Paenibacillus plantiphilus sp. nov. from the plant environment of Zea mays

Antonie van Leeuwenhoek - Tập 116 - Trang 883-892 - 2023
Peter Kämpfer1, André Lipski2, Lucie Lamothe3,4, Dominique Clermont5, Alexis Criscuolo4, John A. McInroy6, Stefanie P. Glaeser1
1Institut für Angewandte Mikrobiologie, Justus-Liebig-Universität Giessen, Giessen, Germany
2Institut für Ernährungs– und Lebensmittelwissenschaften, Lebensmittelmikrobiologie und –hygiene, Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, Germany
3CNRS, IFB-Core, UMS 3601, Institut Français de Bioinformatique, Evry, France
4Institut Pasteur, Bioinformatics and Biostatistics Hub, Université de Paris, Paris, France
5Institut Pasteur, CIP - Collection of Institut Pasteur, Université de Paris, Paris, France
6Department of Entomology and Plant Pathology, Auburn University, Alabama, USA

Tóm tắt

A Gram-strain positive, aerobic, endospore-forming bacterial strain (JJ-246T) was isolated from the rhizosphere of Zea mays. The 16S rRNA gene sequence similarity comparisons showed a most closely relationship to Paenibacillus oenotherae DT7-4T (98.4%) and Paenibacillus xanthinolyticus 11N27T (98.0%). The pairwise average nucleotide identity and digital DNA-DNA hybridisation values of the JJ-246T genome assembly against publicly available Paenibacillus type strain genomes were below 82% and 33%, respectively. The draft genome of JJ-246T shared many putative plant-beneficial functions contributing (PBFC) genes, related to plant root colonisation, oxidative stress protection, degradation of aromatic compounds, plant growth-promoting traits, disease resistance, drug and heavy metal resistance, and nutrient acquisition. The quinone system of strain JJ-246T, the polar lipid profile and the major fatty acids were congruent with those reported for members of the genus Paenibacillus. JJ-246T was shown to represent a novel species of the genus Paenibacillus, for which the name Paenibacillus plantiphilus sp. nov. is proposed, with JJ-246T (= LMG 32093T = CCM 9089T = CIP 111893T) as the type strain.

Tài liệu tham khảo

Ash C, Priest FG, Collins MD (1993) Molecular identification of rRNA group 3 bacilli (Ash, Farrow, Wallbanks and Collins) using a PCR probe test. Antonie Van Leeuwenhoek 64:253–260. https://doi.org/10.1007/bf00873085 Beneduzi A, Costa PB, Parma M et al (2010) Paenibacillus riograndensis sp. nov., a nitrogen-fixing species isolated from the rhizosphere of Triticum aestivum. Int J Syst Evol Microbiol 60:128–133. https://doi.org/10.1099/ijs.0.011973-0 Blin K, Shaw S, Kloosterman AM et al (2021) antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res 49:W29–W35 Brosius J, Palmer ML, Kennedy PJ et al (1978) Complete nucleotide-sequence of a 16S ribosomal-RNA gene from Escherichia coli. PNAS 75:4801–4805. https://doi.org/10.1073/pnas.75.10.4801 Carro L, Flores-Félix JD, Cerda-Castillo E et al (2013) Paenibacillus endophyticus sp. nov., isolated from nodules of Cicer arietinum. Int J Syst Evol Microbiol 63:4433–4438. https://doi.org/10.1099/ijs.0.050310-0 Cherif-Silini H, Thissera B, Chenari Bouket A et al (2019) Durum wheat stress tolerance induced by endophyte pantoea agglomerans with genes contributing to plant functions and secondary metabolite arsenal. Int J Mol Sci 20:3989. https://doi.org/10.3390/ijms20163989 Criscuolo A (2019) A fast alignment-free bioinformatics procedure to infer accurate distance-based phylogenetic trees from genome assemblies. Res Ideas Outcomes 5:e36178. https://doi.org/10.3897/rio.5.e36178 Criscuolo A (2020) On the transformation of MinHash-based