Skip to main content
NCBI home page
Genome Announcements logoLink to Genome Announcements
. 2016 Apr 7;4(2):e00265-16. doi: 10.1128/genomeA.00265-16

Permanent Draft Genome Sequence for Frankia sp. Strain CeD, a Nitrogen-Fixing Actinobacterium Isolated from the Root Nodules of Casuarina equistifolia Grown in Senegal

Mariama Ngom a,b,c,d, Rediet Oshone a, Sheldon G Hurst IV a, Feseha Abebe-Akele a, Stephen Simpson a, Krystalynne Morris a, Mame Ourèye Sy b,c, Antony Champion b,d,e, W Kelley Thomas a, Louis S Tisa a,✉
PMCID: PMC4824271  PMID: 27056238

Abstract

Frankia strain CeD is a member of Frankia lineage Ib that is able to reinfect plants of the Casuarina families. Here, we report a 5.0-Mbp draft genome sequence with a G+C content of 70.1% and 3,847 candidate protein-encoding genes.

GENOME ANNOUNCEMENT

Members of the genus Frankia are soil-dwelling actinobacteria that are well known for their facultative lifestyle as a plant symbiont of dicotyledonous plants, termed actinorhizal plants (1–3). As ecologically important pioneer community plants, actinorhizal plants are found worldwide in a broad range of ecological and environmental conditions (4). The symbiosis allows actinorhizal plants to colonize harsh environmental terrains.

Based on molecular phylogenetic analysis, four major clusters within the genus are recognized (5–8) and genomes for representatives from each cluster have been sequenced (9–24). Cluster I contains two subclusters: One subcluster (cluster Ia) represents Frankia strains with the ability to infect a wider range of host plants including member of the Betulaceae and Myricaceae families, and the other subcluster (cluster Ib) contains strains limited to Casuarina and Allocasuarina host plants. Members of cluster II infect host plants of the subfamily Dryadoideae (Rosaceae), the families Coriariaceae and Datiscaceae, and the genus Ceanothus (Rhamnaceae). Members of cluster III are the most promiscuous and are infective on Eleagnaceae, Rhamnaceae, Myricaceae, Gynmmostoma (Casuarinaceae), and occasionally Alnus. The fourth Frankia lineage consists of the “atypical” strains which are unable to reinfect actinorhizal host plants or form ineffective root nodule structures that are unable to fix nitrogen.

Under tropic and subtropic conditions, fast growing and highly tolerant trees from the family Casuarinaceae have been used as windbreaks, dune stabilizers, fuel wood, and soil regeneration and these actinorhizal plants grow well under the harsh conditions including high salinity (25). Frankia sp. strain CeD was isolated from root nodules of Casuarina equisetifolia growing in Senegal and effectively reinfects its original host plant, Casuarina spp. (26). Frankia sp. strain CeD has been used extensively in infection studies and is well characterized for its host plant interactions (27).

The draft genome of Frankia sp. strain CeD was generated at the Hubbard Genome Center (University of New Hampshire, Durham, NH, USA) using Illumina technology (28) techniques. A standard Illumina shotgun library was constructed and sequenced using the Illumina HiSeq2000 platform, which generated 29,802,574 reads (260 bp insert size) totaling 4,381.0 Mbp. The Illumina sequence data were assembled using CLC Genomics Workbench (8.0.1) and AllPaths-LG (version r41043) (29). The final draft assembly for Frankia CeD consisted of 154 contigs in 120 scaffolds containing a total sequence of 5,004,600 bp with an N50 contig size of 73.6 kb and G+C content of 70.1%. This assembled draft resulted in 703× coverage of the genome.

The assembled Frankia sp. strain CeD genome was annotated via the Integrated Microbial Genomes (IMG) platform developed by the Joint Genome Institute, Walnut Creek, CA, USA (30, 31) and resulted in 3,847 candidate protein-encoding genes, 45 tRNA, and 2 rRNA regions.

Nucleotide sequence accession numbers.

This whole-genome shotgun project has been deposited at DDBJ/EMBL/GenBank under the accession number JPGU00000000. The version described in this paper is version JPGU01000000.

