Skip to main content
Log in

Paenibacillus aquistagni sp. nov., isolated from an artificial lake accumulating industrial wastewater

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

Abstract

Strain 11T was isolated from water of an artificial lake accumulating industrial wastewater on the outskirts of Celje, Slovenia. Phenotypic characterisation showed strain 11T to be a Gram-stain positive, spore forming bacterium. The 16S rRNA gene sequence identified strain 11T as a member of the genus Paenibacillus, closely related to Paenibacillus alvei (96.2%). Genomic similarity with P. alvei 29T was 73.1% (gANI), 70.2% (ANIb), 86.7% (ANIm) and 21.7 ± 2.3% (GGDC). The DNA G+C content of strain 11T was determined to be 47.5%. The predominant menaquinone of strain 11T was identified as MK-7 and the major fatty acid as anteiso-C15:0. The peptidoglycan was found to contain meso-diaminopimelic acid. In contrast to its close relatives P. alvei DSM 29T, Paenibacillus apiarius DSM 5581T and Paenibacillus profundus NRIC 0885T, strain 11T was found to be able to ferment d-fructose, d-mannose and d-xylose. A draft genome of strain 11T contains a cluster of genes associated with type IV pilin synthesis usually found in clostridia, and only sporadically in other Gram-positive bacteria. Genotypic, chemotaxonomic, physiological and biochemical characteristics of strain 11T presented in this study support the creation of a novel species within the genus Paenibacillus, for which the name Paenibacillus aquistagni sp. nov. is proposed, with strain 11T (=ZIM B1027T =LMG 29561T =CCM 8679T ) as the type strain.

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

  • Alexander SK, Strete D (2001) Microbiology: a photographic atlas for the laboratory. Benjamin Cummings, San Francisco

    Google Scholar 

  • Ash C, Priest FG, Collins MD (1993) Molecular identification of rRNA group 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  Google Scholar 

  • Auch AF, von Jan M, Klenk HP, Göker M (2010) Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genom Sci 2:117–134

    Article  Google Scholar 

  • Ayers M, Sampaleanu LM, Tammam S, Koo J, Harvey H, Howell PL, Burrows LL (2009) PilM/N/O/P proteins form an inner membrane complex that affects the stability of the Pseudomonas aeruginosa type IV pilus secretin. J Mol Biol 394:128–142

    Article  CAS  PubMed  Google Scholar 

  • Bankevich A et al (2012) SPAdes: a new genome assembly algorithm and its applications to single–cell sequencing. J Comput Biol 19:455–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boesch C, Trček J, Sievers M, Teuber M (1998) Acetobacter intermedius, sp. nov. Syst Appl Microbiol 21:220–229

    Article  CAS  PubMed  Google Scholar 

  • Borriello SP, Davies HA, Kamiya S, Reed PJ, Seddon S (1990) Virulence factors of Clostridium difficile. Rev Infect Dis 12(Suppl 2):S185–S191

    Article  CAS  PubMed  Google Scholar 

  • Bushnell B (2014) BBTools software package. http://sourceforge.net/projects/bbmap

  • Chen IM, Markowitz VM, Palaniappan K, Szeto E, Chu K, Huang J, Ratner A, Pillay M, Hadjithomas M, Huntemann M, Mikhailova N, Ovchinnikova G, Ivanova NN, Kyrpides NC (2016) Supporting Community annotation and user collaboration in the Integrated Microbial Genomes (IMG) system. BMC Genom 17:307

    Article  Google Scholar 

  • Chen IA, Markowitz VM, Chu K, Palaniappan K, Szeto E, Pillay M, Ratner A, Huang J, Andersen E, Huntemann M, Varghese N, Hadjithomas M, Tennessen K, Nielsen T, Ivanova NN, Kyrpides NC (2017) IMG/M: integrated genome and metagenome comparative data analysis system. Nucleic Acids Res 45(D1):D507–D516

    Article  PubMed  Google Scholar 

  • Craig L, Pique ME, Tainer JA (2004) Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2:363–378

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (2002) PHYLIP (Phylogeny Inference Package) version 3.6. Department of Genetics, University of Washington, Seattle

    Google Scholar 

  • Fives-Taylor PM, Thompson DW (1985) Surface properties of Streptococcus sanguis FW213 mutants nonadherent to saliva-coated hydroxyapatite. Infect Immun 47:752–759

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gerhardt P, Murray RGE, Wood WA (1994) Methods for general and molecular bacteriology. American Society for Microbiology, Washington

    Google Scholar 

  • Han TY, Tong XM, Wang YW, Wang HM, Chen XR, Kong DL, Guo X, Ruan ZY (2015) Paenibacillus populi sp. nov., a novel bacterium isolated from the rhizosphere of Populus alba. Antonie Van Leeuwenhoek 108:659–666

    Article  CAS  PubMed  Google Scholar 

  • Huntemann M, Ivanova NN, Mavromatis K et al (2015) The standard operating procedure of the DOE-JGI Microbial genome annotation pipeline (MGAP v4). Stand Genomic Sci 10:86

    Article  PubMed  PubMed Central  Google Scholar 

  • Imam S, Chen Z, Roos DS, Pohlschröder M (2011) Identification of surprisingly diverse type IV Pili, across a broad range of gram-positive bacteria. PLoS ONE 6(12):e28919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim KK, Lee KC, Yu H, Ryoo S, Park Y, Lee JS (2010) Int J Syst Evol Microbiol 60:2371–2376

