Genome assembly, comparative genomics, and identification of genes/pathways underlying plant growth-promoting traits of an actinobacterial strain, Amycolatopsis sp. (BCA-696).
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
10 Jul 2024
10 Jul 2024
Historique:
received:
16
10
2023
accepted:
04
07
2024
medline:
11
7
2024
pubmed:
11
7
2024
entrez:
10
7
2024
Statut:
epublish
Résumé
The draft genome sequence of an agriculturally important actinobacterial species Amycolatopsis sp. BCA-696 was developed and characterized in this study. Amycolatopsis BCA-696 is known for its biocontrol properties against charcoal rot and also for plant growth-promotion (PGP) in several crop species. The next-generation sequencing (NGS)-based draft genome of Amycolatopsis sp. BCA-696 comprised of ~ 9.05 Mb linear chromosome with 68.75% GC content. In total, 8716 protein-coding sequences and 61 RNA-coding sequences were predicted in the genome. This newly developed genome sequence has been also characterized for biosynthetic gene clusters (BGCs) and biosynthetic pathways. Furthermore, we have also reported that the Amycolatopsis sp. BCA-696 produces the glycopeptide antibiotic vancomycin that inhibits the growth of pathogenic gram-positive bacteria. A comparative analysis of the BCA-696 genome with publicly available closely related genomes of 14 strains of Amycolatopsis has also been conducted. The comparative analysis has identified a total of 4733 core and 466 unique orthologous genes present in the BCA-696 genome The unique genes present in BCA-696 was enriched with antibiotic biosynthesis and resistance functions. Genome assembly of the BCA-696 has also provided genes involved in key pathways related to PGP and biocontrol traits such as siderophores, chitinase, and cellulase production.
Identifiants
pubmed: 38987320
doi: 10.1038/s41598-024-66835-y
pii: 10.1038/s41598-024-66835-y
doi:
Substances chimiques
Vancomycin
6Q205EH1VU
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
15934Subventions
Organisme : DBT's Ramalingaswami grant
ID : BT/RLF/Re-entry/47/2015
Organisme : Human Resource Development Centre, Council of Scientific And Industrial Research
ID : 09/0414(13976)/2022-EMR-I
Informations de copyright
© 2024. The Author(s).
Références
Leontidou, K. et al. Plant growth promoting rhizobacteria isolated from halophytes and drought-tolerant plants: Genomic characterisation and exploration of phyto-beneficial traits. Sci. Rep. 10, 14857 (2020).
pubmed: 32908201
pmcid: 7481233
doi: 10.1038/s41598-020-71652-0
Gu, Y., Ma, Y., Wang, J., Xia, Z. & Wei, H. Genomic insights into a plant growth-promoting Pseudomonas koreensis strain with cyclic lipopeptide-mediated antifungal activity. Microbiologyopen 9, 133 (2020).
doi: 10.1002/mbo3.1092
Chen, X. H. et al. Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat. Biotechnol. 25, 1007–1014 (2007).
pubmed: 17704766
doi: 10.1038/nbt1325
Olanrewaju, O. S., Ayilara, M. S., Ayangbenro, A. S. & Babalola, O. O. Genome mining of three plant growth-promoting bacillus species from maize rhizosphere. Appl. Biochem. Biotechnol. 193, 3949–3969 (2021).
pubmed: 34529229
pmcid: 8610958
doi: 10.1007/s12010-021-03660-3
Chandra, A., Chandra, P. & Tripathi, P. Whole genome sequence insight of two plant growth-promoting bacteria (B. subtilis BS87 and B. megaterium BM89) isolated and characterized from sugarcane rhizosphere depicting better crop yield potentiality. Microbiol. Res. 247, 126733 (2021).
pubmed: 33676313
doi: 10.1016/j.micres.2021.126733
Babalola, O. O., Adeleke, B. S. & Ayangbenro, A. S. Whole genome sequencing of sunflower root-associated Bacillus cereus. Evol. Bioinform. 17, 117693432110389 (2021).
doi: 10.1177/11769343211038948
Kwak, Y., Park, G.-S. & Shin, J.-H. High quality draft genome sequence of the type strain of Pseudomonas lutea OK2T, a phosphate-solubilizing rhizospheric bacterium. Stand. Genomic Sci. 11, 51 (2016).
pubmed: 27555890
pmcid: 4994261
doi: 10.1186/s40793-016-0173-7
Devi, U. et al. Genomic and functional characterization of a novel Burkholderia sp. strainAU4i from pea rhizosphere conferring plant growth promoting activities. Adv. Genet. Eng. 2015, 1–8 (2015).
