Advertisement

Antonie van Leeuwenhoek

, Volume 112, Issue 1, pp 67–74 | Cite as

Draft genome sequence of the symbiotic Frankia sp. strain BMG5.30 isolated from root nodules of Coriaria myrtifolia in Tunisia

  • Abdellatif Gueddou
  • Erik Swanson
  • Karima Hezbri
  • Imen Nouioui
  • Amir Ktari
  • Stephen Simpson
  • Krystalynne Morris
  • W. Kelley Thomas
  • Faten Ghodhbane-Gtari
  • Maher GtariEmail author
  • Louis S. TisaEmail author
Original Paper

Abstract

Frankia sp. strain BMG5.30 was isolated from root nodules of a Coriaria myrtifolia seedling on soil collected in Tunisia and represents the second cluster 2 isolate. Frankia sp. strain BMG5.30 was able to re-infect C. myrtifolia generating root nodules. Here, we report its 5.8-Mbp draft genome sequence with a G + C content of 70.03% and 4509 candidate protein-encoding genes.

Keywords

Actinobacteria Actinorhizal symbiosis Hydrogenase Nitrogen fixation Natural products Host microbe interactions Genomes 

Notes

Acknowledgements

Partial funding was provided by the New Hampshire Agricultural Experiment Station. This is Scientific Contribution Number 2740. This work was also supported by the USDA National Institute of Food and Agriculture Hatch 022821 (LST), Agriculture and Food Research Initiative Grant 2015-67014-22849 from the USDA National Institute of Food and Agriculture (LST), and the College of Life Science and Agriculture at the University of New Hampshire-Durham. Sequencing was performed on an Illumina HiSeq 2500 purchased with an NSF MRI Grant: DBI-1229361 to WK Thomas.

Authors Contribution

MG, FGG, and LST conceived the study. AG, ES, HK. AK, IN, KM, ST, and WKT performed the research. ES, AG, MG, FGG, and LST analaized the data. AG, ES, MG, FGG, and LST wrote the manuscript. All the authors approved the paper.

Compliance with ethical standards

Conflict of interest

The authors have declared that they have no competing interest exists.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

10482_2018_1138_MOESM1_ESM.pdf (51 kb)
Supplementary material 1 (PDF 51 kb)
10482_2018_1138_MOESM2_ESM.xlsx (76 kb)
ESM1: COG analysis for the Frankia cluster 2 genomes (XLSX 76 kb)
10482_2018_1138_MOESM3_ESM.xlsx (174 kb)
ESM2: BMG5.30 and BMG5.1 overlap genes from Venn diagram (Figure 3) among the cluster 2 genomes (XLSX 173 kb)
10482_2018_1138_MOESM4_ESM.xlsx (32 kb)
ESM3: Core genome from Venn diagram (Figure 3) among the cluster 2 genomes (XLSX 31 kb)
10482_2018_1138_MOESM5_ESM.xlsx (110 kb)
ESM4: Singleton genes for the cluster 2 genomes (XLSX 110 kb)
10482_2018_1138_MOESM6_ESM.xlsx (40 kb)
ESM5: BMG5.30, BMG5.1 and Dg1 overlap genes from Venn diagram (Figure 3) among the cluster 2 genomes (XLSX 39 kb)
10482_2018_1138_MOESM7_ESM.xlsx (34 kb)
ESM6: BMG5.30, BMG5.1 and Dg2 overlap genes from Venn diagram (Figure 3) among the cluster 2 genomes (XLSX 33 kb)
10482_2018_1138_MOESM8_ESM.xlsx (20 kb)
ESM7: BMG5.30and Dg1 overlap genes from Venn diagram (Figure 3) among the cluster 2 genomes (XLSX 20 kb)
10482_2018_1138_MOESM9_ESM.xlsx (51 kb)
ESM8: BMG5.30 and Dg2 overlap genes from Venn diagram (Figure 3) among the cluster 2 genomes (XLSX 51 kb)
10482_2018_1138_MOESM10_ESM.xlsx (22 kb)
ESM9: BMG5.30, Dg1 and Dg2 overlap genes from Venn diagram (Figure 3) among the cluster 2 genomes (XLSX 21 kb)
10482_2018_1138_MOESM11_ESM.xlsx (17 kb)
ESM10: BMG5.1 and Dg1 overlap genes from Venn diagram (Figure 3) among the cluster 2 genomes (XLSX 16 kb)
10482_2018_1138_MOESM12_ESM.xlsx (24 kb)
ESM11: BMG5.1 and Dg2 overlap genes from Venn diagram (Figure 3) among the cluster 2 genomes (XLSX 24 kb)
10482_2018_1138_MOESM13_ESM.xlsx (37 kb)
ESM12: BMG5.1, Dg1 and Dg2 overlap genes from Venn diagram (Figure 3) among the cluster 2 genomes (XLSX 36 kb)
10482_2018_1138_MOESM14_ESM.pdf (39 kb)
ESM13: Dg1 and Dg2 overlap genes from Venn diagram (Figure 3) among the cluster 2 genomes (PDF 39 kb)

