Skip to main content
Log in

Paenibacillus piscarius sp. nov., a novel nitrogen-fixing species isolated from the gut of the armored catfish Parotocinclus maculicauda

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

Abstract

A Gram-positive, nitrogen-fixing and endospore-forming strain, designated P121T, was isolated from the gut of the armored catfish (Parotocinclus maculicauda) and identified as a member of the genus Paenibacillus based on the sequences of the 16S rRNA encoding gene, rpoB, gyrB and nifH genes and phenotypic analyses. The most closely related species to strain P121T were Paenibacillus rhizoplanae DSM 103993T, Paenibacillus silagei DSM 101953T and Paenibacillus borealis DSM 13188T, with similarity values of 98.9, 98.3 and 97.6%, respectively, based on 16S rRNA gene sequences. Genome sequencing revealed a genome size of 7,513,698 bp, DNA G + C content of 53.9 mol% and the presence of the structural nitrogenase encoding genes (nifK, nifD and nifH) and of other nif genes necessary for nitrogen fixation. Digital DNA-DNA hybridization (dDDH) experiments and average nucleotide identity (ANI) analyses between strain P121T and the type strains of the closest species demonstrated that the highest values were below the thresholds of 70% dDDH (42.3% with P. borealis) and 95% ANI (84.28% with P. silagei) for bacterial species delineation, indicating that strain P121T represents a distinct species. Its major cellular fatty acid was anteiso-C15:0 (42.4%), and the major isoprenoid quinone was MK-7. Based on physiological, genomic, biochemical and chemotaxonomic characteristics, we propose that strain P121T represents a novel species for which the name Paenibacillus piscarius sp. nov. is proposed (type strain = DSM 25072 = LFB-Fiocruz 1636).

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alikhan NF, Petty NK, Zakour NLB, Beatson SA (2011) BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genom 12:402

    CAS  Google Scholar 

  • Andrews S (2010) FastQC: a quality control tool for high throughput sequence data [Online]. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/

  • Ash C, Farrow JAE, Wallbanks S, Collins MD (1991) Phylogenetic heterogeneity of the genus Bacillus revealed by comparative analysis of small subunit-ribosomal RNA sequences. Lett Appl Microbiol 13:202–206

    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

    CAS  PubMed  Google Scholar 

  • Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al (2008) The RAST Server: Rapid Annotations using Subsystems Technology. BMC Genom 9:75

    Google Scholar 

  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    CAS  PubMed  PubMed Central  Google Scholar 

  • Blin K, Shaw S, Steinke K, Villebro R, Ziemert N, Lee SY, Medema MH, Weber T (2019) antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucl Acids Res 47:81–87

    Google Scholar 

  • Castro ALM, Vollú RE, Peixoto RS, Grigorevski-Lima AL, Coelho RRR, Bon EPS, Rosado AS, Seldin L (2011) Cellulolytic potential of a novel strain of Paenibacillus sp. isolated from the armored catfish Parotocinclus maculicauda gut. Braz J Microbiol 42(4):1608–1615

    PubMed  PubMed Central  Google Scholar 

  • Elo S, Suominen I, Kämpfer P, Juhanoja J, Salkinoja-Salonen M, Haahtela K (2001) Paenibacillus borealis sp. nov., a nitrogen-fixing species isolated from spruce forest humus in Finland. Int J Syst Evol Microbiol 51:535–545

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Fu L, Niu B, Zhu Z, Wu S, Li W (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28:3150–3152

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garavello JC (1977) Systematics and geographical distribution of the genus Parotocinclus, Eigenmann & Eigenmann, 1889 (Ostariophysi, Loricariidae). Arq Zool S Paulo 28:1–37

    Google Scholar 

  • Gordon R E, Haynes WC, Pang H-N (1973) The genus Bacillus. Agriculture Handbook 427, Agricultural Research Service, U.S. Department of Agriculture, Washington, D.C.

