Skip to main content
SpringerLink
Log in

Culturable halophilic bacteria inhabiting Algerian saline ecosystems: A source of promising features and potentialities

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

This paper aims to characterize halophilic bacteria inhabiting Algerian Saline Ecosystems (Sebkha and Chott) located in arid and semi-arid ecoclimate zones (Northeastern Algeria). In addition, screening of enzymatic activities, heavy metal tolerance and antagonistic potential against phytopathogenic fungi were tested. A total of 74 bacterial isolates were screened and phylogenetically characterized using 16S rRNA gene sequencing. The results showed a heterogeneous group of microorganisms falling within two major phyla, 52 strains belonging to Firmicutes (70.2%) and 22 strains (30.8%) of γ-Proteobacteria. In terms of main genera present, the isolates were belonging to Bacillus, Halobacillus, Lentibacillus, Oceanobacillus, Paraliobacillus, Planomicrobium, Salicola, Terribacillus, Thalassobacillus, Salibacterium, Salinicoccus, Virgibacillus, Halomonas, Halovibrio, and Idiomarina. Most of the enzymes producers were related to Bacillus, Halobacillus, and Virgibacillus genera and mainly active at 10% of growing salt concentrations. Furthermore, amylase, esterase, gelatinase, and nuclease activities ranked in the first place within the common hydrolytic enzymes. Overall, the isolates showed high minimal inhibitory concentration values (MIC) for Ni2+ and Cu2+ (0.625 to 5 mM) compared to Cd2+ (0.1 to 2 mM) and Zn2+ (0.156 to 2 mM). Moreover, ten isolated strains belonging to Bacillus, Virgibacillus and Halomonas genera, displayed high activity against the pathogenic fungi (Botrytis cinerea, Fusarium oxyporum, F. verticillioides and Phytophthora capsici). This study on halophilic bacteria of unexplored saline niches provides potential sources of biocatalysts and novel bioactive metabolites as well as promising candidates of biocontrol agents and eco-friendly tools for heavy metal bioremediation.

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Addinsoft's (2014). XLSTAT Version 2014 3 07.https://www.xlstat.com. Copyright Addinsoft, (1995–2014)

  • Aguilera M, Jiménez-Pranteda ML, Kharroub K, González-Paredes A, Durban JJ, Russell NJ, Ramos CA, Monteoliva-Sánchez M (2009) Marinobacter lacisalsi sp. nov., a moderately halophilic bacterium isolated from the saline-wetland wildfowl reserve Fuente de Piedra in southern Spain. Int J Syst Evol Microbiol 59:1691–1695

    Article  CAS  Google Scholar 

  • Allais JJ, Kammoun S, Blanc P, Girard C, Baratti JC (1986) Isolation and characterization of bacterial strains with inulinase activity. Appl Environ Microbiol 52:1086–1090

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aliat T, Kaabeche M, Khomri H, Nouri L, Neffar S, Chenchouni H (2016) A pedological characterisation of some inland wetlands and Ramsar sites in Algeria. Land Degrad. Dev 27:693–705

    Article  Google Scholar 

  • Amoozegar MA, Hamedi J, Dadashipour M, Shariatpanahi S (2005) Effect of salinity on the tolerance to toxic metals and oxyanions in native moderately halophilic spore-forming bacilli. World J Microbiol Biotechnol 21:1237–1243

    Article  CAS  Google Scholar 

  • Baati H, Amdouni R, Gharsallah N, Sghir A, Ammar E (2010) Isolation and characterization of moderately halophilic bacteria from Tunisian solar saltern. Curr Microbiol 60:157–161

    Article  CAS  Google Scholar 

  • Benammar L, Menasria T, Ayachi M, Benounis M (2015) Phosphate removal using aerobic bacterial consortium and pure cultures isolated from activated sludge. Process Saf Environ 95:237–246

    Article  CAS  Google Scholar 

  • Benhadj M, Gacemi-Kirane D, Menasria T, Guebla K, Ahmane Z (2018) Screening of rare actinomycetes isolated from natural wetland ecosystem (Fetzara Lake, northeastern Algeria) for hydrolytic enzymes and antimicrobial activities. J King Saud Univ-Sci. https://doi.org/10.1016/j.jksus.2018.03.008

    Article  Google Scholar 

  • Boutaiba S, Hacène H, Bidle KA, Maupin-Furlow JA (2011) Microbial diversity of the hypersaline Sidi Ameur and Himalatt salt lakes of the Algerian Sahara. J Arid Environ 75:909–916

