Halobacterium salinarum storage and rehydration after spray drying and optimization of the processes for preservation of carotenoids

Abstract

Spray drying is appropriate for the preservation of halophilic microorganisms due to the nature of these microorganisms, as they survive in adverse environmental conditions by being encapsulated in salt crystals. Artificial neural networks were in this study used to optimize practically significant spray-drying regimes of the C50-carotenoids producer Halobacterium salinarum. Immediately after drying, the samples contained up to 54% halobacterial biomass and less than 5% moisture, and the level of preservation of carotenoids was 95–97%. The storage of biomass at 4 °C resulted in the gradual degradation of the carotenoids, which reached 58–64% in the best samples after 1 year. A comprehensive study of changes in halobacteria biomass after spray drying and the nature of the damage provided new data on the survival and preservation of cells and biologically active substances in the various spray-drying regimes and at different storage times.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Abbreviations

DMSO:

Dimethyl sulfoxide

ANN:

Artificial neural network

CFU:

Colony forming unit

References

  1. Akolkar AV, Durai D, Desai AJ (2009) Halobacterium sp. SP1(1) as a starter culture for accelerating fish sauce fermentation. J Appl Microbiol 109:44–53. https://doi.org/10.1111/j.1365-2672.2009.04626.x

    PubMed  Google Scholar 

  2. Ananta E, Volkert M, Knorr D (2005) Cellular injuries and storage stability of spray-dried Lactobacillus rhamnosus GG. Int Dairy J 15:399–409. https://doi.org/10.1016/j.idairyj.2004.08.004

    CAS  Article  Google Scholar 

  3. Association of Official Analytical Chemists (2016) Official methods of analysis of AOAC international, 20th edn. AOAC Press, Gaithersburg

    Google Scholar 

  4. Baliga NS, Bjork SJ, Bonneau R, Pan M, Iloanusi C, Kottemann MC, Hood L, DiRuggiero J (2004) Systems level insights into the stress response to UV radiation in the halophilic archaeon Halobacterium NRC-1. Genome Res 14:1025–1035. https://doi.org/10.1101/gr.1993504

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. Behboudi-Jobbehdar S, Soukoulis C, Yonekura L, Fisk I (2013) Optimization of spray-drying process conditions for the production of maximally viable microencapsulated L. acidophilus NCIMB 701748. Dry Technol 31:1274–1283. https://doi.org/10.1080/07373937.2013.788509

    CAS  Article  Google Scholar 

  6. DasSarma S, DasSarma P (2017) Halophiles. In: eLS. Wiley, Chichester, UK, pp 1–13. https://doi.org/10.1002/9780470015902.a0000394.pub4

    Google Scholar 

  7. DasSarma P, Coker JA, Huse V, DasSarma S (2010) Halophiles, industrial applications. In: Flickinger MC (ed) Encyclopedia of industrial biotechnology: bioprocess, bioseparation and cell technology. Wiley, Hoboken, NJ, pp 1–43

    Google Scholar 

  8. Desmond C, Stanton C, Fitzgerald GF, Collins K, Ross RP (2001) Environmental adaptation of probiotic lactobacilli towards improvement of performance during spray drying. Int Dairy J 11:801–808. https://doi.org/10.1016/S0958-6946(01)00121-2

    Article  Google Scholar 

  9. Dummer AM, Bonsall JC, Cihla JB, Lawry SM, Johnson GC, Peck RF (2011) Bacterioopsin-mediated regulation of bacterioruberin biosynthesis in Halobacterium salinarum. J Bacteriol 193:5658–5667. https://doi.org/10.1128/JB.05376-11

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. El-Agamey A, Lowe GM, McGarvey DJ, Mortensen A, Phillip DM, Truscott TG, Young AJ (2004) Carotenoid radical chemistry and antioxidant/pro-oxidant properties. Arch Biochem Biophys 430:37–48. https://doi.org/10.1016/j.abb.2004.03.007

    CAS  Article  PubMed  Google Scholar 

  11. Fendrihan S, Bérces A, Lammer H, Musso M, Rontó G, Polacsek TK, Holzinger A, Kolb C, Stan-Lotter H (2009) Investigating the effects of simulated Martian ultraviolet radiation on Halococcus dombrowskii and other extremely halophilic archaebacteria. Astrobiology 9:104–112. https://doi.org/10.1089/ast.2007.0234

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. Fu W-Y, Etzel MR (1995) Spray drying of Lactococcus lactis ssp. lactis C2 and cellular injury. J Food Sci 60:195–200. https://doi.org/10.1111/j.1365-2621.1995.tb05636.x

    CAS  Article  Google Scholar 

  13. Ghandi A, Powell IB, Howes T, Chen XD, Adhikari B (2012) Effect of shear rate and oxygen stresses on the survival of Lactococcus lactis during the atomization and drying stages of spray drying: a laboratory and pilot scale study. J Food Eng 113:194–200. https://doi.org/10.1016/j.jfoodeng.2012.06.005

    CAS  Article  Google Scholar 

  14. Goh F, Jeon YJ, Barrow K, Neilan BA, Burns BP (2011) Osmoadaptive strategies of the archaeon Halococcus hamelinensis isolated from a hypersaline stromatolite environment. Astrobiology 11:529–536. https://doi.org/10.1089/ast.2010.0591

    CAS  Article  PubMed  Google Scholar 

  15. Golowczyc MA, Silva J, Abraham AG, De Antoni GL, Teixeira P (2010) Preservation of probiotic strains isolated from kefir by spray drying. Lett Appl Microbiol 50:7–12. https://doi.org/10.1111/j.1472-765X.2009.02759.x

    CAS  Article  PubMed  Google Scholar 

  16. Gong P, Zhang L, Han X, Shigwedha N, Song W, Yi H, Du M, Cao C (2014) Injury mechanisms of lactic acid bacteria starter cultures during spray drying: a review. Drying Technol 32:793–800. https://doi.org/10.1080/07373937.2013.860458

    CAS  Article  Google Scholar 

  17. Gruber C, Legat A, Pfaffenhuemer M, Radax C, Weidler G, Busse HJ, Stan-Lotter H (2004) Halobacterium noricense sp. nov., an archaeal isolate from a bore core of an alpine Permian salt deposit, classification of Halobacterium sp. NRC-1 as a strain of H. salinarum and emended description of H. salinarum. Extremophiles 8:431–439. https://doi.org/10.1007/s00792-004-0403-6

    CAS  Article  PubMed  Google Scholar 

  18. Jaakkola ST, Zerulla K, Guo Q, Liu Y, Ma H, Yang C, Bamford DH, Chen X, Soppa J, Oksanen HM (2014) Halophilic archaea cultivated from surface sterilized middle-late Eocene rock salt are polyploid. PLoS One 9:e110533. https://doi.org/10.1371/journal.pone.0110533

    Article  PubMed  PubMed Central  Google Scholar 

  19. Kalenov SV, Baurina MM, Skladnev DA, Kuznetsov AY (2016) High-effective cultivation of Halobacterium salinarum providing with bacteriorhodopsin production under controlled stress. J Biotechnol 233:211–218. https://doi.org/10.1016/j.jbiotec.2016.07.014

    CAS  Article  PubMed  Google Scholar 

  20. Kochish II, Naidenskiy MS, Totoevva ME (2008) Efficacy of the immunostimulating Baxinum-vet preparation poultry (article in Russian). Poult Chick Prod 5:29–31

    Google Scholar 

  21. Kosanke JW, Osburn RM, Shuppe GI, Smith RS (1992) Slow rehydration improves the recovery of dried bacterial populations. Can J Microbiol 38:520–525. https://doi.org/10.1139/m92-086

    CAS  Article  PubMed  Google Scholar 

  22. Kottemann M, Kish A, Iloanusi C, Bjork S, DiRuggiero J (2005) Physiological responses of the halophilic archaeon Halobacterium sp. strain NRC1 to desiccation and gamma irradiation. Extremophiles 9:219–227. https://doi.org/10.1007/s00792-005-0437-4

    CAS  Article  PubMed  Google Scholar 

  23. Lavari L, Ianniello R, Páez R, Zotta T, Cuatrin A, Reinheimer J, Parente E, Vinderola G (2015) Growth of Lactobacillus rhamnosus 64 in whey permeate and study of the effect of mild stresses on survival to spray drying. LWT Food Sci Technol 63:322–330. https://doi.org/10.1016/j.lwt.2015.03.066

    CAS  Article  Google Scholar 

  24. Leach G, Oliveira G, Morais R (1998) Spray-drying of Dunaliella salina to produce a β-carotene rich powder. J Ind Microbiol Biotechnol 20:82–85. https://doi.org/10.1038/sj.jim.2900485

    CAS  Article  Google Scholar 

  25. López-Cortés A, Ochoa JL (1998) The biological significance of Halobacteria on nucleation and sodium chloride crystal growth. Stud Surf Sci Catal 120:903–923. https://doi.org/10.1016/S0167-2991(99)80384-X

    Article  Google Scholar 

  26. Margesin R, Schinner F (2001) Potential of halotolerant and halophilic microorganisms for biotechnology. Extremophiles 5:73–83. https://doi.org/10.1007/s007920100184

    CAS  Article  PubMed  Google Scholar 

  27. Morgan CA, Herman N, White PA, Vesey G (2006) Preservation of micro-organisms by drying; a review. J Microbiol Methods 66:183–193. https://doi.org/10.1016/j.mimet.2006.02.017

    CAS  Article  PubMed  Google Scholar 

  28. Oren A (2002) Halophilic microorganisms and their environments. Kluwer Academic Publishers, Dordrecht, The Netherlands, p 575. https://doi.org/10.1007/0-306-48053-0

    Google Scholar 

  29. Oren A (2016) Life in hypersaline environments. In: Hurst CJ (ed) Their world: a diversity of microbial environments. Springer International Publishing, Cham, pp 301–339

    Google Scholar 

  30. Peighambardoust SH, Golshan Tafti A, Hesari J (2011) Application of spray drying for preservation of lactic acid starter cultures: a review. Trends Food Sci Technol 22:215–224. https://doi.org/10.1016/j.tifs.2011.01.009

    CAS  Article  Google Scholar 

  31. Raposo MFJ, Morais AMMB, Morais RMSC (2012) Effects of spray-drying and storage on astaxanthin content of Haematococcus pluvialis biomass. World J Microbiol Biotechnol 28:1253–1257. https://doi.org/10.1007/s11274-011-0929-6

    CAS  Article  PubMed  Google Scholar 

  32. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. Rodrigo-Baños M, Garbayo I, Vílchez C, Bonete MJ, Martínez-Espinosa RM (2015) Carotenoids from Haloarchaea and their potential in biotechnology. Mar Drugs 13:5508–5532. https://doi.org/10.3390/md13095508

    Article  PubMed  PubMed Central  Google Scholar 

  34. Sakane T, Fukuda I, Itoh T, Yokota A (1992) Long-term preservation of halophilic archaebacteria and thermoacidophilic archaebacteria by liquid drying. J Microbiol Methods 16:281–287. https://doi.org/10.1016/0167-7012(92)90080-N

    Article  Google Scholar 

  35. Salin ML, Brown-Peterson NJ (1993) Dealing with active oxygen intermediates: a halophilic perspective. Cell Mol Life Sci 49:523–529. https://doi.org/10.1007/BF01955155

    CAS  Article  Google Scholar 

  36. Samborska K, Witrowa-Rajchert D, Gonçalves A (2005) Spray-drying of α-amylase—the effect of process variables on the enzyme inactivation. Dry Technol 23:941–953. https://doi.org/10.1081/DRT-200054243

    CAS  Article  Google Scholar 

  37. Schuck P, Dolivet A, Méjean S, Hervé C, Jeantet R (2013) Spray drying of dairy bacteria: new opportunities to improve the viability of bacteria powders. Int Dairy J 31:12–17. https://doi.org/10.1016/j.idairyj.2012.01.006

    Article  Google Scholar 

  38. Stan-Lotter H, Fendrihan S (2013) Survival strategies of halophilic oligotrophic and desiccation resistant prokaryotes. In: Seckbach J, Oren A, Stan-Lotter H (eds) Polyextremophiles. Life under multiple form of stress, Springer, Dordrecht, The Netherlands, pp 233–248. https://doi.org/10.1007/978-94-007-6488-0

    Google Scholar 

  39. Stan-Lotter H, Radax C, Gruber C, Legat A, Pfaffenhuemer M, Wieland H, Leuko S, Weidler G, Kömle N, Kargl G (2002) Astrobiology with haloarchaea from Permo-Triassic rock salt. Int J Astrobiol 1:S1473550403001307. https://doi.org/10.1017/S1473550403001307

    Article  Google Scholar 

  40. Staroselov MA, Basova NY, Skhatum AK, Fedorov YuE, Pachina VV, Markov AN (2016) Effect of prebiotic Baxinum-vet on the intestinal microbiocenosis of newborn calves (article in Russian). Russ J Probl Vet Sanit Hyg Ecol 1:72–75

    Google Scholar 

  41. Teixeira P, Castro H, Kirby R (1995) Spray drying as a method for preparing concentrated cultures of Lactobacillus bulgaricus. J Appl Bacteriol 78:456–462. https://doi.org/10.1111/j.1365-2672.1995.tb03433.x

    Article  Google Scholar 

  42. Teixeira P, Castro H, Kirby R (1996) Evidence of membrane lipid oxidation of spray-dried Lactobacillus bulgaricus during storage. Lett Appl Microbiol 22:34–38. https://doi.org/10.1111/j.1472-765X.1996.tb01103.x

    CAS  Article  Google Scholar 

  43. Tindall BJ (1991) Cultivation and preservation of members of the family Halobacteriaceae. World J Microbiol Biotechnol 7:95–98. https://doi.org/10.1007/BF02310924

    CAS  Article  PubMed  Google Scholar 

  44. Vasil’ev IK (2007) Baxinum (book in Russian). Nikopharm, Moscow

    Google Scholar 

Download references

Acknowledgements

The work is financially supported with the Grant of Russian Science Foundation No. 16-19-10469.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Sergei V. Kalenov.

Additional information

Communicated by A. Oren.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1969 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kalenov, S.V., Gordienko, M.G., Murzina, E.D. et al. Halobacterium salinarum storage and rehydration after spray drying and optimization of the processes for preservation of carotenoids. Extremophiles 22, 511–523 (2018). https://doi.org/10.1007/s00792-018-1013-z

Download citation

Keywords

  • Halobacterium salinarum
  • Spray drying
  • Carotenoids
  • Halophiles, artificial neural network