uncorrected distances into proper evolutionary distances for phylogenetic inference. F1000Research 9:1309. https://doi.org/10.12688/f1000research.26930.1 Criscuolo A, Gribaldo S (2010) BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol 10:210. https://doi.org/10.1186/1471-2148-10-210 de Andrade LA, Santos CHB, Frezarin ET, Sales LR, Rigobelo EC (2023) Plant growth-promoting rhizobacteria for sustainable agricultural production. Microorganisms 11(4):1088. https://doi.org/10.3390/microorganisms11041088 Din ARJM, Rosli MA, Azam ZM, Othman NZ, Sarmidi MR (2020) Paenibacillus polymyxa role involved in phosphate solubilization and growth promotion of Zea mays under abiotic stress condition. Proc Natl Acad Sci USA 90:63–71. https://doi.org/10.1007/s40011-019-01081-1 Elo S, Suominen I, Kämpfer P et al (2001) Paenibacillus borealis sp. nov., a nitrogen-fixing species isolated from spruce forest humus in Finland. Int J Syst Evol Microbiol 51:535–545 Felsenstein J (1985) Confidence limits of phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle Gao JL, Lv FY, Wang XM et al (2015) Paenibacillus wenxiniae sp. nov., a nifH gene-harbouring endophytic bacterium isolated from maize. Antonie Van Leeuwenhoek 108:1015–1022. https://doi.org/10.1007/s10482-015-0554-8 Gerhardt P, Murray RGE, Wood W et al (1994) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, DC Grady EN, MacDonald J, Liu L et al (2016) Current knowledge and perspectives of Paenibacillus: a review. Microb Cell Fact 15:203. https://doi.org/10.1186/s12934-016-0603-7 Han T-Y, Tong X-M, Wang Y-W et al (2015) Paenibacillus populi sp. nov., a novel bacterium isolated from the rhizosphere of Populus alba. Antonie Van Leeuwenhoek 108:659–666. https://doi.org/10.1007/s10482-015-0521-4 Hong YY, Ma YC, Zhou YG et al (2009) Paenibacillus sonchi sp. nov., a nitrogen-fixing species isolated from the rhizosphere of Sonchus oleraceus. Int J Syst Evol Microbiol 59:2656–2661. https://doi.org/10.1099/ijs.0.009308-0 Huang E, Guo Y, Yousef AE (2014) Biosynthesis of the new broad-spectrum lipopeptide antibiotic paenibacterin in Paenibacillus thiaminolyticus OSY-SE. Res Microbiol 165:243–251. https://doi.org/10.1016/j.resmic.2014.02.002 Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler V, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589. https://doi.org/10.1038/nmeth.4285 Kämpfer P (1990) Evaluation of the Titertek-Enterobac-Automated system (TTE-AS) for identification of Enterobacteriaceae. Zentbl Bakteriol 273:164–172. https://doi.org/10.1016/s0934-8840(11)80244-6 Kämpfer P, Steiof M, Becker P, Dott W (1993) Characterization of chemoheterotrophic bacteria associated with the in situ bioremediation of a waste-oil contaminated site. Microb Ecol 26:161–188. https://doi.org/10.1007/BF00177050 Kämpfer P, Kroppenstedt RM (1996) Numerical analysis of fatty acid patterns of coryneform bacteria and related taxa. Can J Microbiol 42:989–1005. https://doi.org/10.1139/m96-128 Kämpfer P, Steiof M, Dott W (1991) Microbiological characterisation of a fuel-oil contaminated site including numerical identification of heterotrophic water and soil bacteria. Microbiol Ecol 21:227–243. https://doi.org/10.1007/bf02539156 Kämpfer P, Busse HJ, McInroy JA et al (2021) Paenibacillus allorhizosphaerae sp. Nov., from soil of the rhizosphere of Zea mays. Int J Syst Evol Microbiol. https://doi.org/10.1099/ijsem.0.005051 Kämpfer P, Busse HJ, Kloepper JW et al (2016) Paenibacillus cucumis sp. nov., isolated from a cucumber plant. Int J Syst Evol Microbiol 66:2599–2603 Kämpfer P, Busse HJ, McInroy JA et al (2017a) Paenibacillus nebraskensis sp. nov., isolated from the root surface of field-grown maize. Int J Syst Evol Microbiol 67:4956–4961. https://doi.org/10.1099/ijsem.0.002357 Kämpfer P, Busse HJ, McInroy JA et al (2017b) Paenibacillus rhizoplanae sp. nov., isolated from the rhizosphere of Zea mays. Int J Syst Evol Microbiol 67:1058–1063. https://doi.org/10.1099/ijsem.0.001779 Kämpfer P, Lipski A, Lamothe L, Clermont D, Criscuolo A et al (2022) Paenibacillus allorhizoplanae sp. Nov. from the rhizoplane of a Zea mays root. Arch Microbiol 204:630. https://doi.org/10.1007/s00203-022-03225-w Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010 Katoh K, Standley DM (2016) A simple method to control over-alignment in the MAFFT multiple sequence alignment program. Bioinformatics 32:1933–1942. https://doi.org/10.1093/bioinformatics/btw108 Kim BC, Lee KH, Kim MN et al (2009a) Paenibacillus pini sp. nov., a cellulolytic bacterium isolated from the rhizosphere of pine tree. J Microbiol 47:699–704. https://doi.org/10.1007/s12275-009-0343-z Kim BC, Lee KH, Kim MN et al (2009b) Paenibacillus pinihumi sp. nov., a cellulolytic bacterium isolated from the rhizosphere of Pinus densiflora. J Microbiol 47:530–535. https://doi.org/10.1007/s12275-009-0270-z Kim Du, Kim SG, Lee H, Chun J, Cho JC et al (2015a) Paenibacillus xanthinilyticus sp. nov., isolated from agricultural soil. Int J Syst Evol Microbiol 65:2937–2942 Kim TS, Han JH, Joung Y, Kim SB (2015b) Paenibacillus oenotherae sp. nov. and Paenibacillus hemerocallicola sp. nov., isolated from the roots of herbaceous plants. Int J Syst Evol Microbiol 65:2717–2715 Kittiwongwattana C, Thawai C (2015) Paenibacillus lemnae sp. nov., an endophytic bacterium of duckweed (Lemna aequinoctialis). Int J Syst Evol Microbiol 65:107–112. https://doi.org/10.1099/ijs.0.067876-0 Lai WA, Hameed A, Lin SY et al (2015) Paenibacillus medicaginis sp. nov. a chitinolytic endophyte isolated from the root nodule of alfalfa (Medicago sativa L.). Int J Syst Evol Microbiol 65:3853–3860. https://doi.org/10.1099/ijsem.0.000505 Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–175 Li JY, Gao TT, Wang Q (2020) Comparative and functional analyses of two sequenced Paenibacillus polymyxa genomes provides insights into their potential genes related to plant growth-promoting features and biocontrol mechanisms. Front Genet 11:564939. https://doi.org/10.3389/fgene.2020.564939 Liu Y, Zhai L, Wang R et al (2015) Paenibacillus zeae sp. nov., isolated from maize (Zea mays L.) seeds. Int J Syst Evol Microbiol 65:4533–4538. https://doi.org/10.1099/ijsem.0.000608 Ludwig W, Strunk O, Westram R et al (2004) ARB: a software environment for sequence data. Nucleic Acid Res 32:1363–1371. https://doi.org/10.1093/nar/gkh293 Ma Y, Xia Z, Liu X et al (2007) Paenibacillus sabinae sp. nov., a nitrogen-fixing species isolated from the rhizosphere soils of shrubs. Int J Syst Evol Microbiol 57:6–11. https://doi.org/10.1099/ijs.0.64519-0 Minh BQ, Schmidt HA, Chernomor O et al (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 37:1530–1534. https://doi.org/10.1093/molbev/msaa015 Minnikin DE, O’Donnell AG, Goodfellow M et al (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiological Method 2:233–241. https://doi.org/10.1016/0167-7012(84)90018-6 Parks DH, Chuvochina M, Waite DW et al (2018) A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 36:996–1004. https://doi.org/10.1038/nbt.4229 Rivas R, García-Fraile P, Mateos PF et al (2006) Paenibacillus cellulosilyticus sp. nov., a cellulolytic and xylanolytic bacterium isolated from the bract phyllosphere