  • 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

    CAS  PubMed  Google Scholar 

  • Grady EN, MacDonald J, Liu L, Richman A, Yuan Z-C (2016) Current knowledge and perspectives of Paenibacillus: a review. Microb Cell Fact 15(1):203

    PubMed  PubMed Central  Google Scholar 

  • Hansen GH, Olafsen JA (1999) Bacterial interactions in early life stages of marine cold water fish. Microb Ecol 38:1–26

    CAS  PubMed  Google Scholar 

  • Hao T, Chen S (2017) Colonization of wheat, maize and cucumber by Paenibacillus polymyxa WLY78. PLoS ONE 12(1):e0169980

    PubMed  PubMed Central  Google Scholar 

  • Hernandez D, François P, Farinelli L, Osterås M, Schrenzel J (2008) De novo bacterial genome sequencing: millions of very short reads assembled on a desktop computer. Genome Res 18(5):802–809

    CAS  PubMed  PubMed Central  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

    CAS  PubMed  Google Scholar 

  • Jeong H, Choi S-K, Ryu C-M, Seung-Hwan Park S-H (2019) Chronicle of a soil bacterium: Paenibacillus polymyxa E681 as a tiny guardian of plant and human health. Front Microbiol 10:467

    PubMed  PubMed Central  Google Scholar 

  • Kampfer P, Busse H-J, McInroy JA, Hu C-H, Kloepper JW, Glaeser SP (2017) Paenibacillus rhizoplanae sp. nov. isolated from the rhizosphere of Zea mays. Int J Syst Evol Microbiol 67:1058–1063

    PubMed  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Li Q, Li Y, Gao J, Fan X (2016) Draft genome sequence of Paenibacillus polymyxa KF-1, an excellent producer of microbicides. Genome Announc 4(4):e00727-e816

    PubMed  PubMed Central  Google Scholar 

  • Li Q, Li Y, Liu X, Chen S (2021) Paenibacillus sinensis sp. nov., a nitrogen-fixing species isolated from plant rhizospheres. Antonie Van Leeuwenhoek. https://doi.org/10.1007/s10482-021-01677-6

    Article  PubMed  PubMed Central  Google Scholar 

  • Lindgreen (2012) AdapterRemoval: easy cleaning of next-generation sequencing reads. BMC Res Notes 5:337

    PubMed  PubMed Central  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

    CAS  PubMed  Google Scholar 

  • Ma Y, Xia Z, Liu X, Chen S (2007a) Paenibacillus sabinae sp. nov., a nitrogen-fixing species isolated from the rhizosphere soils of shrubs. Int J Syst Evol Microbiol 57:6–11

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Maksimov MO, Pan SJ, James Link AJ (2012) Lasso peptides: structure, function, biosynthesis, and engineering. Nat Prod Rep 29:996–1006

    CAS  PubMed  Google Scholar 

  • Massol-Deya AA, Odelson DA, Hichey RP, Tiedje JM (1995). Bacterial community fingerprinting of amplified 16S and 16–23S ribosomal DNA gene sequences and restriction endonuclease analysis (ARDRA). In: Akkermans ADL, van Elsas JD, de Bruijn FJ (eds) Molecular Microbial Ecology Manual, Kluwer Academic Publishers, Netherlands, pp. 3.3.2: 1–8

  • Meier-Kolthoff JP, Auch AF, Klenk HP, Goker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60

    PubMed  PubMed Central  Google Scholar 

  • Melsted P, Halldórsson BV (2014) KmerStream: streaming algorithms for k-mer abundance estimation. Bioinformatics 30:3541–3547

    CAS  PubMed  Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA, pp 1–8

  • Nivina A, Yuet KP, Hsu J, Khosla C (2019) Evolution and diversity of assembly line polyketide synthases. Chem Rev 119:12524–12547

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pajor M, Sogin J, Worobo R, Szweda P (2020) Draft genome sequence of antimicrobial producing Paenibacillus alvei strain MP1 reveals putative novel antimicrobials. BMC Res Notes 13:280

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qi SS, Cnockaert M, Carlier A, Vandamme PA (2021) Paenibacillus foliorum sp. nov., Paenibacillus phytohabitans sp. nov., Paenibacillus plantarum sp. nov., Paenibacillus planticolens sp. nov., Paenibacillus phytorum sp. nov., and Paenibacillus germinis sp. nov., isolated from the Arabidopsis thaliana phyllosphere. Int J Syst Evol Microbiol. https://doi.org/10.1099/ijsem.0.004781

    Article  PubMed  Google Scholar 

  • Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106(45):19126–19131

  • Richter M, Rosselló-Móra R, Glöckner FO, Peplies J (2016) JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 32:29–31

    Google Scholar 

  • Ripa FA, Tong S, Cao W-D, Wang ET, Wang T, Liu HC, Gao J-L, Sun J-G (2019) Paenibacillus rhizophilus sp. nov., a nitrogen-fixing bacterium isolated from the rhizosphere of wheat (Triticum aestivum L.). Int J Syst Evol Microbiol 69:3689–3695