Matteoli, F. P. et al. Genome sequencing and assessment of plant growth-promoting properties of a Serratia marcescens strain isolated from vermicompost. BMC Genomics 19, 750 (2018).
pubmed: 30326830
pmcid: 6192313
doi: 10.1186/s12864-018-5130-y
Suarez, C. et al. Complete genome sequence of the plant growth-promoting bacterium Hartmannibacter diazotrophicus strain E19
doi: 10.1155/2019/7586430
Gupta, A. et al. Whole genome sequencing and analysis of plant growth promoting bacteria isolated from the rhizosphere of plantation crops coconut, cocoa and arecanut. PLoS One 9, e104259 (2014).
pubmed: 25162593
pmcid: 4146471
doi: 10.1371/journal.pone.0104259
Singh, R. P., Nalwaya, S. & Jha, P. N. The draft genome sequence of the plant growth promoting rhizospheric bacterium Enterobacter cloacae SBP-8. Genomics Data 12, 81–83 (2017).
pubmed: 28386532
pmcid: 5374853
doi: 10.1016/j.gdata.2017.03.006
Kang, S.-M. et al. Complete genome sequence of Pseudomonas psychrotolerans CS51, a plant growth-promoting bacterium, under heavy metal stress conditions. Microorganisms 8, 382 (2020).
pubmed: 32182882
pmcid: 7142416
doi: 10.3390/microorganisms8030382
Subramaniam, G. et al. Complete genome sequence of sixteen plant growth promoting Streptomyces strains. Sci. Rep. 10, 10294 (2020).
pubmed: 32581303
pmcid: 7314817
doi: 10.1038/s41598-020-67153-9
Alekhya, G. & Gopalakrishnan, S. Exploiting plant growth-promoting Amycolatopsis sp. in chickpea and sorghum for improving growth and yield. J. Food Legum. 29, 225–231 (2016).
Gopalakrishnan, S., Srinivas, V., Naresh, N., Alekhya, G. & Sharma, R. Exploiting plant growth-promoting Amycolatopsis sp. for bio-control of charcoal rot of sorghum (Sorghum bicolor L.) caused by Macrophomina phaseolina (Tassi) Goid. Arch. Phytopathol. Plant Prot. 52, 543–559 (2019).
doi: 10.1080/03235408.2018.1553472
Hazen, W., de Bruyn, J. C. & van Dijken, J. P. Nocardia sp. 239, a facultative methanol utilizer with the ribulose monophosphate pathway of formaldehyde fixation. Arch. Microbiol. 135, 205–210 (1983).
doi: 10.1007/BF00414481
Lechevalier, M. P., Prauser, H., Labeda, D. P. & Ruan, J.-S. Two new genera of nocardioform actinomycetes: Amycolata gen. nov. and Amycolatopsis gen. nov. Int. J. Syst. Bacteriol. 36, 29–37 (1986).
doi: 10.1099/00207713-36-1-29
Frasch, H.-J. et al. Alternative pathway to a glycopeptide-resistant cell wall in the Balhimycin producer Amycolatopsis balhimycina. ACS Infect. Dis. 1, 243–252 (2015).
pubmed: 27622740
doi: 10.1021/acsinfecdis.5b00011
Nigam, A. et al. Modification of rifamycin polyketide backbone leads to improved drug activity against rifampicin-resistant Mycobacterium tuberculosis. J. Biol. Chem. 289, 21142–21152 (2014).
pubmed: 24923585
pmcid: 4110317
doi: 10.1074/jbc.M114.572636
Xu, L. et al. Complete genome sequence and comparative genomic analyses of the vancomycin-producing Amycolatopsis orientalis. BMC Genomics 15, 363 (2014).
