Diversity of actinobacteria in the marshes of Ezzemoul and Djendli in northeastern Algeria

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Abstract

The main purpose of this research is to study the microbial diversity of actinobacteria, living in “Ezzemoul” and “Djendli” sebkhas soils. These salt lakes are situated in the east of Algeria and they are microbiologically underexploited. Such unexplored ecological niches have been considered by many authors as sources of novel actinobacteria and bioactive molecules. Actinobacteria play an important role in safeguarding the environment by improving plant growth through nitrogen fixation, biodegradation, and bioremediation. Therefore, studying the diversity and distribution of actinobacteria in such special environments is important for determining the ecological and biotechnological roles of these microorganisms. In this article, we focused on the occurrence and the diversity of actinobacteria from sebkhas using two techniques: cultural and culture-independent (molecular cloning). The latter are based on phylogenetic analysis of the 16S rDNA gene. Thus, the cultural method allowed us to obtain 62 isolates: 40 from the “Ezzemoul” site and 22 from the “Djendli” site. These isolates tolerate mainly 2, 5, and 10% sodium chloride (NaCl) and belong to the genera Nocardiopsis, Streptomyces, and Rhodococcus. Moreover, the molecular cloning gave us 39 clones. Twenty-four clone sequences from “Ezzemoul” site are affiliated to the genera Demequina, Plantactinospora, Friedmanniella, and Mycobacterium. Also, 15 clone sequences from “Djendli” site are related to the genera Marmoricola, Phytoactinopolyspora, Streptomyces, and to an unclassified actinobacterial clone. Some sequences from both sites are related to uncultured clones. In addition to the data provided by the cultural method, molecular cloning allowed us to have additional information about the unknown actinobacteria, uncultured ones as well as on the genera that exist in both sites. So, the cultural method is complementary to the culture-independent one, and their combination revealed an important diversity in targeted saline environments. Furthermore, all new isolated strains that tolerate 10% NaCl may have a very interesting biotechnological potential in the future.

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  • Aberkane M (2014) Ecologie de la Sarcelle marbrée Marmaronetta angustirostris dans les zones humides de l’Est algérien. PhD thesis Badji Mokhtar University Annaba Algeria (in French).

  • Aliat T Kaabeche M Khomri H et al (2016) A Pedological Characterisation of Some Inland Wetlands and Ramsar Sites in Algeria. Land Degrad Dev 27:693–705. doi: 10.1002/ldr.2467

  • Altschul SF Gish W Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410

  • Balla A (2012) Synthèse écologique sur les zones humides algériennes d’importance internationale be “Sites Ramsar”. PhD thesis Batna University Algeria (in French).

  • Bedford BL Walbridge MR Aldous A (1999) Patterns in Nutrient Availability and Plant Diversity of Temperate North American Wet-lands. Ecology 80:2151–2169. doi: 10.2307/176900

  • Bellagoune S (2015) Hivernage du Tadorne de Belon Tadorna tadorna (Anatidés) dans la sebkha de Djendli (Batna Est algérien).PhD thesis Badji Mokhtar University Annaba Algeria (in French).

  • Bennur T Ravi Kumar A Zinjarde SS Javdekar V (2016) Nocardiopsis species: a potential source of bioactive compounds. J Appl Microbiol 120:1–16. doi: 10.1111/jam.12950

  • Borsodi AK Felföldi T Máthé I et al (2013) Phylogenetic diversity of bacterial and archaeal communities inhabiting the saline Lake Red located in Sovata Romania. Extremophiles 17:87–98. doi: 10.1007/s00792-012-0496-2

  • Boughachiche F Rachedi K Duran R et al (2016) Optimization of alkaline protease production by Streptomyces sp. strain isolated from saltpan environment. Afr J Biotechnol 15:1401–1412

  • Cai Y Xue Q Chen Z Zhang R (2009) Classification and salt-tolerance of actinomycetes in the Qinghai lake water and lakeside saline soil. J Sustain Dev 2:107–110

  • Chenchouni H (2009) Place des argiles dans la caractérisation écopédologique du Chott de Djendli (Batna Algérie) et mise en évidence de la relation salinité–répartition des halophytes (in French). In: Proceedings of the 3rd Maghrebin Symposium on Clays ‘SMA. pp 23–25

  • Cocolin L Alessandria V Dolci P et al (2013) Culture independent methods to assess the diversity and dynamics of microbiota during food fermentation. International Journal of Food Microbiology 167:29–43. doi: 10.1016/j.ijfoodmicro.2013.05.008