    CAS  PubMed  Google Scholar 

  • Rosado AS, de Azevedo FS, da Cruz DW, van Elsas JD, Seldin L (1998) Phenotypic and genetic diversity of Paenibacillus azotofixans strains isolated from the rhizoplane or rhizosphere soil of different grasses. J Appl Microbiol 84:216–226

    Google Scholar 

  • Ruiu L (2020) Plant-Growth-Promoting Bacteria (PGPB) against insects and other agricultural pests. Agronomy 10(6):861

    CAS  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 

  • Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30(14):2068–2069

    CAS  PubMed  Google Scholar 

  • Seldin L (2011) Paenibacillus, nitrogen fixation and soil fertility. In: Logan NA, De Vos P (eds) Aerobic, endospore-forming soil bacteria. Springer-Verlag, Berlin-Heidelberg-New York, p 315

    Google Scholar 

  • Seldin L, Dubnau D (1985) DNA homology among Bacillus polymyxa, Bacillus macerans, Bacillus azotofixans and others nitrogen fixing Bacillus strains. Int Syst Bacteriol 35:151–154

    CAS  Google Scholar 

  • Seldin L, Penido EGC (1986) Identification of Bacillus azotofixans using API tests. Antonie Van Leeuwenhoek J Microbiol Serol 52:403–409

    CAS  Google Scholar 

  • Seldin L, van Elsas JD, Penido EGC (1983) Bacillus nitrogen fixers from Brazilian soils. Plant Soil 70:243–255

    Google Scholar 

  • Seldin L, van Elsas JD, Penido EGC (1984) Bacillus azotofixans sp. nov., a nitrogen-fixing species from Brazilian soils and grass roots. Int J Syst Bacteriol 34:451–456

    CAS  Google Scholar 

  • Seldin L, Rosado AS, Cruz DW, Nobrega A, van Elsas JD, Paiva E (1998) Comparison of Paenibacillus azotofixans strains isolated from rhizoplane, rhizosphere and non-rhizosphere soil from maize planted in two different Brazilian soils. Appl Environ Microbiol 64:3860–3868

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tohno M, Sakamoto M, Ohkuma M, Tajima K (2016) Paenibacillus silagei sp. nov. isolated from corn silage. Int J Syst Evol Microbiol 66:3873–3877

    CAS  PubMed  Google Scholar 

  • von der Weid I, Duarte GF, van Elsas JD, Seldin L (2002) Paenibacillus brasilensis sp. nov., a new nitrogen-fixing species isolated from the maize rhizosphere in Brazil. Int J Syst Evol Microbiol 52:2147–2153

    PubMed  Google Scholar 

  • Xu L, Dong Z, Fang L, Luo Y, Wei Z, Guo H, Zhang G, Gu YQ, Coleman-Derr D, Xia Q, Wang Y (2019) OrthoVenn2: a web server for whole-genome comparison and annotation of orthologous clusters across multiple species. Nucl Acids Res 47:W52–W58

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu S, Hegemann J, Fage C, Zimmermann M, Xie X, Linne U, Marahiel M (2016) Insights into the unique phosphorylation of the lasso peptide paeninodin. J Biol Chem 291:26

    Google Scholar 

Download references

Acknowledgements

This study was supported by grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, financial code 001) and Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ).

Funding

Conselho Nacional de Desenvolvimento Científico e Tecnológico, Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior.

Author information

Authors and Affiliations

Authors

Contributions

LS and ASR conceived the study. REV performed deposition, and LS and REV performed the polyphasic taxonomy. MBFS and EAL performed genome analysis. FA provided transmission electron microscope data. LS drafted the manuscript. All authors revised the manuscript, provided comments and approved the final version of the manuscript.

Corresponding author

Correspondence to Lucy Seldin.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants. The isolation of the Paenibacillus strain from the gut of the armored catfish described here followed the recommendations of the Guide for the Care and Use of Laboratory Animals of the Laboratory of Biology and Fisheries Technology, Institute of Biology, UFRJ.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 3466 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

da Silva, M.B.F., Lemos, E.A., Vollú, R.E. et al. Paenibacillus piscarius sp. nov., a novel nitrogen-fixing species isolated from the gut of the armored catfish Parotocinclus maculicauda. Antonie van Leeuwenhoek 115, 155–165 (2022). https://doi.org/10.1007/s10482-021-01694-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-021-01694-5

Keywords

Navigation