The genome of a new Halorubrum distributum strain ICIS4 isolated from the culture of a microalga Dunaliella salina

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

The complete genome sequence of a new strain of the haloarchaeaon Halorubrum distributum ICIS4 was revealed and analyzed. The strain was isolated from a culture of a carotenogenic microalga Dunaliella salina maintained in laboratory conditions for a long period of time. The genome (3.32 Mb) contained 3236 protein-coding genes. Of the 2817 groups of homologous genes, 11 were unique to this strain. In the genome, the genes were revealed, which were responsible for utilization of glycerol and starch and for synthesis of vitamins, pigments, and siderophores. These genes may be involved in formation and maintenance of the association with microalgae. A region similar to the HRPV9 virus and another circular contig similar to a phage of the haloarchaean Haloquadratum walsbyi were revealed in the genome assembly.

Full Text

Restricted Access

About the authors

Е. А. Selivanova

Orenburg Federal Research Center, Ural Branch of RAS

Author for correspondence.
Email: selivanova-81@mail.ru

Institute for Cellular and Intracellular Symbiosis

Russian Federation, Orenburg

А. S. Balkin

Orenburg Federal Research Center, Ural Branch of RAS

Email: selivanova-81@mail.ru

Institute for Cellular and Intracellular Symbiosis

Russian Federation, Orenburg

Yu. А. Khlopko

Orenburg Federal Research Center, Ural Branch of RAS

Email: selivanova-81@mail.ru

Institute for Cellular and Intracellular Symbiosis

Russian Federation, Orenburg

V. Ya. Kataev

Orenburg Federal Research Center, Ural Branch of RAS

Email: selivanova-81@mail.ru

Institute for Cellular and Intracellular Symbiosis

Russian Federation, Orenburg

А. О. Plotnikov

Orenburg Federal Research Center, Ural Branch of RAS

Email: selivanova-81@mail.ru

Institute for Cellular and Intracellular Symbiosis

Russian Federation, Orenburg

References

  1. Немцева Н. В., Селиванова Е. А., Игнатенко М. Е., Шарапова Н. В. Характеристика нового штамма Dunaliella salina (Chlorophyta) и оценка параметров его культивирования // Физиология растений. 2013. Т. 60. С. 561–568.
  2. Nemtseva N. V., Selivanova E. A., Ignatenko M. E., Sharapova N. V. Characterization of a novel Dunaliella salina (Chlorophyta) strain and the assessment of its cultivation parameters // Russ. J. Plant Physiol. 2013. V. 60. P. 529–535.
  3. Соловченко А. Е., Селиванова Е. А., Чеканов К. А., Сидоров Р. А., Немцева Н. В., Лобакова Е. С. Индукция вторичного каротиногенеза у новых галофильных микроводорослей из рода Dunaliella (Chlorophyceae) // Биохимия. 2015. Т. 80. С. 1724–1730.
  4. Solovchenko A. E., Selivanova E. A., Chekanov K. A., Sidorov R. A., Nemtseva N. V., Lobakova E. S. Induction of secondary carotenogenesis in new halophile microalgae from the genus Dunaliella (Chlorophyceae) // Biochemistry (Moscow). 2015. V. 80. P. 1508–1513.
  5. Amin S. A., Green D. H., Hart M. C., Küpper F. C., Sunda W. G., Carrano C. J. Photolysis of iron-siderophore chelates promotes bacterial-algal mutualism // Proc. Natl. Acad. Sci. USA. 2009. V. 106. P. 17071–17076.
  6. Arndt D., Grant J., Marcu A., Sajed T., Pon A., Liang Y., Wishart D. S. PHASTER: a better, faster version of the PHAST phage search tool // Nucleic Acids Res. 2016. V. 44. P. 16–21.
  7. Atanasova N. S., Demina T. A., Shanthi S. N.K.R., Oksanen H. M., Bamford D. H. Extremely halophilic pleomorphic archaeal virus HRPV9 extends the diversity of pleolipoviruses with integrases // Res. Microbiol. 2018. V. 169. P. 500–504.
  8. Bardavid R. E., Khristo P., Oren A. Interrelationships between Dunaliella and halophilic prokaryotes in saltern crystallizer ponds // Extremophiles. 2008. V. 12. P. 5–14.
  9. Bolger A. M., Lohse M., Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data // Bioinformatics. 2014. V. 30. P. 2114–2120.
  10. Cantalapiedra C. P., Hernández-Plaza A., Letunic I., Bork P., Huerta-Cepas J. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale // Mol. Biol. Evol. 2021. V. 38. P. 5825–5829.
  11. Cao J., Ma H. Y., Li H. Y., Wang K. R., Ruan K., Bai L. H. Halomonas socia sp. nov., isolated from high salt culture of Dunaliella salina // Extremophiles. 2013. V. 17. P. 663–668.
  12. Croft M., Lawrence A., Raux-Deery E. Warren M. J., Smith A. G. Algae acquire vitamin B12 through a symbiotic relationship with bacteria // Nature. 2005. V. 438. P. 90–93.
  13. Chun J., Oren A., Ventosa A., Christensen H., Arahal D. R., da Costa M. S., Rooney A. P., Yi H., Xu X.-W., De Meyer S., Trujillo M. E. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes // Int. J. Syst. Evol. Microbiol. 2018. V. 68. P. 461–466.
