Exploring the antimicrobial potential of two haloarchaeal strains belonging to the genera Halopiger and Natrialba isolated from the Algerian Sahara
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Abstract
Background and Objectives: Halophilic archaea commonly produce antimicrobial peptides (halocins), but only a few studies have been conducted on these molecules. This study explores the antimicrobial potential of two strains belonging to Halopiger and Natrialba genera, isolated from hypersaline environments in the Algerian Sahara. Antimicrobial compounds produced by these genera have rarely been studied before.
Materials and Methods: The antimicrobial activity of the strains was evaluated, along with the effects of UV radiation and culture conditions on growth and compound production. Stability assays and the effects of extracted compounds on target cells and peripheral blood mononuclear cells (PBMC) were assessed.
Results: The strains exhibited high anti-archaeal activities and cross-domain interactions. Producing extracellular compounds associated with halocin, in the cell-free supernatant (CFS). These compounds remained stable at different temperatures (4°C, 60°C, 80°C, and 100°C) and different pH ranges (4-10 and 5-11), with antimicrobial profiles changed in response to UV light. The active compounds resembled known halocins but displayed unique features suggesting the discovery of new halocins. Additionally, Natrialba extracts showed significant activity against PBMC.
Conclusion: This investigation confirms that Algerian saline soils are a promising source of interesting antimicrobial compounds.
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2. Oren A. Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Syst 2008; 4: 2.
3. Quadri I, Hassani II, l'Haridon S, Chalopin M, Hacène H, Jebbar M. Characterization and antimicrobial potential of extremely halophilic archaea isolated from hypersaline environments of the Algerian Sahara. Microbiol Res 2016; 186-187: 119-131.
4. Oren A. Molecular ecology of extremely halophilic Archaea and Bacteria. FEMS Microbiol Ecol 2002; 39: 1-7.
5. Cui HL, Hou J, Amoozegar MA, Dyall-Smith ML, de la Haba RR, Minegishi H, et al. Proposed minimal standards for description of new taxa of the class Halobacteria. Int J Syst Evol Microbiol 2024; 74: 006290.
6. Gupta RS, Naushad S, Baker S. Phylogenomic analyses and molecular signatures for the class halobacteria and its two major clades: a proposal for division of the class halobacteria into an emended order Halobacteriales and two new orders, Haloferacales ord. nov. and Natrialbales ord. nov., containing the novel families Haloferacaceae fam. nov. and Natrialbaceae fam. nov. Int J Syst Evol Microbiol 2015; 65: 1050-1069.
7. Gupta RS, Naushad S, Fabros R, Adeolu M. Erratum to: A phylogenomic reappraisal of family-level divisions within the class halobacteria: proposal to divide the order Halobacteriales into the families Halobacteriaceae, Haloarculaceae fam. nov., and Halococcaceae fam. nov., and the order Haloferacales into the families, Haloferacaceae and Halorubraceae fam nov. Antonie Van Leeuwenhoek 2016; 109: 1521-1523.
8. Hassani II, Quadri I, Yadav A, Bouchard S, Raoult D, Hacène H, et al. Assessment of diversity of archaeal communities in Algerian chott. Extremophiles 2022; 27: 2.
9. Kis-Papo T, Oren A. Halocins: are they involved in the competition between halobacteria in saltern ponds? Extremophiles 2000; 4: 35-41.
10. Besse A, Peduzzi J, Rebuffat S, Carre-Mlouka A. Antimicrobial peptides and proteins in the face of extremes: Lessons from archaeocins. Biochimie 2015; 118: 344-355.
11. Kumar V, Singh B, van Belkum MJ, Diep DB, Chikindas ML, Ermakov AM, et al. Halocins, natural antimicrobials of Archaea: Exotic or special or both? Biotechnol Adv 2021; 53: 107834.
12. Naor A, Yair Y, Gophna U. A halocin-H4 mutant Haloferax mediterranei strain retains the ability to inhibit growth of other halophilic archaea. Extremophiles 2013; 17: 973-979.
