/s10482-016-0807-1

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