  • Dastager SG Lee J-C Ju Y-J et al (2008) Marmoricola bigeumensis sp. nov. a member of the family Nocardioidaceae. Int J Syst Evol Microbiol 58:1060–1063. doi: 10.1099/ijs.0.65576-0

  • Dupain R Lanchon R Saint-Arroman JC (2000) Granulats sols ciments et bétons: caractérisation des matériaux de génie civil par les essais de laboratoire (in French). Paris: Casteilla

  • Ebihara H Takada A Kobasa D et al (2006) Molecular Determinants of Ebola Virus Virulence in Mice. PLOS Pathog 2:e73. doi: 10.1371/journal.ppat.0020073

  • Eswaran H Rice T Ahrens R Stewart B. (2002) Soil classification: a global desk reference. Boca Raton: CRC Press

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

  • Fidalgo C Henriques I Rocha J et al (2016) Culturable endophytic bacteria from the salt marsh plant Halimione portulacoides: phylogenetic diversity functional characterization and influence of metal(loid) contamination. Environ Sci Pollut Res 23:10200–10214. doi: 10.1007/s11356-016-6208-1

  • Finster KW Herbert RA Kjeldsen KU et al (2009) Demequina lutea sp. nov. isolated from a high Arctic permafrost soil. Int J Syst Evol Microbiol 59:649–653. doi: 10.1099/ijs.0.004929-0

  • Gagnard J Huguet C Ryser J-P (1988) L’analyse du sol et du végétal dans la conduite de la fertilisation. Le controle de la qualite des fruits (in French).

  • Gasmi M Kitouni M (2017) Optimization of chitinase production by a new Streptomyces griseorubens C9 isolate using response surface methodology. Ann Microbiol 67:175–183. doi: 10.1007/s13213-016-1249-8

  • Ghai R Mizuno CM Picazo A et al (2013) Metagenomics uncovers a new group of low GC and ultra-small marine Actinobacteria. Sci Rep 3:2471. doi: 10.1038/srep02471

  • Guo X Guan X Liu C et al (2016) Plantactinospora soyae sp. nov. an endophytic actinomycete isolated from soybean root [Glycine max (L.) Merr]. Int J Syst Evol Microbiol 66:2578–2584. doi: 10.1099/ijsem.0.001088

  • Hamada M Tamura T Yamamura H et al (2013) Demequina flava sp. nov. and Demequina sediminicola sp. nov. isolated from sea sediment. Int J Syst Evol Microbiol 63:249–253. doi: 10.1099/ijs.0.039297-0

  • Hocinat A Boudemagh A (2015) Biodegradation of commercial Ortiva fungicide by isolated actinomycetes from the activated sludge. Desalination Water Treat 57:6091–6097. doi: 10.1080/19443994.2015.1022799

  • Hozzein WN (2015) Biodiversity of Halophilic and Halotolerant Actinobacteria. In: DK Maheshwari M Saraf (Eds.) Halophiles Sustainable Development and Biodiversity (pp.1-28). Switzerland: Springer International Publishing

  • Iwai K Aisaka K Suzuki M (2010) Friedmanniella luteola sp. nov. Friedmanniella lucida sp. nov. Friedmanniella okinawensis sp. nov. and Friedmaniella sagamiharensis sp. nov. isolated from spiders. Int J Syst Evol Microbiol 60:113–120. doi: 10.1099/ijs.0.007815-0

  • Ji Y Chunyu W-X Li E-Y et al (2017) Phytoactinopolyspora halotolerans sp. nov. a halotolerant actinobacterium isolated from a saline soil in Xinjiang northwest of China. Antonie Van Leeuwenhoek 111:27–34. doi: 10.1007/s10482-017-0923-6

  • Jose PA Jebakumar SRD (2013) Phylogenetic appraisal of antagonistic slow growing actinomycetes isolated from hypersaline inland solar salterns at Sambhar salt Lake India. Front Microbiol 4:190. doi: 10.3389/fmicb.2013.00190

  • Kharroub K (2007) Identification et étude moléculaire des bactéries et des archéobactéries aérobies halophiles de la sebkha Ezzemoul (Ain M’Lila). PhD thesis Mentouri University Constantine Algeria (in French)

  • Kim S-J Hamada M Ahn J-H et al (2016) Friedmanniella aerolata sp. nov. isolated from air. Int J Syst Evol Microbiol 66:1970–1975. doi: 10.1099/ijsem.0.000973

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. doi: 10.1007/BF01731581

  • Kitouni M Boudemagh A Oulmi L et al (2005) Isolation of actinomycetes producing bioactive substances from water soil and tree bark samples of the north–east of Algeria. J Mycol Médicale-Journal Med Mycol 15:45–51

