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Microbial Diversity in an Arid, Naturally Saline Environment

  • Soil Microbiology
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Abstract

The Arava Valley in is a rock desert within the Great African Rift valley. Soil from this area is covered with a salt crust. Here, we report microbial diversity from arid, naturally saline samples collected near Ein Yahav from the Arava Valley by culture-independent as well as culture-dependent analysis. High-throughput sequencing of the hypervariable region V4 of the 16S rRNA gene revealed that the microbial community consists of halophiles from the domain Bacteria as well as Archaea. Bacterial diversity was mainly represented by the genus Salinimicrobium of the order Flavobacteriales within the phylum Bacteroidetes, from the gammaproteobacterial orders Alteromonadales and Oceanospirillales as well as representatives from the order Bacillales of the phylum Firmicutes. Archaeal diversity was dominated by euryarchaeal Halobacteria from the orders Halobacteriales, Haloferacales, and Natrialbales. But more than 40% of the sequences affiliated with Archaea were assigned to unknown or unclassified archaea. Even if taxonomic resolution of the 16S rRNA gene V4 region for Archaea is limited, this study indicates the need of further and more detailed studies of Archaea. By using culture-dependent analysis, bacteria of the order Bacillales as well as archaea from all three halobacterial orders Halobacteriales, Haloferacales, and Natrialbales including potentially novel species from the genera Halorubrum and Haloparvum were isolated.

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References

  1. Ma Y, Galinski EA, Grant WD, Oren A, Ventosa A (2010) Halophiles 2010: life in saline environments. Appl Environ Microbiol 76:6971–6981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Konings WN, Albers SV, Koning S, Driessen AJM (2002) The cell membrane plays a crucial role in survival of bacteria and archaea in extreme environments. Anton Leeuw 81:61–72

    Article  CAS  Google Scholar 

  3. Oren A (2013) Life at high salt concentrations, intracellular KCl concentrations, and acidic proteomes. Front Microbiol 4:315. https://doi.org/10.3389/fmicb.2013.00315

    Article  PubMed  PubMed Central  Google Scholar 

  4. Pandit AS, Joshi MN, Bhargava P, Shaikh I, Ayachit GN, Raj SR, Saxena AK, Bagatharia SB (2015) A snapshot of microbial communities from the Kutch: one of the largest salt deserts in the World. Extremophiles 19:973–987

    Article  PubMed  Google Scholar 

  5. Hollister EB, Engledow AS, Hammett AJM, Provin TL, Wilkinson HH, Gentry TJ (2010) Shifts in microbial community structure along an ecological gradient of hypersaline soils and sediments. ISME J 4:829–838

    Article  CAS  PubMed  Google Scholar 

  6. Patel R, Mevada V, Prajapati D, Dudhagara P, Koringa P, Joshi CG (2015) Metagenomic sequence of saline desert microbiota from wild ass sanctuary, Little Rann of Kutch, Gujarat, India. Genomics Data 3:137–139

    Article  PubMed  PubMed Central  Google Scholar 

  7. Gupta RS, Naushad S, Fabros R, Adeolu M (2016) 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. Anton Leeuw 109:565–587

    Article  Google Scholar 

  8. Gupta RS, Naushad S, Baker S (2015) 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 65:1050–1069

    Article  CAS  PubMed  Google Scholar 

  9. McDuff S, King GM, Neupane S, Myers MR (2016) Isolation and characterization of extremely halophilic CO-oxidizing Euryarchaeota from hypersaline cinders, sediments and soils and description of a novel CO oxidizer, Haloferax namakaokahaiae Mke2.3T, sp. nov. FEMS Microbiol Ecol 92:fiw028

    Article  CAS  PubMed  Google Scholar 

  10. Chen YG, Cui XL, Zhang YQ, Li WJ, Wang YX, Kim CJ, Lim JM, Xu LH, Jiang CL (2008) Salinimicrobium terrae sp. nov., isolated from saline soil, and emended description of the genus Salinimicrobium. Int J Syst Evol Microbiol 58:2501–2504

    Article  CAS  PubMed  Google Scholar 

  11. Naghoni A, Emtiazi G, Amoozegar MA, Cretoiu MS, Stal LJ, Etemadifar Z, Fazeli SAS, Bolhuis H (2017) Microbial diversity in the hypersaline Lake Meyghan, Iran. Sci Rep 7:11522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Gibtan A, Park K, Woo M, Shin JK, Lee DW, Sohn JH, Song M, Roh SW, Lee SJ, Lee HS (2017) Diversity of extremely halophilic archaeal and bacterial communities from commercial salts. Front Microbiol 8:799