13. Atanasova NS, Pietilä MK, Oksanen HM. Diverse antimicrobial interactions of halophilic archaea and bacteria extend over geographical distances and cross the domain barrier. Microbiologyopen 2013; 2: 811-825.
14. Thompson TP, Gilmore BF. Exploring halophilic environments as a source of new antibiotics. Crit Rev Microbiol 2024; 50: 341-370.
15. Mazguene S, Rossi M, Gogliettino M, Palmieri G, Cocca E, Mirino S, et al. Isolation and characterization from solar salterns of North Algeria of a haloarchaeon producing a new halocin. Extremophiles 2018; 22: 259-270.
16. Kumar V, Tiwari SK. Activity-guided separation and characterization of new halocin HA3 from fermented broth of Haloferax larsenii HA3. Extremophiles 2017; 21: 609-621.
17. Hassani II, Robert C, Michelle C, Raoult D, Hacene H, Desnues C. Non-contiguous finished genome sequence and description of Halopiger djelfamassiliensis sp nov. Stand Genomic Sci 2013; 9: 160-174.
18. Oren A, Garrity GM. List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol 2016; 66: 2463-2466.
19. Balouiri M, Sadiki M, Ibnsouda SK. Methods for in vitro evaluating antimicrobial activity: A review. J Pharm Anal 2016; 6: 71-79.
20. Strober W. Trypan blue exclusion test of cell viability. Curr Protoc Immunol 2015; 111: A3.B.1-A3.B.3.
21. Hegazy GE, Abu-Serie MM, Abo-Elela GM, Ghozlan H, Sabry SA, Soliman NA, et al. In vitro dual (anticancer and antiviral) activity of the carotenoids produced by haloalkaliphilic archaeon Natrialba sp. M6. Sci Rep 2020; 10: 5986.
22. Hezayen FF, Rehm BH, Tindall BJ, Steinbuchel A. Transfer of Natrialba asiatica B1T to Natrialba taiwanensis sp. nov. and description of Natrialba aegyptiaca sp. nov., a novel extremely halophilic, aerobic, non pigmented member of the Archaea from Egypt which produces extracellular poly(glutamic acid). Int J Syst Evol Microbiol 2001; 51: 1133-1142.
23. Price LB, Shand RF. Halocin S8: a 36-amino-acid microhalocin from the haloarchaeal strain S8a. J Bacteriol 2000; 182: 4951-4958.
24. O'Connor EM, Shand RF. Halocins and sulfolobicins: the emerging story of archaeal protein and peptide antibiotics. J Ind Microbiol Biotechnol 2002; 28: 23-31.
25. Platas G, Meseguer I, Amils R. Purification and biological characterization of halocin H1 from Haloferax mediterranei M2a. Int Microbiol 2002; 5: 15-19.
26. Li Y, Xiang H, Liu J, Zhou M, Tan H. Purification and biological characterization of halocin C8, a novel peptide antibiotic from Halobacterium strain AS7092. Extremophiles 2003; 7: 401-407.
27. Jones DL, Baxter BK. Bipyrimidine signatures as a photoprotective genome strategy in G+ C-rich halophilic archaea. Life (Basel) 2016; 6: 37.
28. Martínez-Espinosa RM. Halocins and C50 Carotenoids from Haloarchaea: Potential Natural Tools against Cancer. Mar Drugs 2024; 22: 448.
29. Chen S, Sun S, Korfanty GA, Liu J, Xiang H. A Halocin Promotes DNA Uptake in Haloferax mediterranei. Front Microbiol 2019; 10: 1960.
30. Pasić L, Velikonja BH, Ulrih NP. Optimization of the culture conditions for the production of a bacteriocin from halophilic archaeon Sech7a. Prep Biochem Biotechnol 2008; 38: 229-245.
31. Sun C, Li Y, Mei S, Lu Q, Zhou L, Xiang H. A single gene directs both production and immunity of halocin C8 in a haloarchaeal strain AS7092. Mol Microbiol 2005; 57: 537-549.