ACKNOWLEDGMENTS

Partial funding was provided by the New Hampshire Agricultural Experiment Station. This work was also supported by the USDA National Institute of Food and Agriculture Hatch 022821 (L.S.T.), Agriculture and Food Research Initiative Grant 2015-67014-22849 from the USDA National Institute of Food and Agriculture (L.S.T.), and the College of Life Science and Agriculture at the University of New Hampshire–Durham. M.N. was supported by an ARTS (Allocation de Recherche pour une Thèse au Sud) Ph.D. grant from the IRD (Institut de recherche pour le développement). Sequencing was performed on an Illumina HiSeq2500 purchased with NSF MRI grant DBI-1229361to W.K.T.

Footnotes

Citation Ngom M, Oshone R, Hurst SG, IV, Abebe-Akele F, Simpson S, Morris K, Sy MO, Champion A, Thomas WK, Tisa LS. 2016. Permanent draft genome sequence for Frankia sp. strain CeD, a nitrogen-fixing actinobacterium isolated from the root nodules of Casuarina equistifolia grown in Senegal. Genome Announc 4(2):e00265-16. doi:10.1128/genomeA.00265-16.

REFERENCES

  • 1.Chaia EE, Wall LG, Huss-Danell K. 2010. Life in soil by actinorhizal root nodule endophyte Frankia. A review. Symbiosis 51:201–226. doi: 10.1007/s13199-010-0086-y. [DOI] [Google Scholar]
  • 2.Normand P, Benson DR, Berry AM, Tisa LS. 2014. Family Frankiaceae, p. 339–356. In Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (ed), The prokaryote—Actinobacteria, 4th ed. Springer-Verlag Berlin Heidelberg. [Google Scholar]
  • 3.Schwencke J, Carú M. 2001. Advances in actinorhizal symbiosis: host plant-Frankia interactions, biology, and applications in arid land reclamation. A review. Arid Land Res Manag 15:285–327. doi: 10.1080/153249801753127615. [DOI] [Google Scholar]
  • 4.Benson DR, Dawson JO. 2007. Recent advances in the biogeography and genecology of symbiotic Frankia and its host plants. Physiol Plant 130:318–330. doi: 10.1111/j.1399-3054.2007.00934.x. [DOI] [Google Scholar]
  • 5.Normand P, Orso S, Cournoyer B, Jeannin P, Chapelon C, Dawson JO, Evtushenko L, Misra AK. 1996. Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae. Int J Syst Bacteriol 46:1–9. doi: 10.1099/00207713-46-1-1. [DOI] [PubMed] [Google Scholar]
  • 6.Cournoyer B, Lavire C. 1999. Analysis of Frankia evolution radiation using glnII sequences. FEMS Microbiol Lett 177:29–34. [DOI] [PubMed] [Google Scholar]
  • 7.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. Ant Van Leeuw 100:579–587. doi: 10.1007/s10482-011-9613-y. [DOI] [PubMed] [Google Scholar]
  • 8.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. doi: 10.1007/s00248-010-9641-6. [DOI] [PubMed] [Google Scholar]
  • 9.Ghodhbane-Gtari F, Beauchemin N, Bruce D, Chain P, Chen A, Walston Davenport K, Deshpande S, Detter C, Furnholm T, Goodwin L, Gtari M, Han C, Han J, Huntemann M, Ivanova N, Kyrpides N, Land ML, Markowitz V, Mavrommatis K, Nolan M, Nouioui I, Pagani I, Pati A, Pitluck S, Santos CL, Sen A, Sur S, Szeto E, Tavares F, Teshima H, Thakur S, Wall LG, Woyke T, Tisa LS. 2013. Draft genome sequence of Frankia sp. strain CN3, an atypical, noninfective (nod-) ineffective (fix-) isolate from Coriaria nepalensis. Genome Announc 1(2):00085-13. doi: 10.1128/genomeA.00085-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Ghodhbane-Gtari F, Hurst SG IV, Oshone R, Morris K, Abebe-Akele F, Thomas WK, Ktari A, Salem K, Gtari M, Tisa LS. 2014. Draft genome sequence of Frankia sp. strain BMG5.23, a salt-tolerant nitrogen-fixing actinobacterium isolated from the root nodules of Casuarina glauca grown in Tunisia. Genome Announc 2(3):e00520-14. doi: 10.1128/genomeA.00520-14. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Gtari M, Ghodhbane-Gtari F, Nouioui I, Ktari A, Hezbri K, Minouni W, Sbissi I, Ayari A, Sghaier H, Normand P, Tisa LS, Yamanaka T, Boudabous A. 2015. Cultivating the uncultured: growing the recalcitrant cluster-2 Frankia strains. Sci Rep 5:13112. doi: 10.1038/srep13112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Hurst SG IV, Ghodhbane-Gtari F, Oshone R, Morris K, Abebe-Akele F, Thomas WK, Ktari A, Salem K, Mansour S, Gtari M, Tisa LS. 2014. Draft genome sequence of Frankia sp. strain Thr, a nitrogen-fixing actinobacterium isolated from the root nodules of Casuarina cunninghamiana grown in Egypt. Genome Announc 2(3):e00493-14 doi: 10.1128/genomeA.00493-14. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Mansour SR, Oshone R, Hurst SG IV, Morris K, Thomas WK, Tisa LS. 2014. Draft genome sequence of Frankia sp. strain CcI6, a salt-tolerant nitrogen-fixing actinobacterium isolated from the root nodule of Casuarina cunninghamiana. Genome Announc 2(1):e01205-13 doi: 10.1128/genomeA.01205-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N, Bagnarol E, Bassi CA, Berry AM, Bickhart DM, Choisne N, Couloux A, Cournoyer B, Cruveiller S, Daubin V, Demange N, Francino MP, Goltsman E, Huang Y, Kopp OR, Labarre L, Lapidus A, Lavire C, Marechal J, Martinez M, Mastronunzio JE, Mullin BC, Niemann J, Pujic P, Rawnsley T, Rouy Z, Schenowitz C, Sellstedt A, Tavares F, Tomkins JP, Vallenet D, Valverde C, Wall LG, Wang Y, Medigue C, Benson DR. 2007. Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res 17:7–15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Nouioui I, Beauchemin N, Cantor MN, Chen A, Detter JC, Furnholm T, Ghodhbane-Gtari F, Goodwin L, Gtari M, Han C, Han J, Huntemann M, Hua SX, Ivanova N, Kyrpides N, Markowitz V, Mavrommatis K, Mikhailova N, Nordberg HP, Ovchinnikova G. 2013. Draft genome sequence of Frankia sp. strain BMG5.12, a nitrogen-fixing actinobacterium isolated from Tunisian soils. Genome Announc 1(4):e00468-13 doi: 10.1128/genomeA.00468-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Oshone R, Hurst SG IV, Abebe-Akele F, Simpson S, Morris K, Thomas WK, Tisa LS. 2016. Permeant draft genome sequences for two variants of Frankia sp. strain CpI1, the first Frankia strain isolated from the root nodule of Comptonia peregrina. Genome Announc 4(1):e01588-15. doi: 10.1128/genomeA.01588-15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Persson T, Benson DR, Normand P, Vanden Heuvel B, Pujic P, Chertkov O, Teshima H, Bruce DC, Detter C, Tapia R, Han S, Han J, Woyke T, Pitlock S, Pennacchio L, Nolan M, Ivanova N, Pati A, Land ML, Pawlowski K, Berry AM. 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. doi: 10.1128/JB.06208-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Pujic P, Bolotin A, Fournier P, Sorokin A, Lapidus A, Richau KH, Briolay J, Mebarki F, Normand P, Sellstedt A. 2105. Genome sequence of the atypical symbiotic Frankia R43 strain, a nitrogen-fixing and hydrogen-evolving actinobacterium. Genome Announc 3(6):e01387-15. doi: 10.1128/genomeA.01387-15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Sen A, Beauchemin N, Bruce D, Chain P, Chen A, Walston Davenport K, Deshpande S, Detter C, Furnholm T, Ghodhbane-Gtari F, Goodwin L, Gtari M, Han C, Han J, Huntemann M, Ivanova N, Kyrpides N, Land ML, Markowitz V, Mavrommatis K, Nolan M, Nouioui I, Pagani I, Pati A, Pitluck S, Santos CL, Sur S, Szeto E, Tavares F, Teshima H, Thakur S, Wall L, Wishart J, Woyke T, Tisa LS. 2013. Draft genome sequence of Frankia sp. strain QA3, a nitrogen-fixing actinobacterium isolated from the root nodule of Alnus nitida. Genome Announc 1(2):e00103-13. doi: 