    Article  Google Scholar 

  • Buck JD (1982) Non staining (KOH) method for determination of Gram reactions of marine bacteria. Appl Environ Microbiol 44:992–993

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burns DG, Camakaris HM, Janssen PH, Dyall-Smith ML (2004) Combined use of cultivation-dependent and cultivation-independent methods indicates that members of most haloarchaeal groups in an Australian crystallizer pond are cultivable. Appl Environ Microbiol 70:5258–5265

    Article  CAS  Google Scholar 

  • Chen L, Wang G, Bu T, Zhang Y, Wang Y, Liu M, Lin X (2010) Phylogenetic analysis and screening of antimicrobial and cytotoxic activities of moderately halophilic bacteria isolated from the Weihai Solar Saltern (China). World J Microbiol Biotechnol 26:879–888

    Article  Google Scholar 

  • Chenchouni H, Menasria T, Neffar S, Chafaa S, Bradai L, Chaibi R, Mekahlia MN, Bendjoudi D, Si Bachir A (2015) Spatiotemporal diversity, structure and trophic guilds of insect assemblages in a semi-arid Sabkha ecosystem. PeerJ 3:e860

    Article  Google Scholar 

  • DasSarma S, DasSarma P (2015) Halophiles and their enzymes: negativity put to good use. Curr Opin Microbiol 25:120–126. https://doi.org/10.1016/j.mib.2015.05.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de la Haba RR, Sánchez-Porro C, Márquez MC, Ventosa A (2011) Taxonomy of halophiles. Extremophiles handbook, pp 255–308

  • de Lourdes Moreno M, Pérez D, García MT, Mellado E (2013) Halophilic bacteria as a source of novel hydrolytic enzymes. Life 3:38–51

    Article  Google Scholar 

  • Dean R, van Kan JAL, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430

    Article  Google Scholar 

  • Dekak A, Chabi R, Menasria T, Benhizia Y (2018) Phenotypic characterization of rhizobia nodulating legumes Genista microcephala and Argyrolobium uniflorum growing under arid conditions. J Adv Res 14:35–42

    Article  CAS  Google Scholar 

  • Edbeib MF, Wahab RA, Huyop F (2016) Halophiles: biology, adaptation, and their role in decontamination of hypersaline environments. World J Microbiol Biotechnol 32:1–23

    Article  CAS  Google Scholar 

  • Essghaier B, Fardeau ML, Cayol JL, Hajlaoui MR, Boudabous A, Jijakli H, Sadfi-Zouaoui N (2009) Biological control of grey mould in strawberry fruits by halophilic bacteria. J Appl Microbiol 106:833–846

    Article  CAS  Google Scholar 

  • Ezziyyani M, Requena ME, Egea-Gilabert C, Candela ME (2007) Biological control of Phytophthora root rot of pepper using Trichoderma harzianum and Streptomyces rocheiin combination. Phytopathology J 6:342–349

    Article  Google Scholar 

  • Frazier WC (1926) A method for detection of changes in gelatin due to bacteria. J Infect Dis 39:302–309

    Article  Google Scholar 

  • Ghio S, Sabarís Di Lorenzo GJ, Lia V, Talia P, Cataldi A, Grasso D, Campos E (2012) Isolation of Paenibacillus sp. and Variovorax sp. strains from decaying woods and characterization of their potential for cellulose deconstruction. Int J Biochem Mol Biol 3:352–364

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ghozlan H, Deif H, Kandil RA, Sabry S (2006) Biodiversity of moderately halophilic bacteria in hypersaline habitats. J Gen Appl Microbiol 52:63–72

    Article  CAS  Google Scholar 

  • Gonzalez C, Gutierrez C, Ramirez C (1978) Halobacterium vallismortis sp. nov. An amylolytic and carbohydrate-metabolizing: extremely halophilic bacterium. Can J Microbiol 24:710–715

    Article  CAS  Google Scholar 

  • Hacène H, Rafa F, Chebhouni N, Boutaiba S, Bhatnagar T, Baratti JC, Ollivier B (2004) Biodiversity of prokaryotic microflora in El Golea salt lake, Algerian sahara. J Arid Environ 58:273–284

    Article  Google Scholar 

  • Jeffries CD, Holtman DF, Guse DG (1957) Rapid method for determining the activity of microorganisms on nucleic acids. J Bacteriol 73:590–591

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721

    Article  CAS  Google Scholar 

  • Kim M, Oh HS, Park SC, Chun J (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–351