    Article  PubMed  PubMed Central  Google Scholar 

  13. Selenska-Pobell S, Kampf G, Flemming K, Radeva G, Satchanska G (2001) Bacterial diversity in soil samples from two uranium waste piles as determined by rep-APD, RISA and 16S rDNA retrieval. Anton Leeuw 79:149–161

    Article  CAS  Google Scholar 

  14. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108:4516–4522

    Article  PubMed  Google Scholar 

  15. Data Analysis Methodology RTL Genomics. http://www.rtlgenomics.com/docs/Data_Analysis_Methodology.pdf

  16. Robertson CE, Harris JK, Wagner BD, Granger D, Browne K, Tatem B, Feazel LM, Park K, Pace NR, Frank DN (2013) Explicet: graphical user interface software for metadata-driven management, analysis and visualization of microbiome data. Bioinformatics 29:3100–3101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Delong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci U S A 89:5685–5689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Nedashkovskaya OI, Vancanneyt M, Kim SB, Han J, Zhukova NV, Shevchenko LS (2010) Salinimicrobium marinum sp. nov., a halophilic bacterium of the family Flavobacteriaceae, and emended descriptions of the genus Salinimicrobium and Salinimicrobium catena. Int J Syst Evol Microbiol 60:2303–2306

    Article  CAS  PubMed  Google Scholar 

  21. Yoon J-H, Kang S-J, Jung Y-T, Oh T-K (2007) Halobacillus campisalis sp. nov., containing mesodiaminopimelic acid in the cell-wall peptidoglycan, and emended description of the genus Halobacillus. Int J Syst Evol Microbiol 57:2021–2025

    Article  CAS  PubMed  Google Scholar 

  22. Garcia MT, Gallego V, Ventosa A, Mellado E (2005) Thalassobacillus devorans gen. nov., sp nov., a moderately halophilic, phenol-degrading, Gram-positive bacterium. Int J Syst Evol Microbiol 55:1789–1795

    Article  CAS  PubMed  Google Scholar 

  23. Sanchez-Porro C, Yilmaz P, de la Haba RR, Birbir M, Ventosa A (2011) Thalassobacillus pellis sp nov., a moderately halophilic, Gram-positive bacterium isolated from salted hides. Int J Syst Evol Microbiol 61:1206–1210

    Article  CAS  PubMed  Google Scholar 

  24. Gao XH, Gao S, Zhou Y, Guan HL, Zhang YJ, Jia M, Huang HW, Yang DX, Li WJ, Tang SK (2013) Tenuibacillus halotolerans sp nov., a novel bacterium isolated from a soil sample from a salt lake in Xinjiang, China and emended description of the genus Tenuibacillus. Anton Leeuw 103:207–215

    Article  CAS  Google Scholar 

  25. Amoozegar MA, Bagheri M, Didari M, Mehrshad M, Schumann P, Sproer C, Sanchez-Porro C, Ventosa A (2014) Aquibacillus halophilus gen. nov., sp nov., a moderately halophilic bacterium from a hypersaline lake, and reclassification of Virgibacillus koreensis as Aquibacillus koreensis comb. nov and Virgibacillus albus as Aquibacillus albus comb. nov. Int J Syst Evol Microbiol 64:3616–3623

    Article  CAS  PubMed  Google Scholar 

  26. Lim JM, Jeon CO, Park DJ, Kim HR, Yoon BJ, Kim CJ (2005) Pontibacillus marinus sp nov., a moderately halophilic bacterium from a solar saltern, and emended description of the genus Pontibacillus. Int J Syst Evol Microbiol 55:1027–1031

    Article  CAS  PubMed  Google Scholar 

  27. Podell S, Ugalde JA, Narasingarao P, Banfield JF, Heidelberg KB, Allen EE (2013) Assembly-driven community genomics of a hypersaline microbial ecosystem. PLoS One 8:e61692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Wang ZJ, Liu QQ, Zhao LH, Du ZJ, Chen GJ (2015) Bradymonas sediminis gen. nov., sp nov., isolated from coastal sediment, and description of Bradymonadaceae fam. nov and Bradymonadales ord. nov. Int J Syst Evol Microbiol 65:1542–1549

    Article  CAS  PubMed  Google Scholar 

  29. Gutierrez MC, Castillo AM, Kamekura M, Xue Y, Ma Y, Cowan DA, Jones BE, Grant WD, Ventosa A (2007) Halopiger xanaduensis gen. nov., sp nov., an extremely halophilic archaeon isolated from saline Lake Shangmatala in Inner Mongolia, China. Int J Syst Evol Microbiol 57:1402–1407

