Skip to main content
Log in

Paenibacillus frigoriresistens sp. nov., a novel psychrotroph isolated from a peat bog in Heilongjiang, Northern China

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

Abstract

A novel cold-resistant bacterium, designated YIM 016T, was isolated from a peat bog sample collected from Mohe County, Heilongjiang Province, Northern China and its taxonomic position was investigated using a polyphasic approach. The strain was Gram-positive, aerobic, endospore-forming, motile and rod-shaped. Phylogenetic analyses based on the 16S rRNA gene sequence clearly revealed that strain YIM 016T is a member of the genus Paenibacillus. The strain is closely related to Paenibacillus alginolyticus DSM 5050T, Paenibacillus chondroitinus DSM 5051T and Paenibacillus pocheonensis Gsoil 1138T with similarities of 99.0 %, 97.0 % and 96.3 %, respectively. Meanwhile, the low DNA–DNA relatedness levels between strain YIM 016T and its closely related phylogenetic neighbours demonstrated that this isolate represents a new genomic species in the genus Paenibacillus. Phenotypic and chemotaxonomic tests showed that growth of strain YIM 016T occurred at 4–37 °C, pH 6.0–8.0 and with a NaCl tolerance up to 0.5 % (w/v). The peptidoglycan contained meso-diaminopimelic acid, alanine and glutamic acid. The whole-cell hydrolysates mainly contained glucose, galactose and ribose. The predominant menaquinone was MK-7 and the major fatty acids were anteiso-C15:0 and iso-C16:0. The DNA G+C content of strain YIM 016T was 51.7 mol %. On the basis of phylogenetic, phenotypic and chemotaxonomic characteristics, strain YIM 016T could be clearly distinguished from other species of the genus Paenibacillus. It is therefore concluded that strain YIM 016T represents a novel species in the genus Paenibacillus, for which the name Paenibacillus frigoriresistens sp. nov. is proposed. The type strain is YIM 016T (= CCTCC AB 2011150T = JCM 18141T).

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Baik KS, Choe HN, Park SC, Kim EM, Seong CN (2011) Paenibacillus wooponensis sp. nov., isolated from wetland freshwater. Int J Syst Evol Microbiol 61:2763–2768

    Article  PubMed  CAS  Google Scholar 

  • Barrow GI, Feltham RKA (1993) Cowan and Steel’ manual for the identification of medical bacteria, 3rd edn. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Beneduzi A, Costa PB, Parma M, Melo IS, Bodanese-Zanettini MH, Passaglia LMP (2010) Paenibacillus riograndensis sp. nov., a nitrogen-fixing species isolated from the rhizosphere of Triticum aestivum. Int J Syst Evol Microbiol 60:128–133

    Article  PubMed  CAS  Google Scholar 

  • Buck JD (1982) Nonstaining (KOH) method for determination of Gram reactions of marine bacteria. Appl Environ Microbiol 44:992–993

    PubMed  CAS  Google Scholar 

  • Choi KK, Park CW, Kim SY, Lyoo WS, Lee SH, Lee JW (2004) Polyvinyl alcohol degradation by Microbacterium barkeri KCCM 10507 and Paeniblacillus amylolyticus KCCM 10508 in dyeing wastewater. J Microbiol Biotechnol 14:1009–1013

    CAS  Google Scholar 

  • Christensen H, Angen O, Mutters R, Olsen JE, Bisgaard M (2000) DNA–DNA hybridization determined in micro-wells using covalent attachment of DNA. Int J Syst Evol Microbiol 50:1095–1102

    Article  PubMed  CAS  Google Scholar 

  • Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, Lim YW (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

    Article  PubMed  CAS  Google Scholar 

  • Collins MD, Pirouz T, Goodfellow M, Minnikin DE (1977) Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol 100:221–230

    Article  PubMed  CAS  Google Scholar 

  • De Vos P, Ludwig W, Schleifer KH, Whitman WB (2010) Paenibacillaceae fam. nov. in list of new names and new combinations previously effectively, but not validly, published, validation list no. 132. Int J Syst Evol Microbiol 60:469–472

    Article  Google Scholar 

  • Ezaki T, Hashimoto Y, Yabuuchi E (1989) Fluorometric deoxyribonucleic acid-deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int J Syst Bacteriol 39:224–229

    Article  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–789

    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 

  • Girardin H, Albagnac C, Dargaignaratz C, Nguyen-The C, Carlin F (2002) Antimicrobial activity of foodborne Paenibacillus and Bacillus spp. against Clostridium botulinum. J Food Prot 65:806–813

    PubMed  CAS  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurae algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704

    Article  PubMed  Google Scholar 

  • He L, Li W, Huang Y, Wang LM, Liu ZH, Lanoot BJ, Vancanneyt M, Swings J (2005) Streptomyces jietaisiensis sp. nov., isolated from soil in northern China. Int J Syst Evol Microbiol 55:1939–1944