  • Lahoum A Verheecke-Vaessen C Bouras N et al (2017) Taxonomy of mycelial actinobacteria isolated from Saharan soils and their efficiency to reduce aflatoxin B1 content in a solid-based medium. Ann Microbiol 67:231–237. doi: 10.1007/s13213-017-1253-7

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: E Stackebrandt M Good-fellow (Eds.) Nucleic acid techniques in bacterial systematics (pp.115–175). New York: John Wiley and Sons

  • Larkin MA Blackshields G Brown NP et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. doi: 10.1093/bioinformatics/btm404

  • Lawson PA Collins MD Schumann P et al (2000) New LL-diaminopimelic acid-containing actinomycetes from hypersaline heliothermal and meromictic Antarctic Ekho Lake: Nocardioides aquaticus sp. nov. and Friedmanniella [correction of Friedmannielly] lacustris sp. nov. Syst Appl Microbiol 23:219–229

  • Lee JY Hwang BK (2002) Diversity of antifungal actinomycetes in various vegetative soils of Korea. Can J Microbiol 48:407–417. doi: 10.1139/w02-025

  • Lee SD Lee DW Ko Y-H (2011) Marmoricola korecus sp. nov. Int J Syst Evol Microbiol 61:1628–1631. doi: 10.1099/ijs.0.025460-0

  • Lee S-Y Im W-T Kang M-S et al (2016) Marmoricola ginsengisoli sp. nov. and Marmoricola pocheonensis sp. nov. isolated from a ginseng-cultivating field. Int J Syst Evol Microbiol 66:1996–2001. doi: 10.1099/ijsem.0.000977

  • Li J Zhao G-Z Long L-J et al (2012) Rhodococcus nanhaiensis sp. nov. an actinobacterium isolated from marine sediment. Int J Syst Evol Microbiol 62:2517–2521. doi: 10.1099/ijs.0.038067-0

  • Li L Ma J-B Abdalla Mohamad O et al (2015) Phytoactinopolyspora endophytica gen. nov. sp. nov. a halotolerant filamentous actinomycete isolated from the roots of Glycyrrhiza uralensis F. Int J Syst Evol Microbiol 65:2671–2677. doi: 10.1099/ijs.0.000322

  • Lv Z. Zhang L. Li Y et al (2006) Biodiversity of halophilic actinomycetes of Cangzhou salty environments. 26(1):1-6. J Hebei Univ Nat Sci Ed 26:1–6

  • Maszenan AM Seviour RJ Patel BK et al (1999) Friedmanniella spumicola sp. nov. and Friedmanniella capsulata sp. nov. from activated sludge foam: gram-positive cocci that grow in aggregates of repeating groups of cocci. Int J Syst Bacteriol 49 Pt 4:1667–1680. doi: 10.1099/00207713-49-4-1667

  • Matsumoto A Nakai K Morisaki K et al (2010) Demequina salsinemoris sp. nov. isolated on agar media supplemented with ascorbic acid or rutin. Int J Syst Evol Microbiol 60:1206–1209. doi: 10.1099/ijs.0.012617-0

  • Meklat A Sabaou N Zitouni A et al (2011) Isolation Taxonomy and Antagonistic Properties of Halophilic Actinomycetes in Saharan Soils of Algeria. Appl Environ Microbiol 77:6710–6714. doi: 10.1128/AEM.00326-11

  • Naikpatil SV Rathod JL (2011) Selective isolation and antimicrobial activity of rare actinomycetes from mangrove sediment of Karwar. J Ecobiotechnology 3:48–53

  • Neffar S Chenchouni H Si Bachir A (2016) Floristic composition and analysis of spontaneous vegetation of Sabkha Djendli in northeast Algeria. Plant Biosyst - Int J Deal Asp Plant Biol 150:396–403. doi: 10.1080/11263504.2013.810181

  • Norris PR (2012) Class Acidimicrobiia. In: M Goodfellow P Kämpfer HJ Busse ME Trujillo K Suzuki W Ludwig WB Whitman (Eds.) Bergey’s Manual of Systematic Bacteriology 2nd edn (pp.1968–1969). New York: Springer

  • Okoro CK Brown R Jones A et al (2009) Diversity of culturable actinomycetes in hyper-arid soils of the Atacama Desert Chile. Antonie Van Leeuwenhoek 95:121–133. doi: 10.1007/s10482-008-9295-2

  • Oskay M Tamer AU Azeri C et al (2004) International Conference on the Great Himalayas: Climate Health Ecology Management and Conservation Kathmandu Organized by Kathmandu University and the Aquatic Ecosystem Health and Management Society Canada. Afr J Biotechnol 3:441–446

  • Pandey B Ghimire P Agrawal VP (2004) International Conference on the Great Himalayas: Climate Health Ecology Management and Conservation Kathmandu Organized by Kathmandu University and the Aquatic Ecosystem Health and Management Society Canada.