    Article  CAS  PubMed  Google Scholar 

  30. Minegishi H, Shimogaki R, Enomoto S, Echigo A, Kondo Y, Nagaoka S, Shimane Y, Kamekura M, Itoh T, Ohkuma M, Nunoura T, Takai K, Usami R (2016) Halopiger thermotolerans sp nov., a thermo-tolerant haloarchaeon isolated from commercial salt. Int J Syst Evol Microbiol 66:4975–4980

    Article  CAS  PubMed  Google Scholar 

  31. Jaakkola ST, Pfeiffer F, Ravantti JJ, Guo QG, Liu Y, Chen XD, Ma HL, Yang CH, Oksanen HM, Bamford DH (2016) The complete genome of a viable archaeum isolated from 123-million-year-old rock salt. Environ Microbiol 18:565–579

    Article  CAS  PubMed  Google Scholar 

  32. Jaakkola ST, Zerulla K, Guo QG, Liu Y, Ma HL, Yang CH, Bamford DH, Chen XD, Soppa J, Oksanen HM (2014) Halophilic archaea cultivated from surface sterilized Middle-Late Eocene rock salt are polyploid. PLoS One 9:e110533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Kondo Y, Minegishi H, Echigo A, Shimane Y, Kamekura M, Itoh T, Ohkuma M, Takahashi-Ando N, Fukushima Y, Yoshida Y, Usami R (2015) Halorubrum gandharaense sp nov., an alkaliphilic haloarchaeon from commercial rock salt. Int J Syst Evol Microbiol 65:2345–2350

    Article  CAS  PubMed  Google Scholar 

  34. Cui HL, Li XY, Gao X, Xu XW, Zhou YG, Liu HC, Oren A, Zhou PJ (2010) Halopelagius inordinatus gen. nov., sp. nov., a new member of the family Halobacteriaceae isolated from a marine solar saltern. Int J Syst Evol Microbiol 60:2089–2093

    Article  CAS  PubMed  Google Scholar 

  35. Vreeland RH, Straight S, Krammes J, Dougherty K, Rosenzweig WD, Kamekura M (2002) Halosimplex carlsbadense gen. nov., sp nov., a unique halophilic archaeon, with three 16S rRNA genes, that grows only in defined medium with glycerol and acetate or pyruvate. Extremophiles 6:445–452

    Article  CAS  PubMed  Google Scholar 

  36. Chen SX, Liu HC, Zhou J, Xiang H (2016) Haloparvum sedimenti gen. nov., sp nov., a member of the family Haloferacaceae. Int J Syst Evol Microbiol 66:2327–2334

    Article  CAS  PubMed  Google Scholar 

  37. Robinson CK, Wierzchos J, Black C, Crits-Christoph A, Ma B, Ravel J, Ascaso C, Artieda O, Valea S, Roldan M, Gomez-Silva B, DiRuggiero J (2015) Microbial diversity and the presence of algae in halite endolithic communities are correlated to atmospheric moisture in the hyper-arid zone of the Atacama Desert. Environ Microbiol 17:299–315

    Article  PubMed  Google Scholar 

  38. Canfora L, Bacci G, Pinzari F, Lo Papa G, Dazzi C, Benedetti A (2014) Salinity and bacterial diversity: to what extent does the concentration of salt affect the bacterial community in a saline soil? PLoS One 9:e106662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Oren A (2008) Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Syst 4:2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Vreeland RH, Litchfield CD, Martin EL, Elliot E (1980) Halomonas elongata, a new genus and species of extremely salt-tolerant bacteria. Int J Syst Bacteriol 30:485–495

    Article  CAS  Google Scholar 

  41. Lim JM, Jeon CO, Lee SS, Park DJ, Xu LH, Jiang CL, Kim CJ (2008) Reclassification of Salegentibacter catena Ying et al. 2007 as Salinimicrobium catena gen. nov., comb. nov and description of Salinimicrobium xinjiangense sp nov., a halophilic bacterium isolated from Xinjiang province in China. Int J Syst Evol Microbiol 58:438–442

    Article  CAS  PubMed  Google Scholar 

  42. Sella S, Vandenberghe LPS, Soccol CR (2014) Life cycle and spore resistance of spore-forming Bacillus atrophaeus. Microbiol Res 169:931–939

    Article  CAS  PubMed  Google Scholar 

  43. Gu J, Cai H, Yu SL, Qu R, Yin B, Guo YF, Zhao JY, Wu XL (2007) Marinobacter gudaonensis sp nov., isolated from an oil-polluted saline soil in a Chinese oilfield. Int J Syst Evol Microbiol 57:250–254

    Article  CAS  PubMed  Google Scholar 

  44. Jiang JQ, Pan YY, Hu SX, Zhang XX, Hu BZ, Huang HP, Hong S, Meng J, Li C, Wang KB (2014) Halomonas songnenensis sp nov., a moderately halophilic bacterium isolated from saline and alkaline soils. Int J Syst Evol Microbiol 64:1662–1669

    Article  CAS  PubMed  Google Scholar 

  45. Quillaguaman J, Hatti-Kaul R, Mattiasson B, Alvarez MT, Delgado O (2004) Halomonas boliviensis sp nov., an alkalitolerant, moderate halophile isolated from soil around a Bolivian hypersaline lake. Int J Syst Evol Microbiol 54:721–725

    Article  CAS  PubMed  Google Scholar 

  46. Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ, Castelle CJ, Butterfield CN, Hernsdorf AW, Amano Y, Ise K, Suzuki Y, Dudek N, Relman DA, Finstad KM, Amundson R, Thomas BC, Banfield JF (2016) A new view of the tree of life. Nat Microbiol 1:16048

    Article  CAS  PubMed  Google Scholar 

  47. Yang Y, Cui HL, Zhou PJ, Liu SJ (2006) Halobacterium jilantaiense sp nov., a halophilic archaeon isolated from a saline lake in Inner Mongolia, China. Int J Syst Evol Microbiol 56:2353–2355

    Article  CAS  PubMed  Google Scholar 

  48. Zhang WY, Huo YY, Zhang XQ, Zhu XF, Wu M (2013) Halolamina salifodinae sp nov and Halolamina sauna sp nov., two extremely halophilic archaea isolated from a salt mine. Int J Syst Evol Microbiol 63:4380–4385

    Article  CAS  PubMed  Google Scholar 

  49. Corral P, de la Haba RR, Sanchez-Porro C, Amoozegar MA, Papke RT, Ventosa A (2015) Halorubrum persicum sp nov., an extremely halophilic archaeon isolated from sediment of a hypersaline lake. Int J Syst Evol Microbiol 65:1770–1778

    Article  CAS  PubMed  Google Scholar 

  50. Rasooli M, Naghoni A, Amoozegar MA, Mirfeizi L, Nikou MM, Fazeli SAS, Minegishi H, Ventosa A (2017) Natrinema soli sp nov., a novel halophilic archaeon isolated from a hypersaline wetland. Int J Syst Evol Microbiol 67:2142–2147

    Article  CAS  PubMed  Google Scholar 

  51. Caton TM, Caton IR, Witte LR, Schneegurt MA (2009) Archaeal diversity at the Great Salt Plains of Oklahoma described by cultivation and molecular analyses. Microb Ecol 58:519–528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Angel R, Soares MIM, Ungar ED, Gillor O (2010) Biogeography of soil archaea and bacteria along a steep precipitation gradient. ISME J 4:553–563

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank Osnat Gillor from the Zuckerberg Institute for Water Research, J. Blaustein Institutes for Desert Research, Ben-Gurion University, Sede Boqer Campus, Israel; Ines M Soares, a former colleague from the Zuckerberg Institute for Water Research, J. Blaustein Institutes for Desert Research, Ben-Gurion University, Sede Boqer Campus, Israel; and Sonja Selenska-Pobell, a former colleague of the Institute of Resource Ecology from the Helmholtz-Zentrum Dresden-Rossendorf for collecting and providing the samples. Additionally, we admire the support from the Analytics Group of the Institute of Resource Ecology from the Helmholtz-Zentrum Dresden-Rossendorf.

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  1. Institute of Resource Ecology, Helmholtz-Zentrum Dresden-Rossendorf, Bautzner Landstraße 400, 01328, Dresden, Germany

    Madlen Bachran, Sindy Kluge, Margarita Lopez-Fernandez & Andrea Cherkouk

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  1. Madlen Bachran
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  2. Sindy Kluge
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Correspondence to Margarita Lopez-Fernandez or Andrea Cherkouk.

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Bachran, M., Kluge, S., Lopez-Fernandez, M. et al. Microbial Diversity in an Arid, Naturally Saline Environment. Microb Ecol 78, 494–505 (2019). https://doi.org/10.1007/s00248-018-1301-2

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