32. Karthikeyan P, Bhat SG, Chandrasekaran M. Halocin SH10 production by an extreme haloarchaeon Natrinema sp. BTSH10 isolated from salt pans of South India. Saudi J Biol Sci 2013; 20: 205-212.
33. Lequerica JL, O’Connor JE, Such L, Alberola A, Meseguer I, Dolz M, et al. A halocin acting on Na+/H+ exchanger of Haloarchaea as a new type of inhibitor in NHE of mammals. J Physiol Biochem 2006; 62: 253-262.
2. Oren A. Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Syst 2008; 4: 2.
3. Quadri I, Hassani II, l'Haridon S, Chalopin M, Hacène H, Jebbar M. Characterization and antimicrobial potential of extremely halophilic archaea isolated from hypersaline environments of the Algerian Sahara. Microbiol Res 2016; 186-187: 119-131.
4. Oren A. Molecular ecology of extremely halophilic Archaea and Bacteria. FEMS Microbiol Ecol 2002; 39: 1-7.
5. Cui HL, Hou J, Amoozegar MA, Dyall-Smith ML, de la Haba RR, Minegishi H, et al. Proposed minimal standards for description of new taxa of the class Halobacteria. Int J Syst Evol Microbiol 2024; 74: 006290.
6. Gupta RS, Naushad S, Baker S. Phylogenomic analyses and molecular signatures for the class halobacteria and its two major clades: a proposal for division of the class halobacteria into an emended order Halobacteriales and two new orders, Haloferacales ord. nov. and Natrialbales ord. nov., containing the novel families Haloferacaceae fam. nov. and Natrialbaceae fam. nov. Int J Syst Evol Microbiol 2015; 65: 1050-1069.
7. Gupta RS, Naushad S, Fabros R, Adeolu M. Erratum to: A phylogenomic reappraisal of family-level divisions within the class halobacteria: proposal to divide the order Halobacteriales into the families Halobacteriaceae, Haloarculaceae fam. nov., and Halococcaceae fam. nov., and the order Haloferacales into the families, Haloferacaceae and Halorubraceae fam nov. Antonie Van Leeuwenhoek 2016; 109: 1521-1523.
8. Hassani II, Quadri I, Yadav A, Bouchard S, Raoult D, Hacène H, et al. Assessment of diversity of archaeal communities in Algerian chott. Extremophiles 2022; 27: 2.
9. Kis-Papo T, Oren A. Halocins: are they involved in the competition between halobacteria in saltern ponds? Extremophiles 2000; 4: 35-41.
10. Besse A, Peduzzi J, Rebuffat S, Carre-Mlouka A. Antimicrobial peptides and proteins in the face of extremes: Lessons from archaeocins. Biochimie 2015; 118: 344-355.
11. Kumar V, Singh B, van Belkum MJ, Diep DB, Chikindas ML, Ermakov AM, et al. Halocins, natural antimicrobials of Archaea: Exotic or special or both? Biotechnol Adv 2021; 53: 107834.
12. Naor A, Yair Y, Gophna U. A halocin-H4 mutant Haloferax mediterranei strain retains the ability to inhibit growth of other halophilic archaea. Extremophiles 2013; 17: 973-979.
13. Atanasova NS, Pietilä MK, Oksanen HM. Diverse antimicrobial interactions of halophilic archaea and bacteria extend over geographical distances and cross the domain barrier. Microbiologyopen 2013; 2: 811-825.
14. Thompson TP, Gilmore BF. Exploring halophilic environments as a source of new antibiotics. Crit Rev Microbiol 2024; 50: 341-370.
15. Mazguene S, Rossi M, Gogliettino M, Palmieri G, Cocca E, Mirino S, et al. Isolation and characterization from solar salterns of North Algeria of a haloarchaeon producing a new halocin. Extremophiles 2018; 22: 259-270.
16. Kumar V, Tiwari SK. Activity-guided separation and characterization of new halocin HA3 from fermented broth of Haloferax larsenii HA3. Extremophiles 2017; 21: 609-621.
17. Hassani II, Robert C, Michelle C, Raoult D, Hacene H, Desnues C. Non-contiguous finished genome sequence and description of Halopiger djelfamassiliensis sp nov. Stand Genomic Sci 2013; 9: 160-174.