    Article  PubMed  CAS  Google Scholar 

  • Heyndrickx M, Vandemeulebroecke K, Scheldeman P, Kersters K, De Vos P, Logan NA, Aziz AM, Ali N, Berkeley RCW (1996) A polyphasic reassessment of the genus Paenibacillus, Reclassification of Bacillus lautus (Nakamura 1984) as Paenibacillus lautus comb. nov. and of Bacillus peoriae (Montefusco et al. 1993) as Paenibacillus peoriae comb. nov., and emended descriptions of P. lautus and of P. peoriae. Int J Syst Bacteriol 46:998–1003

    Google Scholar 

  • Hong YY, Ma YC, Zhou YG, Gao F, Liu HC, Chen SF (2009) Paenibacillus sonchi sp. nov., a nitrogen-fixing species isolated from the rhizosphere of Sonchus oleraceus. Int J Syst Evol Microbiol 59:2656–2661

    Article  PubMed  CAS  Google Scholar 

  • Jin HJ, Lv J, Chen SF (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  PubMed  CAS  Google Scholar 

  • Kämpfer P, Falsen E, Lodders N, Martin K, Kassmannhuber J, Busse HJ (2011) Paenibacillus chartarius sp. nov. isolated from a papermill. Int J Syst Evol Microbiol 59:2656–2661

    Google Scholar 

  • Khianngam S, Tanasupawat S, Lee JS, Lee KC, Akaracharanya A (2009) Paenibacillus siamensis sp. nov., Paenibacillus septentrionalis sp. nov. and Paenibacillus montaniterrae sp. nov., xylanase-producing bacteria from Thai soils. Int J Syst Evol Microbiol 59:130–140

    Article  PubMed  CAS  Google Scholar 

  • Khianngam S, Tanasupawat S, Akaracharanya A, Kim KK, Lee KC, Lee JS (2011) Paenibacillus xylanisolvens sp. nov., a xylan-degrading bacterium from soil. Int J Syst Evol Microbiol 61:160–164

    Article  PubMed  CAS  Google Scholar 

  • Kim DS, Bae CY, Jeon JJ, Chun SJ, Oh HW, Hong SG, Baek KS, Moon EY, Bae KS (2004) Paenibacillus elgii sp. nov., with broad antimicrobial activity. Int J Syst Evol Microbiol 54:2031–2035

    Article  PubMed  CAS  Google Scholar 

  • Kim kk, Lee KC, Yu H, Ryoo S, Park Y, Lee JS (2010) Paenibacillus sputi sp. nov., isolated from the sputum of a patient with pulmonary disease. Int J Syst Evol Microbiol 60:2371–2376

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge

    Google Scholar 

  • Kishore KH, Begum Z, Pathan AAK, Shivaji S (2010) Paenibacillus glacialis sp. nov., isolated from the Kafni glacier of the himalayas,India. Int J Syst Evol Microbiol 60:1909–1913

    Article  PubMed  CAS  Google Scholar 

  • Konishi J, Maruhashi K (2003) 2-(2’-Hydroxyphenyl)benzene sulfinate desulfinase from the thermophilic desulfurizing bacterium Paenibacillus sp. strain A11-2: purification and characterization. Appl Microbiol Biotechnol 62:356–361

    Article  PubMed  CAS  Google Scholar 

  • Kovacs N (1956) Identification of Pseudomonas pyocyanea by the Oxidase Reaction. Nature 178:703

    Google Scholar 

  • Lal S, Tabacchioni S (2009) Ecology and biotechnological potential of Paenibacillus polymyxa: a minireview. Indian J. Microbiol 49:2–10

    Article  CAS  Google Scholar 

  • Leifson E (1960) Atlas of bacterial flagellation. Academic Press, London

    Google Scholar 

  • Li WJ, Xu P, Schumann P, Zhang YQ, Pukall R, Xu LH, Stackebrandt E, Jiang CL (2007) Georgenia ruanii sp. nov., a novel actinobacterium isolated from forest soil in Yunnan (China) and emended description of the genus Georgenia. Int J Syst Evol Microbiol 57:1424–1428

    Article  PubMed  Google Scholar 

  • MacFaddin JF (1980) Biochemical tests for identificat bacteria, 2nd edn. Williams & Wilkins, Baltimore

    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 

  • Minnikin DE, Collins MD, Goodfellow M (1979) Fatty acid and polar lipid composition in the classification of Cellulomonas, Oerskovia and related taxa. J Appl Bacteriol 47:87–95

    Article  CAS  Google Scholar 

  • Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett JH (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241

    Article  CAS  Google Scholar 

  • Moon JC, Jung YJ, Jung JH, Jung HS, Cheong YR, Jeon CO, Lee KO, Lee SY (2011) Paenibacillus sacheonensis sp. nov., a xylanolytic and cellulolytic bacterium isolated from tidal flat sediment. Int J Syst Evol Microbiol 61:2753–2757