References

  1. Bennett S (2004) Solexa Ltd. Pharmacogenomics 5:433–438.  https://doi.org/10.1517/14622416.5.4.433 CrossRefGoogle Scholar
  2. Blin K, Medema MH, Kazempour D, Fischbach MA, Breitling R, Takano E, Weber T (2013) antiSMASH 2.0-a versatile platform for genome mining of secondary metabolite producers. Nucleic Acids Res 41:W204–W212.  https://doi.org/10.1093/nar/gkt449 CrossRefGoogle Scholar
  3. Blin K et al (2017) antiSMASH 4.0-improvements in chemistry prediction and gene cluster boundary identification. Nucleic Acids Res 45:W36–W41.  https://doi.org/10.1093/nar/gkx319 CrossRefGoogle Scholar
  4. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120.  https://doi.org/10.1093/bioinformatics/btu170 CrossRefGoogle Scholar
  5. Chabaud M et al (2016) Chitinase-resistant hydrophilic symbiotic factors secreted by Frankia activate both Ca2 + spiking and NIN gene expression in the actinorhizal plant Casuarina glauca. New Phytol 209:86–93.  https://doi.org/10.1111/nph.13732 CrossRefGoogle Scholar
  6. Chaia EE, Wall LG, Huss-Danell K (2010) Life in soil by the actinorhizal root nodule endophyte Frankia. A Rev Symbiosis 51:201–226.  https://doi.org/10.1007/s13199-010-0086-y CrossRefGoogle Scholar
  7. Clavijo F et al (2015) The Casuarina NIN gene is transcriptionally activated throughout Frankia root infection as well as in response to bacterial diffusible signals. New Phytol 208:887–903.  https://doi.org/10.1111/nph.13506 CrossRefGoogle Scholar
  8. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797.  https://doi.org/10.1093/nar/gkh340 CrossRefGoogle Scholar
  9. Felsenstein J (1981) Evolutionary trees from gene-frequencies and quantitative characters—finding maximum-likelihood estimates. Evolution 35:1229–1242.  https://doi.org/10.2307/2408134 CrossRefGoogle Scholar
  10. Ghodhbane-Gtari F, Nouioui I, Chair M, Boudabous A, Gtari M (2010) 16S-23S rRNA intergenic spacer region variability in the genus Frankia. Microb Ecol 60:487–495.  https://doi.org/10.1007/s00248-010-9641-6 CrossRefGoogle Scholar
  11. Gnerre S et al (2011) High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci USA 108:1513–1518.  https://doi.org/10.1073/pnas.1017351108 CrossRefGoogle Scholar
  12. 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 Micr 57:81–91.  https://doi.org/10.1099/ijs.0.64483-0 CrossRefGoogle Scholar
  13. Gtari M et al (2015) Cultivating the uncultured: growing the recalcitrant cluster-2 Frankia strains. Sci Rep-UK.  https://doi.org/10.1038/srep13112 Google Scholar
  14. Ktari A et al (2017a) Host plant compatibility shapes the proteogenome of Frankia coriariae. Front Microbiol.  https://doi.org/10.3389/fmicb.2017.00720 Google Scholar
  15. Ktari A, Nouioui I, Furnholm T, Swanson E, Ghodhbane-Gtari F, Tisa LS, Gtari M (2017b) Permanent draft genome sequence of Frankia sp NRRL B-16219 reveals the presence of canonical nod genes, which are highly homologous to those detected in Candidatus Frankia Dg1 genome. Stand Genomic Sci.  https://doi.org/10.1186/s40793-017-0261-3 Google Scholar
  16. Markowitz VM et al (2006) The integrated microbial genomes (IMG) system. Nucleic Acids Res 34:D344–D348.  https://doi.org/10.1093/nar/gkj024 CrossRefGoogle Scholar
  17. Markowitz VM, Mavromatis K, Ivanova NN, Chen IMA, Chu K, Kyrpides NC (2009) IMG ER: a system for microbial genome annotation expert review and curation. Bioinformatics 25:2271–2278.  https://doi.org/10.1093/bioinformatics/btp393 CrossRefGoogle Scholar
  18. Meier-Kolthoff JP, Auch AF, Klenk HP, Goker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform.  https://doi.org/10.1186/1471-2105-14-60 Google Scholar