    Article  CAS  PubMed  Google Scholar 

  • Lee FL, Kuo HP, Tai CJ, Yokota A, Lo CC (2007) Paenibacillus taiwanensis sp. nov., isolated from soil in Taiwan. Int J Syst Evol Microbiol 57:1351–1354

    Article  CAS  PubMed  Google Scholar 

  • Ludwig W, Schleifer KH, Whitman WB (2009) Family IV. Paenibacillaceae fam. nov. In: De Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W, Rainey F, Schleifer KH, Whitman WB (eds) Bergey´s manual of systematic bacteriology, vol 3, 2nd edn. Springer, New York, p 269

    Google Scholar 

  • Mah JH, Chang YH, Hwang HJ (2008) Paenibacillus tyraminigenes sp. nov. isolated from Myeolchi-jeotgal, a traditional Korean salted and fermented anchovy. Int J Food Microbiol 127:209–214

    Article  CAS  PubMed  Google Scholar 

  • Meier-Kolthoff JO, Alexander AF, Hans-Peter K, Markus K (2013) Genome sequence-based specie delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:60

    Article  Google Scholar 

  • Melville S, Craig L (2013) Type IV Pili in gram-positive bacteria. Microbiol Mol Biol Rev 77(3):323–341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura LK (1996) Paenibacillus apiarius sp. nov. Int J Syst Bacteriol 46:688–693

    Article  CAS  PubMed  Google Scholar 

  • Page RDM (2000) TreeView version 1.6.6. http://taxonomy.zoology.gla.ac.uk/rod/treeview.html. Accessed 20 Jan 2005.

  • Pati A, Ivanova NN, Mikhailova N, Ovchinnikova G, Hooper SD, Lykidis A, Kyrpides NC (2010) GenePRIMP: a GENE PRediction IMprovement Pipeline for Prokaryotic genomes. Nat Methods 7(6):455–457

    Article  CAS  PubMed  Google Scholar 

  • Priest FG (2015) Paenibacillus. Bergey’s manual of systematics of archaea and bacteria. Wiley, Hoboken, pp 1–40

    Book  Google Scholar 

  • Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131

    Article  CAS  PubMed  PubMed Central  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 

  • Rosselló-Móra R, Trujillo ME, Sutcliffe IC (2017) Introducing a digital protologue: a timely move towards a database-driven systematics of archaea and bacteria. Antonie Van Leeuwenhoek 110:455–456

    Article  PubMed  Google Scholar 

  • Roux V, Raoult D (2004) Paenibacillus massiliensis sp. nov., Paenibacillus sanguinis sp. nov. and Paenibacillus timonensis sp. nov., isolated from blood cultures. Int J Syst Evol Microbiol 54:1049–1054

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Saha P, Mondal AK, Mayilraj S, Krishnamurthi S, Bhattacharya A, Chakrabarti T (2005) Paenibacillus assamensis sp. nov., a novel bacterium isolated from a warm spring in Assam. India. Int J Syst Evol Microbiol 55:2577–2581

    Article  CAS  PubMed  Google Scholar 

  • Schumann P (2011) Peptidoglycan structure. In: Rainey FA, Oren A (eds) Taxonomy of prokaryotes. Academic Press, Chennai, pp 102–129

    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 

  • Sitdhipol J, Paek J, Sin Y, Park IS, Thamacharoensuk T, Wannissorn B, Tanasupawat S, Chang YH (2016) Paenibacillus cathormii sp. nov., isolated from tree bark. Int J Syst Evol Microbiol 66:1187–1192

    Article  CAS  Google Scholar 

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

    Google Scholar 

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

    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 

  • Trček J, Raspor P, Teuber M (2000) Molecular identification of Acetobacter isolates from submerged vinegar production, sequence analysis of plasmid pJK2-1 and application in development of a cloning vector. Appl Microbiol Biotechnol 53:289–295

    Article  PubMed  Google Scholar 

  • Varghese N, Mukherjee S, Ivanova NN, Konstantidinis K, Mavrommatis K, Kyrpides NC, Pati A (2015) Microbial species delineation using whole genome sequences. Nucleic Acids Res 43(14):6761–6771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whitman WB, Woyke T, Klenk HP, Zhou Y, Lilburn TG, Beck BJ, De Vos P, Vandamme P, Eisen JA, Garrity G, Hugenholtz P, Kyrpides NC (2015) Genomic encyclopedia of bacterial and archaeal type strains, phase III: the genomes of soil and plant-associated and newly described type strains. Stand Genom Sci 10:26

    Article  Google Scholar 

Download references

Acknowledgements

This research was partially funded by the Slovenian Research Agency through programme P2-0006. The genome sequencing was conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, and supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. The work performed by the BCCM/LMG Bacteria Collection was supported by the Federal Public Planning Service—Science Policy, Belgium. Stefanie Van Trappen from the BCCM/LMG Bacteria Collection is acknowledged for the FAME analysis of Paenibacillus aquistagni 11T. Analysis of respiratory quinones were carried out by the Identification Service and Dr. Brian Tindall from DSMZ.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Janja Trček.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Simon, L., Škraban, J., Kyrpides, N.C. et al. Paenibacillus aquistagni sp. nov., isolated from an artificial lake accumulating industrial wastewater. Antonie van Leeuwenhoek 110, 1189–1197 (2017). https://doi.org/10.1007/s10482-017-0891-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-017-0891-x

Keywords

Navigation