18. Oren A, Garrity GM. List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol 2016; 66: 2463-2466.
19. Balouiri M, Sadiki M, Ibnsouda SK. Methods for in vitro evaluating antimicrobial activity: A review. J Pharm Anal 2016; 6: 71-79.
20. Strober W. Trypan blue exclusion test of cell viability. Curr Protoc Immunol 2015; 111: A3.B.1-A3.B.3.
21. Hegazy GE, Abu-Serie MM, Abo-Elela GM, Ghozlan H, Sabry SA, Soliman NA, et al. In vitro dual (anticancer and antiviral) activity of the carotenoids produced by haloalkaliphilic archaeon Natrialba sp. M6. Sci Rep 2020; 10: 5986.
22. Hezayen FF, Rehm BH, Tindall BJ, Steinbuchel A. Transfer of Natrialba asiatica B1T to Natrialba taiwanensis sp. nov. and description of Natrialba aegyptiaca sp. nov., a novel extremely halophilic, aerobic, non pigmented member of the Archaea from Egypt which produces extracellular poly(glutamic acid). Int J Syst Evol Microbiol 2001; 51: 1133-1142.
23. Price LB, Shand RF. Halocin S8: a 36-amino-acid microhalocin from the haloarchaeal strain S8a. J Bacteriol 2000; 182: 4951-4958.
24. O'Connor EM, Shand RF. Halocins and sulfolobicins: the emerging story of archaeal protein and peptide antibiotics. J Ind Microbiol Biotechnol 2002; 28: 23-31.
25. Platas G, Meseguer I, Amils R. Purification and biological characterization of halocin H1 from Haloferax mediterranei M2a. Int Microbiol 2002; 5: 15-19.
26. Li Y, Xiang H, Liu J, Zhou M, Tan H. Purification and biological characterization of halocin C8, a novel peptide antibiotic from Halobacterium strain AS7092. Extremophiles 2003; 7: 401-407.
27. Jones DL, Baxter BK. Bipyrimidine signatures as a photoprotective genome strategy in G+ C-rich halophilic archaea. Life (Basel) 2016; 6: 37.
28. Martínez-Espinosa RM. Halocins and C50 Carotenoids from Haloarchaea: Potential Natural Tools against Cancer. Mar Drugs 2024; 22: 448.
29. Chen S, Sun S, Korfanty GA, Liu J, Xiang H. A Halocin Promotes DNA Uptake in Haloferax mediterranei. Front Microbiol 2019; 10: 1960.
30. Pasić L, Velikonja BH, Ulrih NP. Optimization of the culture conditions for the production of a bacteriocin from halophilic archaeon Sech7a. Prep Biochem Biotechnol 2008; 38: 229-245.
31. Sun C, Li Y, Mei S, Lu Q, Zhou L, Xiang H. A single gene directs both production and immunity of halocin C8 in a haloarchaeal strain AS7092. Mol Microbiol 2005; 57: 537-549.
32. Karthikeyan P, Bhat SG, Chandrasekaran M. Halocin SH10 production by an extreme haloarchaeon Natrinema sp. BTSH10 isolated from salt pans of South India. Saudi J Biol Sci 2013; 20: 205-212.
33. Lequerica JL, O’Connor JE, Such L, Alberola A, Meseguer I, Dolz M, et al. A halocin acting on Na+/H+ exchanger of Haloarchaea as a new type of inhibitor in NHE of mammals. J Physiol Biochem 2006; 62: 253-262.
| Files | ||
| Issue | Vol 17 No 1 (2025) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v17i1.17812 | |
| Keywords | ||
| Archaea; Halopiger; Natrialba; Extreme environments; Antimicrobial peptides; Peripheral blood mononuclear cells | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Quadri I, Hassani I, Hacène H. Exploring the antimicrobial potential of two haloarchaeal strains belonging to the genera Halopiger and Natrialba isolated from the Algerian Sahara. Iran J Microbiol. 2025;17(1):144-152.