    Article  CAS  Google Scholar 

  • Lizama C, Monteoliva-Sanchez M, Prado B, Ramos Cormenzana A, Weckesser J, Campos V (2001) Taxonomic study of extreme halophilic archaea isolated from the Salar de Atacama, Chile. Syst Appl Microbiol 24:464–474

    Article  CAS  Google Scholar 

  • Margesin R, Schinner F (2001) Potential of halotolerant and halophilic microorganisms for biotechnology. Extremophiles 5:73–83

    Article  CAS  Google Scholar 

  • Margesin R, Płaza GA, Kasenbacher S (2011) Characterization of bacterial communities at heavy-metal-contaminated sites. Chemosphere 82:1583–1588

    Article  CAS  Google Scholar 

  • Menasria T, Aguilera M, Hacene H, Benammar L, Ayachi A, Bachir A et al (2018) Diversity and bioprospecting of extremely halophilic archaea isolated from Algerian arid and semi-arid wetland ecosystems for halophilic-active hydrolytic enzymes. Microbiol Res 207:289–298. https://doi.org/10.1016/j.micres.2017.12.011

    Article  CAS  PubMed  Google Scholar 

  • Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663. https://doi.org/10.1111/1574-6976.12028

    Article  CAS  PubMed  Google Scholar 

  • Mohamad R, Maynaud G, Le Quéré A, Vidal C, Klonowska A, Yashiro E, Cleyet-Marel JC, Brunel B (2017) Ancient heavy metal contamination in soils as a driver of toleranat Anthyllis vulneraria rhizobial communities. Appl Environ Microbiol 83:1735

    Article  Google Scholar 

  • Montalvo-Rodriguez R, Vreeland RH, Oren A, Kessel M, Betancourt C, Lopez- Garriga J (1998) Halogeometricum borinquense gen. nov. sp. nov., a novel halophilic archaeon from Puerto Rico. Int J Syst Bacteriol 48:1305–1312

    Article  CAS  Google Scholar 

  • Mu J, Li X, Jiao J, Ji G, Wu J, Hu F, Hi H (2017) Biocontrol potential of vermicompost through antifungal volatiles produced by indigenous bacteria. Biol Control 112:49–54

    Article  CAS  Google Scholar 

  • Murray RGE, Doetsch RN, Robinow CF (1994) Determinative and cytological light microscopy. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington DC, pp 21–41

    Google Scholar 

  • Nieto JJ, Fernandez Castillo R, Marquez MC, Ventosa A, Quesada E, Ruiz Berraquero F (1989) Survey of metal tolerance in moderately halophilic eubacteria. Appl Environ Microbiol 55(9):2385–2390

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oren A (2002) Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J Ind Microbiol Biotech 28:56–63

    Article  CAS  Google Scholar 

  • Quadri I, Hassani I, Haridon S, Chalopin M, Hacène H, Jebbar M (2016) Characterization and antimicrobial potential of extremely halophilic archaea isolated from hypersaline environments of the Algerian Sahara. Microbiol Res 186–187:119–131. https://doi.org/10.1016/j.micres.2016.04.003

    Article  CAS  PubMed  Google Scholar 

  • Roberts WK, Selitrennikoff CP (1988) Plant and bacterial chitinases differ in antifungal activity. J Gen Microbiol 134:169–176

    CAS  Google Scholar 

  • Rohban R, Amoozegar MA, Ventosa A (2009) Screening and isolation of halophilic bacteria producing extracellular hydrolyses from Howz Soltan Lake. Iran. J Ind Microbiol Biotechnol 36:333–340

    Article  CAS  Google Scholar 

  • Sadfi-Zouaoui N, Essghaier B, Hajlaoui MR, Fardeau ML, Cayaol JL, Ollivier B, Boudabous A (2008) Ability of moderately halophilic bacteria to control grey mould disease on tomato fruits. J Phytopathol 156:42–52. https://doi.org/10.1111/j.1439-0434.2007.01329.x

    Article  CAS  Google Scholar 

  • Sánchez-Porro C, Martin S, Mellado E, Ventosa A (2003) Diversity of moderately halophilic bacteria producing extracellular hydrolytic enzymes. J Appl Microbiol 94:295–300

    Article  Google Scholar 

  • Sierra G (1957) A simple method for the detection of lipolytic activity of microorganisms and some observations on the influence of the contact between cells and fatty substrates. Antonie Van Leeuwenhoek 23:15–22

    Article  CAS  Google Scholar 

  • Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington DC, pp 607–654

    Google Scholar 

  • Soares Marcia MCN, De Silva R, Gomez E (1999) Screening of bacterial strains for pectinolytic activity: characterization of the polygalacturonase produced by Bacillus sp. Rev Microbiol. 30:299–303. https://doi.org/10.1590/S0001-37141999000400002