of Phoenix dactylifera. Int J Syst Evol Microbiol 56:2777–2781. https://doi.org/10.1099/ijs.0.64480-0 Rivas R, Mateos PF, Martínez-Molina E et al (2005) Paenibacillus phyllosphaerae sp. nov., a xylanolytic bacterium isolated from the phyllosphere of Phoenix dactylifera. Int J Syst Evol Microbiol 55:743–746. https://doi.org/10.1099/ijs.0.63323-0 Schauss T, Busse HJ, Golke J et al (2015) Empedobacter stercoris sp. nov., isolated from an input sample of a biogas plant. Int J Syst Evol Microbiol 65:3746–3753. https://doi.org/10.1099/ijsem.0.000486 Shao J, Li S, Zhang N, Cui X, Zhou X, Zhang G, Shen Q, Zhang R (2015) Analysis and cloning of the synthetic pathway of the phytohormone indole-3-acetic acid in the plant-beneficial Bacillus amyloliquefaciens SQR9. Microb Cell Fact 14:130. https://doi.org/10.1186/s12934-015-0323-4 Son J-S, Kang H-U, Ghim S-Y (2014) Paenibacillus dongdonensis sp. nov., isolated from rhizospheric soil of Elymus tsukushiensis. Int J Syst Evol Microbiol 64:2865–2870. https://doi.org/10.1099/ijs.0.061077-0 Stamatakis A (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. https://doi.org/10.1093/bioinformatics/btl446 Tamura K, Stecher G, Kumar S (2021) MEGA11: Molecular evolutionary genetics analysis version 11. Mol Biol Evol 38(7):3022–3027. https://doi.org/10.1093/molbev/msab120 Wang DS, Jiang YY, Wie XM et al (2014) Paenibacillus quercus sp. nov., isolated from rhizosphere of Quercus aliena var. acuteserrata. Antonie Van Leeuwenhoek 105:1173–1178. https://doi.org/10.1007/s10482-014-0178-4 Wang D, Poinsot V, Li W et al (2023) Genomic insights and functional analysis reveal plant growth promotion traits of Paenibacillus mucilaginosus G78. Genes (Basel) 14(2):392. https://doi.org/10.3390/genes14020392 Wiertz R, Schulz SC, Müller U et al (2013) Corynebacterium frankenforstense sp. nov. and Corynebacterium lactis sp. nov., isolated from raw cow milk. Int J Syst Evol Microbiol 63:4495–4501. https://doi.org/10.1099/ijs.0.050757-0 Xie J-B, Du Z, Bai L et al (2014) Comparative genomic analysis of N2-fixing and Non-N2-fixing Paenibacillus spp.: organization, evolution and expression of the nitrogen fixation genes. PLoS Genet 10(3):e1004231. https://doi.org/10.1371/journal.pgen.1004231 Xin K, Li M, Chen C et al (2017) Paenibacillus qinlingensis sp. nov., an indole-3-acetic acid-producing bacterium isolated from roots of Sinopodophyllum hexandrum (Royle) Ying. Int J Syst Evol Microbiol 67:589–595. https://doi.org/10.1099/ijsem.0.001666 Yarza P, Richter M, Peplies J et al (2008) The all-species living tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst Appl Microbiol 31:241–250. https://doi.org/10.1016/j.syapm.2008.07.001 Yuan L, Jiang H, Jiang X et al (2022) Comparative genomic and functional analyses of Paenibacillus peoriae ZBSF16 with biocontrol potential against grapevine diseases, provide insights into its genes related to plant growth-promoting and biocontrol mechanisms. Front Microbiol 13:975344. https://doi.org/10.3389/fmicb.2022.975344 Zhang L, Gao JS, Zhang S et al (2015) Paenibacillus rhizoryzae sp. nov., isolated from rice rhizosphere. Int J Syst Evol Microbiol 65:3053–3059. https://doi.org/10.1099/ijs.0.000376 Zhang J, Wang ZT, Yu HM et al (2013) Paenibacillus catalpae sp. nov., isolated from the rhizosphere soil of Catalpa speciosa. Int J Syst Evol Microbiol 63:1776–1781. https://doi.org/10.1099/ijs.0.040659-0 Zhu S, Hegemann JD, Fage CD et al (2016) Insights into the Unique phosphorylation of the lasso peptide paeninodin. J Biol Chem 291(26):13662–13678. https://doi.org/10.1074/jbc.M116.722108