  14. Delgado-Garcia M., Gómez-Secundino O., Rodríguez J. A., Mateos-Díaz J.C., Muller-Santos M., Aguilar C. N., Camacho-Ruiz R. M. Identification, antioxidant capacity, and matrix metallopeptidase 9 (MMP-9) in silico inhibition of haloarchaeal carotenoids from Natronococcus sp. and Halorubrum tebenquichense // Microorganisms. 2023. V. 11. Art. 2344.
  15. Grossi R., Iliopoulos C. S., Mercas R., Pisanti N., Pissis S. P., Retha A., Vayani F. Circular sequence comparison: algorithms and applications // Algorithms Mol. Biol. 2016. V. 11. P. 1–14.
  16. Gurevich A., Saveliev V., Vyahhi N., Tesler G. QUAST: quality assessment tool for genome assemblies // Bioinformatics. 2013. V. 29. P. 1072–1075.
  17. Infante-Domínguez C., de la Haba R. R., Corral P., Sanchez-Porro C., Arahal D. R., Ventosa A. Genome-based analyses reveal a synonymy among Halorubrum distributum Zvyagintseva and Tarasov 1989; Oren and Ventosa 1996, Halorubrum terrestre Ventosa et al. 2004, Halorubrum arcis Xu et al. 2007 and Halorubrum litoreum Cui et al. 2007. Emended description of Halorubrum distributum Zvyagintseva and Tarasov 1989; Oren and Ventosa 1996 // Int. J. Syst. Evol. Microbiol. 2020. V. 70. P. 1698–1705.
  18. Kanehisa M., Sato Y., Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences // J. Mol. Biol. 2016. V. 428. P. 726–731.
  19. Keerthi S., Koduru U. D., Nittala S. S., Parine N. R. The heterotrophic eubacterial and archaeal co-inhabitants of the halophilic Dunaliella salina in solar salterns fed by Bay of Bengal along south eastern coast of India // Saudi J. Biol. Sci. 2018. V. 25. P. 1411–1419.
  20. Kim J., Na S. I., Kim D., Chun J. UBCG2: Up-to-date bacterial core genes and pipeline for phylogenomic analysis // J. Microbiol. 2021. V. 59. P. 609–615.
  21. Kim D., Park S., Chun J. Introducing EzAAI: a pipeline for high throughput calculations of prokaryotic average amino acid identity // J. Microbiol. 2021. V. 59. P. 476–480.
  22. Le Chevanton M., Garnier M., Bougaran G., Schreiber N., Lukomska E., Bérard J. B., Fouilland E., Bernard O., Cadoret J. P. Screening and selection of growth-promoting bacteria for Dunaliella cultures // Algal Res. 2013. V. 2. P. 212–222.
  23. Lee I., Kim Y. O., Park S. C., Chun J. OrthoANI: an improved algorithm and software for calculating average nucleotide identity // Int. J. Syst. Evol. Microbiol. 2015. V. 66. P. 1100–1103.
  24. Li W., O’Neill K.R., Haft D. H., DiCuccio M., Chetvernin V., Badretdin A., Coulouris G., Chitsaz F., Derbyshire M. K., Durkin A. S., Gonzales N. R., Gwadz M., Lanczycki C. J., Song J. S., Thanki N., Wang J., Yamashita R. A., Yang M., Zheng C., Marchler-Bauer A., Thibaud-Nissen F. RefSeq: expanding the Prokaryotic Genome Annotation Pipeline reach with protein family model curation // Nucleic Acids Res. 2021. V. 8. P. D1020–D1028.
  25. Luk A. W.S., Williams T. J., Erdmann S., Papke R. T., Cavicchioli R. Viruses of Haloarchaea // Life. 2014. V. 4. P. 681–715.
  26. Oren A. Glycerol metabolism in hypersaline environments // Environ. Microbiol. 2017. V. 19. P. 851–863.
  27. Parks D. H., Imelfort M., Skennerton C. T., Hugenholtz P., Tyson G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes // Genome Res. 2015. V. 25. P. 1043–1055.
  28. Selivanova E., Khlopko Y., Plotnikov A. The prokaryotic diversity in cultures of halophilic phototrophic and heterotrophic protists // Studia Universitatis Babes-Bolyai, Biologia. 2019. V. 64. 1. P. 16838.
  29. 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. 2015. V. 31. P. 3210–3212.
  30. Sun J., Lu F., Luo Y., Bie L., Xu L., Wang Y. OrthoVenn3: an integrated platform for exploring and visualizing orthologous data across genomes // Nucleic Acids Res. 2023. V. 51. P. W397–W403.
  31. Wick R. R., Judd L. M., Gorrie C. L., Holt K. E. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads // PLoS Computat. Biol. 2017. V. 13. Art. e1005595.
  32. Williams T. J., Allen M., Tschitschko B., Cavicchioli R. Glycerol metabolism of haloarchaea // Environ. Microbiol. 2017. V. 19. P. 864‒877.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig. 1. Venn diagram showing unique and orthologous gene groups for the genomes of H. distributum ICIS4, H. distributum JCM9100 (GCA_000337055), H. distributum (GCF_000337335), H. litoreum JCM13561 (GCA_000337395), H. terrestre 22502 (GCA_009856455).

Download (133KB)
Indexing metadata
3. Fig. S1. Position of the H. distributum ICIS4 strain on the phylogenetic tree constructed by the maximum likelihood method based on the analysis of the genomes of representatives of the genus Halorubrum using the UBCG2 algorithm (Kim et al., 2021). The gene support index (GSI) levels were calculated based on the construction of 100 alternative gene trees. The Haloferax denitrificans ATCC35960 genome (GCF_000337795) was used as an outgroup.

Download (283KB)
Indexing metadata

Copyright (c) 2024 Russian Academy of Sciences