  19. Murry MA, Fontaine MS, Torrey JG (1984) Growth kinetics and nitrogenase induction in Frankia Sp ArI3 grown in batch culture. Plant Soil 78:61–78.  https://doi.org/10.1007/Bf02277840 CrossRefGoogle Scholar
  20. Nguyen TV et al (2016) An assemblage of Frankia Cluster II strains from California contains the canonical nod genes and also the sulfotransferase gene nodH. BMC Genom.  https://doi.org/10.1186/s12864-016-3140-1 Google Scholar
  21. Normand P et al (1996) Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae. Int J Syst Bacteriol 46:1–9CrossRefGoogle Scholar
  22. Normand P, Benson DR, Berry AM, Tisa LS (2014) Family Frankiaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryote—Actinobacteria, Springer, Berlin, pp 339–356.  https://doi.org/10.1007/978-3-30138-4_183
  23. Nouioui I, Ghodhbane-Gtari F, Beauchemin NJ, Tisa LS, Gtari M (2011) Phylogeny of members of the Frankia genus based on gyrB, nifH and glnII sequences. Anton Leeuw Int J G 100:579–587.  https://doi.org/10.1007/s10482-011-9613-y CrossRefGoogle Scholar
  24. Nouioui I, Sbissi I, Ghodhbane-Gtari F, Benbrahim KF, Normand P, Gtari M (2013) First report on the occurrence of the uncultivated cluster 2 Frankia microsymbionts in soil outside the native actinorhizal host range area. J Biosci 38:695–698.  https://doi.org/10.1007/s12038-013-9366-z CrossRefGoogle Scholar
  25. Nouioui I, Ghodhbane-Gtari F, Rohde M, Klenk HP, Gtari M (2017) Frankia coriariae sp nov., an infective and effective microsymbiont isolated from Coriaria japonica. Int J Syst Evol Microbiol 67:1266–1270.  https://doi.org/10.1099/ijsem.0.001797 CrossRefGoogle Scholar
  26. Persson T et al (2011) Genome sequence of “Candidatus Frankia datiscae” Dg1, the uncultured microsymbiont from nitrogen-fixing root nodules of the Dicot Datisca glomerata. J Bacteriol 193:7017–7018.  https://doi.org/10.1128/Jb.06208-11 CrossRefGoogle Scholar
  27. Persson T et al (2015) Candidatus Frankia datiscae Dg1, the actinobacterial microsymbiont of Datisca glomerata expresses the Canonical nod Genes nodABC in symbiosis with Its host plant. Plos ONE 10:e0127630.  https://doi.org/10.1371/journal.pone.0127630 CrossRefGoogle Scholar
  28. Seto H, Kuzuyama T (1999) Bioactive natural products with carbon-phosphorus bonds and their biosynthesis. Nat Prod Rep 16:589–596.  https://doi.org/10.1039/A809398i CrossRefGoogle Scholar
  29. 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.  https://doi.org/10.1093/molbev/msr121 CrossRefGoogle Scholar
  30. Tisa LS, Oshone R, Sarkar I, Ktari A, Sen A, Gtari M (2016) Genomic approaches toward understanding the actinorhizal symbiosis: an update on the status of the Frankia genomes. Symbiosis 70:5–16.  https://doi.org/10.1007/s13199-016-0390-2 CrossRefGoogle Scholar
  31. Udwary DW et al (2011) Significant natural product biosynthetic potential of actinorhizal symbionts of the genus Frankia, as revealed by comparative genomic and proteomic analyses. Appl Environ Microb 77:3617–3625.  https://doi.org/10.1128/aem.00038-11 CrossRefGoogle Scholar
  32. Wang Y, Coleman-Derr D, Chen GP, Gu YQ (2015) OrthoVenn: a web server for genome wide comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res 43:W78–W84.  https://doi.org/10.1093/nar/gkv487 CrossRefGoogle Scholar
  33. Weber T et al (2015) antiSMASH 3.0-a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res 43:W237–W243.  https://doi.org/10.1093/nar/gkv437 CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Institut National des Sciences Appliquées et de TechnologieUniversité CarthageTunisTunisia
  2. 2.Laboratoire Microorganismes et Biomolécules ActivesUniversité Tunis El Manar (FST)TunisTunisia
  3. 3.Department of Molecular, Cellular, and Biomedical SciencesUniversity of New HampshireDurhamUSA

Personalised recommendations