    Article  PubMed  CAS  Google Scholar 

  • Moore DD, Dowhan D (1995) Preparation and analysis of DNA. In: Ausubel F M, Brent R, Kingston R E, Moore D D, Seidman J G, Smith J A, Struhl K (ed) Current protocols in molecular biology. Wiley, New York, p 2–11

  • Nie GX, Ming H, Li S, Zhou EM, Cheng J, Tang X, Feng HG, Tang SK, Li WJ (2012) Amycolatopsis dongchuanensis sp. nov., a novel actinobacterium isolated from dry-hot valley in Yunnan, south-west China. Int J Syst Evol Microbiol. doi:10.1099/ijs.0.038125-0

    Google Scholar 

  • Nielsen P, Sorensen J (1997) Multi-target and medium-independent fungal antagonism by hydrolytic enzymes in Paenibacillus polymyxa and Bacillus pumilus strains from barley rhizosphere. FEMS Microbiol Ecol 22:183–192

    Article  CAS  Google Scholar 

  • Park MJ, Kim HB, An DS, Yang HC, Oh ST, Chung HJ, Yang DC (2007) Paenibacillus soli sp. nov., a xylanolytic bacterium isolated from soil. Int J Syst Evol Microbiol 57:146–150

    Article  PubMed  CAS  Google Scholar 

  • Park DS, Jeong WJ, Lee KH, Oh HW, Kim BC, Bae KS, Park HY (2009) Paenibacillus pectinilyticus sp. nov., isolated from the gut of Diestrammena apicalis. Int J Syst Evol Microbiol 59:1342–1347

    Article  PubMed  CAS  Google Scholar 

  • Roux V, Fenner L, Raoult D (2008) Paenibacillus provencensis sp. nov., isolated from human cerebrospinal fluid, and Paenibacillus urinalis sp. nov., isolated from human urine. Int J Syst Evol Microbiol 58:682–687

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newsl 20:16

    Google Scholar 

  • Scheldeman P, Goossens K, Rodriguez-Diaz M, Pil A, Goris J, Herman L, De Vos P, Logan NA, Heyndrickx M (2005) Paenibacillus lactis sp. nov., isolated from raw and heat-treated milk. Int J Syst Bacteriol 54:885–891

    Google Scholar 

  • Schleifer KH (1985) Analysis of the chemical composition and primary structure of murein. Methods Microbiol 18:123–156

    Article  CAS  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  PubMed  CAS  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, D.C., pp 607–654

    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 

  • Takeda M, Suzuki L, Koizumi JI (2005) Paenibacillus hodogayensis sp. nov., capable of degrading the polysaccharide produced by Sphaerotilus natans. Int J Syst Evol Microbiol 55:737–741

    Article  PubMed  CAS  Google Scholar 

  • Tamaoka J, Katayama-Fujimura Y, Kuraishi H (1983) Analysis of bacterial menaqui-none mixtures by high performance liquid chromatography. J Appl Bacteriol 300:31–36

    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 28:2731–2739

    Article  PubMed  CAS  Google Scholar 

  • Tang SK, Wang Y, Chen Y, Lou K, Cao LL, Xu LH, Li WJ (2009) Zhihengliuella alba sp. nov., and emended description of the genus Zhihengliuella. Int J Syst Evol Microbiol 59:2025–2032

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Traiwan J, Park MH, Kim W (2011) Paenibacillus puldeungensis sp. nov., isolated from a grassy sandbank. Int J Syst Evol Microbiol 61:670–673

    Article  PubMed  CAS  Google Scholar 

  • Von Der Weid I, Alviano DS, Santos AL, Soares RM, Alviano CS, Seldin L (2003) Antimicrobial activity of Paenibacillus peoriae strain NRRL BD-62 against a broad spectrum of phytopathogenic bacteria and fungi. J Appl Microbiol 95:1143–1151

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Prof. Dr. Hans-Peter Klenk (DSMZ) for his kind providing reference type strains and Prof. Jean Euzéby for the Latin construction of the species name. This research was supported by Science and Technology Innovation Talents Program in Universities of Henan Province of China (HASTIT, No. 2010HASTIT020), Key Technologies R & D Program of Henan Province of China (112102310335,112102210106), and Doctoral Fund of Ministry of Education of China (20100022120009). W-J. Li was also supported by ‘Hundred Talents Program’ of the Chinese Academy of Sciences.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Hong-Chen Jiang or Wen-Jun Li.

Additional information

Hong Ming and Guo-Xing Nie contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 457 kb)

Supplementary material 2 (PPT 797 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ming, H., Nie, GX., Jiang, HC. et al. Paenibacillus frigoriresistens sp. nov., a novel psychrotroph isolated from a peat bog in Heilongjiang, Northern China. Antonie van Leeuwenhoek 102, 297–305 (2012). https://doi.org/10.1007/s10482-012-9738-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-012-9738-7

Keywords

Navigation