    Article  Google Scholar 

  • Subov NN (1931) Oceanographical Tables. USSR Oceanographic Institute Hydrometeorological Commission, Moscow

    Google Scholar 

  • Teather RM, Wood PJ (1982) Use of Congo red-polysaccharide interactions in enumeration and characterization of cellulolytic bacteria from the bovine rumen. Appl Environ Microbiol 43:777–780

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  Google Scholar 

  • Ventosa A, Quesada E, Rodriguez-Valera F, Ruiz-Berraquero F, Ramos-Cormenzana A (1982) Numerical taxonomy of moderately halophilic Gram-negative rods. J Gen Microbiol 128:1959–1968. https://doi.org/10.1099/00221287-128-9-1959

    Article  Google Scholar 

  • Ventosa A, Nieto JJ, Oren A (1998) Biology of moderately halophilic aerobic bacteria. Microbiol. Mol Biol Rev 62:504–544

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ventosa A, Sanchez-Porro C, Martın S, Mellado E (2005) In: Gunde-Cimerman N, Oren A, Plemenitas A (eds) Halophilic Archaea And bacteria as a Source of Extracellularhydrolytic Enzymes, in Adaptation to Life at High Salt Concentrations in Archaea, Bacteria and Eukarya. Springer, Dordrecht, pp 337–350

    Google Scholar 

  • Ventosa A, Mellado E, Sanchez-Porro C, Marquez MC (2008) Halophilic and halotolerant micro-organisms from soils. In: Dion P, Nautiyal CS (eds) Microbiology of extreme soils. Springer, Berlin, pp 87–115

    Chapter  Google Scholar 

  • Voica DM, Bartha L, Banciu HL, Oren A (2016) Heavy metal resistance in halophilic bacteria and archaea. FEMS Microbiol Lett 363(14):146

    Article  Google Scholar 

  • Yeon SH, Jeong WJ, Park JS (2005) The diversity of culturable organotrophic bacteria from local solar salterns. J Microbiol 43:1–10

    PubMed  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge the staff member of the Department of Microbiology (MV. Megias Sanchez) (University of Granada, Spain), and Department of Veterinary Sciences (University of Batna 1, Algeria) for all facilities provided in carrying out this study. Many thanks to H. Chenchouni, R. Megri, MN. Mekahlia and H. Abdessemed for helping to collect the samples. Gratitude to the supports of Junta de Andalucia Group (BIO-190), Spain and the Algerian Ministry of Higher Education and Scientific Research (Programme National Exceptionnel-2016).

Author information

Authors and Affiliations

  1. Department of Microbiology, Faculty of Pharmacy, University of Granada, Granada, Spain

    Taha Menasria, Mercedes Monteoliva-Sánchez, Ana Gonzalez-Paredes & Margarita Aguilera

  2. Department of Applied Biology, Faculty of Exact Sciences and Natural and Life Sciences, Larbi Tebessi University, 12002, Tebessa, Algeria

    Taha Menasria & Mabrouka Benhadj

  3. Department of Microbiology and Biochemistry, Faculty of Natural and Life Sciences, University of Batna 2, 05078, Batna, Algeria

    Taha Menasria & Leyla Benammar

  4. Veterinary and Agricultural Sciences Institute, Department of Veterinary Sciences, University of Batna 1, 05000, Batna, Algeria

    Ammar Ayachi

  5. Cellular and Molecular Biology Laboratory, University of Sciences and Technology Houari Boumediene, Bp 32, El Alia, 16111, Bab Ezzouar, Algiers, Algeria

    Hocine Hacène

Authors
  1. Taha Menasria
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mercedes Monteoliva-Sánchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Leyla Benammar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mabrouka Benhadj
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ammar Ayachi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hocine Hacène
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ana Gonzalez-Paredes
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Margarita Aguilera
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

TM designed the study, collected the samples, carried out the laboratory experiments, conceived and drafted the manuscript; MMS, HH, MM, AA analyzed, conceived and revised the manuscript. BL, MB, AGP gave technical support and conceptual advice.

Corresponding authors

Correspondence to Taha Menasria or Margarita Aguilera.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Menasria, T., Monteoliva-Sánchez, M., Benammar, L. et al. Culturable halophilic bacteria inhabiting Algerian saline ecosystems: A source of promising features and potentialities. World J Microbiol Biotechnol 35, 132 (2019). https://doi.org/10.1007/s11274-019-2705-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-019-2705-y

Keywords

Search

Navigation