pubmed: 24884615
pmcid: 4048454
doi: 10.1186/1471-2164-15-363
Kumari, R., Singh, P. & Lal, R. Genetics and genomics of the genus Amycolatopsis. Indian J. Microbiol. 56, 233–246 (2016).
pubmed: 27407288
pmcid: 4920768
doi: 10.1007/s12088-016-0590-8
Sánchez-Hidalgo, M., González, I., Díaz-Muñoz, C., Martínez, G. & Genilloud, O. Comparative genomics and biosynthetic potential analysis of two lichen-isolated Amycolatopsis strains. Front. Microbiol. 9, 11 (2018).
doi: 10.3389/fmicb.2018.00369
Emms, D. M. & Kelly, S. OrthoFinder: Phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238 (2019).
pubmed: 31727128
pmcid: 6857279
doi: 10.1186/s13059-019-1832-y
Aziz, R. K. et al. The RAST server: Rapid annotations using subsystems technology. BMC Genomics 9, 75 (2008).
pubmed: 18261238
pmcid: 2265698
doi: 10.1186/1471-2164-9-75
Schwartz, D. et al. Biosynthetic gene cluster of the herbicide phosphinothricin tripeptide from Streptomyces viridochromogenes Tü494. Appl. Environ. Microbiol. 70, 7093–7102 (2004).
pubmed: 15574905
pmcid: 535184
doi: 10.1128/AEM.70.12.7093-7102.2004
Riseh, R. S., Vatankhah, M., Hassanisaadi, M. & Barka, E. A. Unveiling the role of hydrolytic enzymes from soil biocontrol bacteria in sustainable phytopathogen management. Front. Biosci. 29, 13 (2024).
Bala, S. et al. Reclassification of Amycolatopsis mediterranei DSM 46095 as Amycolatopsis rifamycinica sp. nov.. Int. J. Syst. Evol. Microbiol. 54, 1145–1149 (2004).
pubmed: 15280283
doi: 10.1099/ijs.0.02901-0
Adamek, M. et al. Comparative genomics reveals phylogenetic distribution patterns of secondary metabolites in Amycolatopsis species. BMC Genomics 19, 426 (2018).
pubmed: 29859036
pmcid: 5984834
doi: 10.1186/s12864-018-4809-4
Tang, B. et al. A systematic study of the whole genome sequence of Amycolatopsis methanolica strain 239 T provides an insight into its physiological and taxonomic properties which correlate with its position in the genus. Synth. Syst. Biotechnol. 1, 169–186 (2016).
pubmed: 29062941
pmcid: 5640789
doi: 10.1016/j.synbio.2016.05.001
Meier-Kolthoff, J. P. & Göker, M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat. Commun. 10, 2182 (2019).
pubmed: 31097708
pmcid: 6522516
doi: 10.1038/s41467-019-10210-3
Murakami, T. et al. The bialaphos biosynthetic genes of Streptomyces hygroscopicus: Molecular cloning and characterization of the gene cluster. Mol. Gen. Genet. MGG 205, 42–53 (1986).
doi: 10.1007/BF02428031
Pal, K. K., Tilak, K. V. B. R., Saxcna, A. K., Dey, R. & Singh, C. S. Suppression of maize root diseases caused by Macrophomina phaseolina, Fusarium moniliforme and Fusarium graminearum by plant growth promoting rhizobacteria. Microbiol. Res. 156, 209–223 (2001).
pubmed: 11716210
doi: 10.1078/0944-5013-00103
Tokala, R. K. et al. Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum ). Appl. Environ. Microbiol. 68, 2161–2171 (2002).
pubmed: 11976085
pmcid: 127534
doi: 10.1128/AEM.68.5.2161-2171.2002
Donate-Correa, J., León-Barrios, M. & Pérez-Galdona, R. Screening for plant growth-promoting rhizobacteria in Chamaecytisus proliferus (tagasaste), a forage tree-shrub legume endemic to the Canary Islands. Plant Soil 266, 261–272 (2005).
doi: 10.1007/s11104-005-0754-5
Ando, T. et al. A new non-protein enediyne antibiotic N11999A2: Unique enediyne chromophore similar to neocarzinostatin and DNA cleavage feature. Tetrahedron Lett. 39, 6495–6498 (1998).
doi: 10.1016/S0040-4039(98)01383-5
Cui, B. et al. Antifungal Enediynes, United States Patent US09/679672.2000-10-05.42.