10.1128/genomeA.00103-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Swanson E, Oshone R, Simpson S, Morris K, Abebe-Akele F, Thomas WK, Tisa TLS. 2015. Draft genome sequence of Frankia sp. strain ACN1ag, a nitrogen-fixing actinobacterium isolated from the root nodule of Alnus glutinosa. Genome Announc 3(6):e01483-15. doi: 10.1128/genomeA.01483-15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Swanson E, Oshone R, Simpson S, Morris K, Abebe-Akele F, Thomas WK, Tisa LS. 2015. Permeant draft genome sequence of Frankia sp. strain AvcI1, a nitrogen-fixing actinobacterium isolated from the root nodule of Alnus viridis ssp. crispa grown in Canada. Genome Announc 3(6):e01511-15. doi: 10.1128/genomeA.01511-15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Tisa LS, Beauchemin N, Gtari M, Sen A, Wall LG. 2013. What stories can the Frankia genomes start to tell us? J Biosci 38:719–726. doi: 10.1007/s12038-013-9364-1. [DOI] [PubMed] [Google Scholar]
  • 23.Tisa LS, Beauchemin N, Cantor MN, Furnholm T, Ghodhbane-Gtari F, Goodwin L, Copeland A, Gtari M, Huntemann M, Ivanova N, Kyrpides N, Markowitz V, Mavrommatis K, Mikhailova N, Nouioui I, Oshone R, Ovchinnikova G, Pagani I, Palaniappan K, Pati A. 2015. Draft genome sequence of Frankia sp. strain DC12, an atypical, noninfective, ineffective isolate from Datisca cannabina. Genome Announc 3(4):e00889-15. doi: 10.1128/genomeA.00889-15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Wall LG, Beauchemin N, Cantor MN, Chaia E, Chen A, Detter JC, Furnholm T, Ghodhbane-Gtari F, Goodwin L, Gtari M, Han C, Han J, Huntemann M, Hua SX, Ivanova N, Kyrpides N, Markowitz V, Mavrommatis K, Mikhailova N, Nordberg HP, Nouioui I, Ovchinnikova G, Pagani I, Pati A, Sen A, Sur S, Szeto E, Thakur S, Wei C-L, Woyke T, Tisa LS. 2013. Draft genome sequence of Frankia sp. strain BCU110501, a nitrogen-fixing actinobacterium isolated from nodules of Discaria trinevis. Genome Announc 1(4):e00503-13 doi: 10.1128/genomeA.00503-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Dommergues YR. 1997. Contribution of actinorhizal plants to tropical soil productivity and rehabilitation. Soil Biol Biochem 29:931–947. doi: 10.1016/S0038-0717(96)00227-1. [DOI] [Google Scholar]
  • 26.Diem HG, Dommergues Y. 1983. The isolation of Frankia from nodules of Casuarina. Can J Bot 61:2822–2825. [Google Scholar]
  • 27.Ngom M, Diagne N, Laplaze L, Champion A, Sy MO. 2 December 2015. Symbiotic ability of diverse Frankia strains on Casuarina glauca plants in hydroponic conditions. Symbiosis. doi: 10.1007/s13199-015-0366-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Bennett S. 2004. Solexa Ltd. Pharmacogenomics 5:433–438. doi: 10.1517/14622416.5.4.433. [DOI] [PubMed] [Google Scholar]
  • 29.Gnerre S, MacCallum I, Przybylski D, Ribeiro FJ, Burton JN, Walker BJ, Sharpe T, Hall G, Shea TP, Sykes S, Berlin AM, Aird D, Costello M, Daza R, Williams L, Nicol R, Gnirke A, Nusbaum C, Lander ES, Jaffe DB. 2011. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci USA 108:1513–1518. doi: 10.1073/pnas.1017351108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Markowitz VM, Korzeniewski F, Palaniappan K, Szeto E, Werner G, Padki A, Zhao XL, Dubchak I, Hugenholtz P, Anderson I, Lykidis A, Mavromatis K, Ivanova N, Kyrpides NC. 2006. The integrated microbial genomes (IMG) system. Nucleic Acids Res 34:D344–D348. doi: 10.1093/nar/gkj024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.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. doi: 10.1093/bioinformatics/btp393. [DOI] [PubMed] [Google Scholar]

Articles from Genome Announcements are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES