Skip to main content
SpringerLink
Log in

Diversity of Bacteria Cultured from Arid Soils and Sedimentary Rocks under Conditions of Available Water Deficiency

  • TAXONOMIC AND FUNCTIONAL DIVERSITY OF SOIL MICROBIOMES
  • Published:
Eurasian Soil Science Aims and scope Submit manuscript

Abstract

The diversity of bacteria cultured from the soil of the Negev Desert (Israel, sample SN2) and from the sedimentary rock of the Sahara Desert (Tunisia, sample Alg) has been studied. To assess the ability of bacteria to metabolism at different moisture availability and to reveal bacterial diversity more completely, the culturing was performed on R2A medium with addition of glycerol to achieve a particular level of water activity (Aw) in the range from 1.0 to 0.9 (with an interval of 0.01 Aw). After the incubation, unique morphotypes of cultured bacteria were isolated, described, identified by 16S rRNA sequencing, and tested for the ability to grow in the Aw gradient in pure cultures. After incubation and isolation, 355 strains were identified and tested. The cultured bacteria were found at Aw = 0.95 and higher. With a decrease in Aw from 1 to 0.95, the number of cultured bacteria dropped from 105 and 107 CFU/g in samples SN2 and Alg, respectively, to 2 × 104 CFU/g in both samples. As a result of culturing, representatives of 34 genera of bacteria mainly assigned to the phylum Actinobacteria were isolated; the Arthrobacter, Kocuria, and Pseudarthrobacter genera predominated. We also revealed 38 strains characterized by low similarity of nucleotide sequences with databases, which were probably representatives of previously undescribed species of Agrococcus, Arthrobacter, Bacillus, Brachybacterium, Cellulomonas, Conyzicola, Kocuria, Microbacterium, Okibacterium, Rathayibacter, and Sphingomonas genera. Testing of the strains for their ability to grow in pure culture in a gradient of Aw enabled us to reveal 18 strains of Arthrobacter, Kocuria, Brachybacterium, Serratia, and Leucobacter genera capable of growing at Aw = 0.91. The study confirms that desert soils and rocks are a depository of previously undescribed bacterial species and may also be a valuable source of biotechnologically promising strains.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

REFERENCES

  1. A. A. Belov, V. S. Cheptsov, and L. V. Lysak, Methods for Identifying Soil Microorganisms (MAKS Press, Moscow, 2020) [in Russian].

    Google Scholar 

  2. R. N. Albdaiwi, H. Khyami-Horani, J. Y. Ayad, K. M. Alananbeh, and R. Al-Sayaydeh, “Isolation and characterization of halotolerant plant growth promoting rhizobacteria from durum wheat (Triticum turgidum subsp. durum) cultivated in saline areas of the dead sea region,” Front. Microbiol. 10, 1639 (2019). https://doi.org/10.3389/fmicb.2019.01639

    Article  Google Scholar 

  3. A. A. Belov, V. S. Cheptsov, and E. A. Vorobyova, “Soil bacterial communities of Sahara and Gibson deserts: Physiological and taxonomical characteristics,” AIMS Microbiol. 4 (4), 685 (2018). https://doi.org/10.3934/microbiol.2018.4.685

    Article  Google Scholar 

  4. A. A. Belov, V. S. Cheptsov, E. A. Vorobyova, N. A. Manucharova, and Z. S. Ezhelev, “Stress-tolerance and taxonomy of culturable bacterial communities isolated from a central Mojave Desert soil sample,” Geosciences 9 (4), 166 (2019). https://doi.org/10.3390/geosciences9040166

    Article  Google Scholar 

  5. A. A. Belov, V. S. Cheptsov, N. A. Manucharova, and Z. S. Ezhelev, “Bacterial communities of Novaya Zemlya archipelago ice and permafrost,” Geosciences 10 (2), 67 (2020). https://doi.org/10.3390/geosciences10020067

    Article  Google Scholar 

  6. M. A. Bianchi and A. J. Bianchi, “Statistical sampling of bacterial strains and its use in bacterial diversity measurement,” Microb. Ecol. 8 (1), 61–69 (1982). https://doi.org/10.1007/BF02011462

    Article  Google Scholar 

  7. H. Bose and T. Satyanarayana, “Microbial carbonic anhydrases in biomimetic carbon sequestration for mitigating global warming: prospects and perspectives,” Front. Microbiol. 8, 1615 (2017). https://doi.org/10.3389/fmicb.2017.01615

    Article  Google Scholar 

  8. A. Brown, “Microbial water stress,” Bacteriol. Rev. 40 (4), 803–846 (1976). https://doi.org/10.1128/br.40.4.803-846.1976

    Article  Google Scholar 

  9. A. T. Bull, “Actinobacteria of the extremobiosphere,” in Extremophiles Handbook, Ed. by K. Horikoshi (Springer, 2011), pp. 1203–1240. https://doi.org/10.1007/978-4-431-53898-1

  10. L. Cervenka, M. Vytrasova, D. Jelinek, and P. Brezina, “Determination of minimum water activity values for the survival of bacteria in a culture medium,” Bull. Food Res. 41 (1), 59–68 (2002). https://agris.fao.org/agris-search/search.do?recordID=SK2002000296

  11. A. Chanal, V. Chapon, K. Benzerara, M. Barakat, R. Christen, W. Achouak, and T. Heulin, “The desert of Tataouine: an extreme environment that hosts a wide diversity of microorganisms and radiotolerant bacteria,” Environ. Microbiol. 8 (3), 514–525 (2006). https://doi.org/10.1111/j.1462-2920.2005.00921.x

    Article  Google Scholar 

  12. M. S. Chen, F. N. Li, X. H. Chen, X. R. Yan, and L. Tuo, “Brachybacterium halotolerans sp. nov., a halotolerant, endophytic actinomycete isolated from branch of Bruguiera gymnoirhiza,” Antonie van Leeuwenhoek 114 (6), 875–884 (2021). https://doi.org/10.1007/s10482-021-01565-z

    Article  Google Scholar 

  13. V. S. Cheptsov, E. A. Vorobyova, N. A. Manucharova, M. V. Gorlenko, A. K. Pavlov, M. A. Vdovina, and S. A. Bulat, “100 kGy gamma-affected microbial communities within the ancient Arctic permafrost under simulated Martian conditions,” Extremophiles 21 (6), 1057–1067 (2017). https://doi.org/10.1007/s00792-017-0966-7

    Article  Google Scholar 

  14. V. Cheptsov, E. Vorobyova, A. Belov, A. Pavlov, D. Tsurkov, V. Lomasov, and S. Bulat, “Survivability of soil and permafrost microbial communities after irradiation with accelerated electrons under simulated Martian and open space conditions,” Geosciences 8 (8), 298 (2018). https://doi.org/10.3390/geosciences8080298

    Article  Google Scholar 

  15. J. Chun, A. Oren, A. Ventosa, H. Christensen, D. R. Arahal, M. S. Costa, and M. E. Trujillo, “Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes,” Int. J. Syst. Evol. Microbiol. 68 (1), 461–466 (2018). https://doi.org/10.1099/ijsem.0.002516

    Article  Google Scholar 

  16. M. M. Cox and J. R. Battista, “Deinococcus radiodurans – the consummate survivor,” Nat. Rev. Microbiol. 3 (11), 882–892 (2005). https://doi.org/10.1038/nrmicro1264

    Article  Google Scholar 

  17. A. Degré, M. J. van der Ploeg, T. Caldwell, and H. P. Gooren, “Comparison of soil water potential sensors: a drying experiment,” Vadose Zone J. 16 (4), 1–8 (2017). https://doi.org/10.2136/vzj2016.08.0067

    Article  Google Scholar 

  18. M. Dieser, M. Greenwood, and C. M. Foreman, “Carotenoid pigmentation in Antarctic heterotrophic bacteria as a strategy to withstand environmental stresses,” Arct., Antarct., Alp. Res. 42 (4), 396–405 (2010). https://doi.org/10.1657/1938-4246-42.4.396

    Article  Google Scholar 

  19. K. P. Drees, J. W. Neilson, J. L. Betancourt, J. Quade, D. A. Henderson, B. M. Pryor, and R. M. Maier, “Bacterial community structure in the hyperarid core of the Atacama Desert, Chile,” Appl. Environ. Microbiol. 72 (12), 7902–7908 (2006). https://doi.org/10.1128/AEM.01305-06

    Article  Google Scholar 

  20. G. I. El-Registan, A. L. Mulyukin, Y. A. Nikolaev, N. E. Suzina, V. F. Gal’chenko, and V. I. Duda, “Adaptogenic functions of extracellular autoregulators of microorganisms,” Microbiology 75 (4), 380–389 (2006). https://doi.org/10.1134/S0026261706040035

    Article  Google Scholar 

  21. A. J. Fontana Jr., “Minimum water activity limits for growth of microorganisms,” Water Act. Foods. 406, 571–572 (2020). https://doi.org/10.1002/9781118765982

    Article  Google Scholar 

  22. M. Goodfellow, I. Nouioui, R. Sanderson, F. Xie, and A. T. Bull, “Rare taxa and dark microbial matter: novel bioactive actinobacteria abound in Atacama Desert soils,” Antonie van Leeuwenhoek 111 (8), 1315–1332 (2018). https://doi.org/10.1007/s10482-018-1088-7

    Article  Google Scholar 

  23. W. D. Grant, “Life at low water activity,” Philos. Trans. R. Soc. London. Ser. B: Biol. Sci. 359 (1448), 1249–1267 (2004). https://doi.org/10.1098/rstb.2004.1502

    Article  Google Scholar 

  24. N. Gunde-Cimerman, A. Plemenitaš, and A. Oren, “Strategies of adaptation of microorganisms of the three domains of life to high salt concentrations,” FEMS Microbiol. Rev. 42 (3), 353–375 (2018). https://doi.org/10.1093/femsre/fuy009

    Article  Google Scholar 

  25. W. Huang, E. Ertekin, T. Wang, L. Cruz, M. Dailey, J. DiRuggiero, and D. Kisailus, “Mechanism of water extraction from gypsum rock by desert colonizing microorganisms,” Proc. Natl. Acad. Sci. U. S. A. 117 (20), 10681–10687 (2020). https://doi.org/10.1073/pnas.2001613117

    Article  Google Scholar 

  26. N. Ishii, S. Fuma, K. Tagami, S. Honma–Takeda, and S. Shikano, “Responses of the bacterial community to chronic gamma radiation in a rice paddy ecosystem,” Int. J. Radiat. Biol. 87 (7), 663–672 (2011). https://doi.org/10.3109/09553002.2010.549534

    Article  Google Scholar 

  27. R. Karan, M. D. Capes, and S. DasSarma, “Function and biotechnology of extremophilic enzymes in low water activity,” Aquat. Biosyst. 8 (1), 1–15 (2012). https://doi.org/10.1186/2046-9063-8-4

    Article  Google Scholar 

  28. M. Köberl, H. Muller, E. M. Ramadan, and G. Berg, “Desert farming benefits from microbial potential in arid soils and promotes diversity and plant health,” PLoS One 6 (9), e24452 (2011). https://doi.org/10.1371/journal.pone.0024452

    Article  Google Scholar 

  29. E. D. Lester, M. Satomi, and A. Ponce, “Microflora of extreme arid Atacama Desert soils,” Soil Biol. Biochem. 39 (2), 704–708 (2007). https://doi.org/10.1016/j.soilbio.2006.09.020

    Article  Google Scholar 

  30. R. Margesin and T. Collins, “Microbial ecology of the cryosphere (glacial and permafrost habitats): current knowledge,” Appl. Microbiol. Biotechnol. 103 (6), 2537–2549 (2019). https://doi.org/10.1007/s00253-019-09631-3

    Article  Google Scholar 

  31. D. T. McKnight, R. Huerlimann, D. S. Bower, L. Schwarzkopf, R. A. Alford, and K. R. Zenger, “Methods for normalizing microbiome data: an ecological perspective,” Methods Ecol. Evol. 10 (3), 389–400 (2019). https://doi.org/10.1111/2041-210X.13115

    Article  Google Scholar 

  32. F. Mohammadipanah and J. Wink, “Actinobacteria from arid and desert habitats: diversity and biological activity,” Front. Microbiol. 6, 1541 (2016). https://doi.org/10.3389/fmicb.2015.01541

    Article  Google Scholar 

  33. E. Molina–Menor, H. Gimeno–Valero, J. Pascual, J. Peretó, and M. Porcar, “High culturable bacterial diversity from a European desert: the Tabernas desert,” Front. Microbiol. 11, 583120 (2021). https://doi.org/10.3389/fmicb.2020.583120

    Article  Google Scholar 

  34. F. E. Moyano, S. Manzoni, and C. Chenu, “Responses of soil heterotrophic respiration to moisture availability: An exploration of processes and models,” Soil Biol. Biochem. 59, 72–85 (2013). https://doi.org/10.1016/j.soilbio.2013.01.002

    Article  Google Scholar 

  35. M. Musilova, G. Wright, J. M. Ward, and L. R. Dartnell, “Isolation of radiation-resistant bacteria from Mars analog Antarctic Dry Valleys by preselection, and the correlation between radiation and desiccation resistance,” Astrobiology 15 (12), 1076–1090 (2015). https://doi.org/10.1089/ast.2014.1278

    Article  Google Scholar 

  36. A. Nafis, A. Raklami, N. Bechtaoui, F. El Khalloufi, A. El Alaoui, B. R. Glick, and L. Hassani, “Actinobacteria from extreme niches in morocco and their plant growth-promoting potentials,” Diversity 11 (8), 139 (2019). https://doi.org/10.3390/d11080139

    Article  Google Scholar 

  37. J. J. NarváezvReinaldo, I. Barba, J. González–López, A. Tunnacliffe, and M. Manzanera, “Rapid method for isolation of desiccation-tolerant strains and xeroprotectants,” Appl. Environ. Microbiol. 76 (15), 5254–5262 (2010). https://doi.org/10.1128/AEM.00855-10

    Article  Google Scholar 

  38. K. Nithya, C. Muthukumar, B. Biswas, N. S. Alharbi, S. Kadaikunnan, J. M. Khaled, and D. Dhanasekaran, “Desert actinobacteria as a source of bioactive compounds production with a special emphases on Pyridine-2, 5-diacetamide a new pyridine alkaloid produced by Streptomyces sp. DA3-7,” Microbiol. Res. 207, 116–133 (2018). https://doi.org/10.1016/j.micres.2017.11.012

    Article  Google Scholar 

  39. C. K. Okoro, R. Brown, A. L. Jones, B. A. Andrews, J. A. Asenjo, M. Goodfellow, and A. T. Bull, “Diversity of culturable actinomycetes in hyper-arid soils of the Atacama Desert, Chile,” Antonie Van Leeuwenhoek 95 (2), 121–133 (2009). https://doi.org/10.1007/s10482-008-9295-2

    Article  Google Scholar 

  40. A. Oren and G. M. Garrity, “Notification that new names of prokaryotes, new combinations, and new taxonomic opinions have appeared in volume 71, part 10 of the IJSEM,” Int. J. Syst. Evol. Microbiol. 72 (1), 005165 (2022). https://doi.org/10.1099/ijsem.0.001620

    Article  Google Scholar 

  41. S. Osman, Z. Peeters, M. T. La Duc, R. Mancinelli, P. Ehrenfreund, and K. Venkateswaran, “Effect of shadowing on survival of bacteria under conditions simulating the Martian atmosphere and UV radiation,” Appl. Environ. Microbiol. 74 (4), 959–970 (2008). https://doi.org/10.1128/AEM.01973-07

    Article  Google Scholar 

  42. I. Pascual, M. C. Antolín, C. García, A. Polo, and M. Sánchez–Díaz, “Effect of water deficit on microbial characteristics in soil amended with sewage sludge or inorganic fertilizer under laboratory conditions,” Bioresour. Technol. 98 (1), 29–37 (2007). https://doi.org/10.1016/j.biortech.2005.11.026

    Article  Google Scholar 

  43. S. Patel, H. N. Jinal, and N. Amaresan, “Isolation and characterization of drought resistance bacteria for plant growth promoting properties and their effect on chilli (Capsicum annuum) seedling under salt stress,” Biocatal. Agric. Biotechnol. 12, 85–89 (2017). https://doi.org/10.1016/j.bcab.2017.09.002

    Article  Google Scholar 

  44. W. Ramakrishna, P. Rathore, R. Kumari, and R. Yadav, “Brown gold of marginal soil: Plant growth promoting bacteria to overcome plant abiotic stress for agriculture, biofuels and carbon sequestration,” Sci. Total Environ. 711, 135062 (2020). https://doi.org/10.1016/j.scitotenv.2019.135062

    Article  Google Scholar 

  45. D. J. Reasoner and E. E. Geldreich, “A new medium for the enumeration and subculture of bacteria from potable water,” Appl. Environ. Microbiol. 49 (1), 1–7 (1985). https://doi.org/10.1128/aem.49.1.1-7.1985

    Article  Google Scholar 

  46. I. Rebelo Romão, A. S. Rodrigues dos Santos, L. Velasco, E. Martínez–Ferri, J. I. Vilchez, and M. Manzanera, “Seed-encapsulation of desiccation-tolerant microorganisms for the protection of maize from drought: phenotyping effects of a new dry bioformulation,” Plants 11 (8), 1024 (2022). https://doi.org/10.3390/plants11081024

    Article  Google Scholar 

  47. D. N. Rietz and R. J. Haynes, “Effects of irrigation-induced salinity and sodicity on soil microbial activity,” Soil Biol. Biochem. 35 (6), 845–854 (2003). https://doi.org/10.1016/S0038-0717(03)00125-1

    Article  Google Scholar 

  48. S. Siebielec, G. Siebielec, A. Klimkowicz–Pawlas, A. Gałazka, J. Grządziel, and T. Stuczynski, “Impact of water stress on microbial community and activity in sandy and loamy soils,” Agronomy 10 (9), 1429 (2020). https://doi.org/10.3390/agronomy10091429

    Article  Google Scholar 

  49. E. Stanaszek–Tomal, “Environmental factors causing the development of microorganisms on the surfaces of national cultural monuments made of mineral building materials,” Coatings 10 (12), 1203 (2020). https://doi.org/10.3390/coatings10121203

    Article  Google Scholar 

  50. A. Stevenson, J. Burkhardt, C. S. Cockell, J. A. Cray, J. Dijksterhuis, M. Fox-Powell, and J. E. Hallsworth, “Multiplication of microbes below 0.690 water activity: implications for terrestrial and extraterrestrial life,” Environ. Microbiol. 17 (2), 257–277 (2015). https://doi.org/10.1111/1462-2920.12598

    Article  Google Scholar 

  51. A. Stevenson and J. E. Hallsworth, “Water and temperature relations of soil Actinobacteria,” Environ. Microbiol. Rep. 6 (6), 744–755 (2014). https://doi.org/10.1111/1758-2229.12199

    Article  Google Scholar 

  52. A. Stevenson, P. G. Hamill, C. J. O’Kane, G. Kminek, J. D. Rummel, M. A. Voytek, and J. E. Hallsworth, “Aspergillus penicillioides differentiation and cell division at 0.585 water activity,” Environ. Microbiol. 19 (2), 687–697 (2017). https://doi.org/10.1111/1462-2920.13597

    Article  Google Scholar 

  53. Y. Sun, Y. L. Shi, H. Wang, T. Zhang, L. Y. Yu, H. Sun, and Y. Q. Zhang, “Diversity of bacteria and the characteristics of actinobacteria community structure in Badain Jaran Desert and Tengger Desert of China,” Front. Microbiol. 9, 1068 (2018). https://doi.org/10.3389/fmicb.2018.01068

    Article  Google Scholar 

  54. K. A. Warren-Rhodes, K. C. Lee, S. D. Archer, N. Cabrol, L. Ng-Boyle, D. Wettergreen, and S. B. Pointing, “Subsurface microbial habitats in an extreme desert Mars-analog environment,” Front. Microbiol. 69, 1–11 (2019). https://doi.org/10.3389/fmicb.2019.00069

    Article  Google Scholar 

  55. M. Wassmann, R. Moeller, G. Reitz, and P. Rettberg, “Adaptation of Bacillus subtilis cells to Archean-like UV climate: relevant hints of microbial evolution to remarkably increased radiation resistance,” Astrobiology 10 (6), 605–615 (2010). https://doi.org/10.1089/ast.2009.0455

    Article  Google Scholar 

  56. J. P. Williams and J. E. Hallsworth, “Limits of life in hostile environments: no barriers to biosphere function?,” Environ. Microbiol. 11 (12), 3292–3308 (2009). https://doi.org/10.1111/j.1462-2920.2009.02079.x

    Article  Google Scholar 

  57. P. W. Winston and D. H. Bates, “Saturated solutions for the control of humidity in biological research,” Ecology 41 (1), 232–237 (1960). https://doi.org/10.2307/1931961

    Article  Google Scholar 

  58. P. C. Wright and T. Tanaka, “Physiological modelling of the response of Kocuria rosea exposed to changing water activity,” Biotechnol. Lett. 24 (8), 603–609 (2002).

    Article  Google Scholar 

  59. G. M. Zenova, N. A. Manucharova, and D. G. Zvyagintsev, “Extremophilic and extremotolerant actinomycetes in different soil types,” Eurasian Soil Sci. 44 (4), 417–436 (2011). https://doi.org/10.1134/S1064229311040132

    Article  Google Scholar 

  60. D. G. Zvyagintsev, G. M. Zenova, I. I. Sudnitsyn, T. A. Gracheva, E. V. Lapygina, K. R. Napol’skaya, and A. E. Sydnitsyna, “Development of actinomycetes in brown semidesert soil under low water pressure,” Eurasian Soil Sci. 45 (7), 717–723 (2012). https://doi.org/10.1134/S1064229312030155

    Article  Google Scholar 

  61. D. G. Zvyagintsev, G. M. Zenova, I. I. Sudnitsyn, T. A. Gracheva, K. R. Napol’skaya, and M. A. Belousova, “Dynamics of spore germination and mycelial growth of streptomycetes under low humidity conditions,” Microbiology 78 (4), 440–444 (2009). https://doi.org/10.1134/S0026261709040079

    Article  Google Scholar 

Download references

Funding

This study was supported by the President of the Russian Federation, project no. MK-664.2021.1.4, and partially supported by the Ministry of Science and Education of the Russian Federation, project no. 075-15-2021-1396 (testing of pure bacterial cultures for the ability to grow under low water availability). The data analysis was performed within the framework of state assignment of the Ministry of Science and Education of the Russian Federation, theme no. 2, no. of the Center of Information Technologies and Systems 121040800174-6 Soil Microbiomes: Genomic Diversity, Functional Activity, Geography, and Biotechnological Potential.

Author information

Authors and Affiliations

  1. Lomonosov Moscow State University, 119991, Moscow, Russia

    V. S. Cheptsov & A. A. Belov

  2. Space Research Institute, Russian Academy of Sciences, 117997, Moscow, Russia

    V. S. Cheptsov

  3. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 119071, Moscow, Russia

    I. V. Sotnikov

Authors
  1. V. S. Cheptsov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. A. Belov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. V. Sotnikov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to V. S. Cheptsov.

Ethics declarations

The authors declare that they have no conflicts of interest.

Additional information

Translated by I. Bel’chenko

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cheptsov, V.S., Belov, A.A. & Sotnikov, I.V. Diversity of Bacteria Cultured from Arid Soils and Sedimentary Rocks under Conditions of Available Water Deficiency. Eurasian Soil Sc. 56, 535–544 (2023). https://doi.org/10.1134/S1064229322602761

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1064229322602761

Keywords:

Search

Navigation