Su, Z.-Z. et al. Evidence for biotrophic lifestyle and biocontrol potential of dark septate endophyte Harpophora oryzae to rice blast disease. PLoS One 8, e61332 (2013).
pubmed: 23637814
pmcid: 3630206
doi: 10.1371/journal.pone.0061332
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
pubmed: 24695404
pmcid: 4103590
doi: 10.1093/bioinformatics/btu170
Luo, R. et al. SOAPdenovo2: An empirically improved memory-efficient short-read de novo assembler. Gigascience 1, 18 (2012).
pubmed: 23587118
pmcid: 3626529
doi: 10.1186/2047-217X-1-18
Bankevich, A. et al. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).
pubmed: 22506599
pmcid: 3342519
doi: 10.1089/cmb.2012.0021
Gurevich, A., Saveliev, V., Vyahhi, N. & Tesler, G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 29, 1072–1075 (2013).
pubmed: 23422339
pmcid: 3624806
doi: 10.1093/bioinformatics/btt086
Xu, M. et al. TGS-GapCloser: A fast and accurate gap closer for large genomes with low coverage of error-prone long reads. Gigascience 9, giaa094 (2020).
pubmed: 32893860
pmcid: 7476103
doi: 10.1093/gigascience/giaa094
Snyder, E. E. et al. PATRIC: The VBI PathoSystems resource integration center. Nucleic Acids Res. 35, D401–D406 (2007).
pubmed: 17142235
doi: 10.1093/nar/gkl858
Larsen, M. V. et al. Benchmarking of methods for genomic taxonomy. J. Clin. Microbiol. 52, 1529–1539 (2014).
pubmed: 24574292
pmcid: 3993634
doi: 10.1128/JCM.02981-13
Bosi, E. et al. MeDuSa: A multi-draft based scaffolder. Bioinformatics 31, 2443–2451 (2015).
pubmed: 25810435
doi: 10.1093/bioinformatics/btv171
Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212 (2015).
pubmed: 26059717
doi: 10.1093/bioinformatics/btv351
Krzywinski, M. I. et al. Circos: An information aesthetic for comparative genomics. Genome Res. https://doi.org/10.1101/gr.092759.109 (2009).
doi: 10.1101/gr.092759.109
pubmed: 19541911
pmcid: 2752132
Bertels, F., Silander, O. K., Pachkov, M., Rainey, P. B. & van Nimwegen, E. Automated reconstruction of whole-genome phylogenies from short-sequence reads. Mol. Biol. Evol. 31, 1077–1088 (2014).
pubmed: 24600054
pmcid: 3995342
doi: 10.1093/molbev/msu088
Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).
doi: 10.1007/978-3-319-24277-4
Page, A. J. et al. Roary: Rapid large-scale prokaryote pan genome analysis. Bioinformatics 31, 3691–3693 (2015).
pubmed: 26198102
pmcid: 4817141
doi: 10.1093/bioinformatics/btv421
Seemann, T. Prokka: Rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014).
pubmed: 24642063
doi: 10.1093/bioinformatics/btu153
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
pubmed: 23329690
pmcid: 3603318
doi: 10.1093/molbev/mst010
Li, W. & Godzik, A. Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659 (2006).
pubmed: 16731699
doi: 10.1093/bioinformatics/btl158
Kanehisa, M. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27–30 (2000).
pubmed: 10592173
pmcid: 102409
doi: 10.1093/nar/28.1.27
Skinnider, M. A. et al. Comprehensive prediction of secondary metabolite structure and biological activity from microbial genome sequences. Nat. Commun. 11, 6058 (2020).
pubmed: 33247171
pmcid: 7699628
doi: 10.1038/s41467-020-19986-1
Blin, K. et al. antiSMASH 70: New and improved predictions for detection, regulation, chemical structures and visualisation. Nucleic Acids Res. 51(W1), W46–W50 (2023).
pubmed: 37140036
pmcid: 10320115
doi: 10.1093/nar/gkad344