  • Park S Jung Y. Won S. Yoon J. (2016) Demequina litorisediminis sp. nov. isolated from a tidal flat and emended description of the genus Demequina. Int J Syst Evol Microbiol 66:4197–4203. doi: 10.1099/ijsem.0.001335

  • Peeters C Depoorter E Praet J Vandamme P (2016) Extensive cultivation of soil and water samples yields various pathogens in patients with cystic fibrosis but not Burkholderia multivorans. J Cyst Fibros 15:769–775. doi: 10.1016/j.jcf.2016.02.014

  • Pham VHT Kim J (2012) Cultivation of unculturable soil bacteria. Trends in Biotechnology 30:475–484. doi: 10.1016/j.tibtech.2012.05.007

  • Piao Z Yang L Zhao L Yin S (2008) Actinobacterial Community Structure in Soils Receiving Long-Term Organic and Inorganic Amendments. Appl Environ Microbiol 74:526–530. doi: 10.1128/AEM.00843-07

  • Pochon J Tardieux P (1962) Techniques d’analyse en microbiologie du sol (in French)

  • Queipo-Ortuño MI Colmenero JDD Macias M et al (2008) Preparation of Bacterial DNA Template by Boiling and Effect of Immunoglobulin G as an Inhibitor in Real-Time PCR for Serum Samples from Patients with Brucellosis. Clinical and Vaccine Immunology 15:293–296. doi: doi:10.1128/CVI.00270-07

  • Rengasamy P (2006) World salinization with emphasis on Australia. Journal of Experimental Botany. 57:1017–1023. doi: DOI:10.1093/jxb/erj108.

  • Richards LA (1954) Diagnostic and improvement of saline and alkaline soils. U.S Department of agriculture Washington D.C

  • Sahraoui N Ballif M Zelleg S et al (2011) Mycobacterium algericum sp. nov. a novel rapidly growing species related to the Mycobacterium terrae complex and associated with goat lung lesions. Int J Syst Evol Microbiol 61:1870–1874. doi: 10.1099/ijs.0.024851-0

  • Saitou N Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. doi: 10.1093/oxfordjournals.molbev.a040454

  • Schumann P Prauser H Rainey FA et al (1997) Friedmanniella antarctica gen. nov. sp. nov. an LL-diaminopimelic acid-containing actinomycete from Antarctic sandstone. Int J Syst Bacteriol 47:278–283. doi: 10.1099/00207713-47-2-278

  • Shirling EB Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340

  • Song Z Zhi X Li W et al (2009) Actinobacterial Diversity in Hot Springs in Tengchong (China) Kamchatka (Russia) and Nevada (USA). Geomicrobiol J 26:256–263. doi: 10.1080/01490450902892373

  • Stach JEM Maldonado LA Ward AC et al (2003) New primers for the class Actinobacteria: application to marine and terrestrial environments. Environ Microbiol 5:828–841. doi: 10.1046/j.1462-2920.2003.00483.x

  • Stackebrandt E Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–5

  • Sudnitsyn II (2009) Specificity of actinomycetes in salt-affected soils. Eurasian Soil Sci 42:235–236. doi: 10.1134/S106422930902015X

  • Tamura K Stecher G Peterson D et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

  • Táncsics A Máthé I Benedek T et al (2017) Rhodococcus sovatensis sp. nov. an actinomycete isolated from the hypersaline and heliothermal Lake Ursu. Int J Syst Evol Microbiol 67:190–196. doi: 10.1099/ijsem.0.001514

  • Tuo L Pan Z Li F-N et al (2016) Friedmanniella endophytica sp. nov. an endophytic actinobacterium isolated from bark of Kandelia candel. Int J Syst Evol Microbiol 66:3057–3062. doi: 10.1099/ijsem.0.001146

  • Urzì C Salamone P Schumann P Stackebrandt E (2000) Marmoricola aurantiacus gen. nov. sp. nov. a coccoid member of the family Nocardioidaceae isolated from a marble statue. Int J Syst Evol Microbiol 50:529–536

  • Valenzuela-Encinas C Neria-González I Alcántara-Hernández RJ et al (2009) Changes in the bacterial populations of the highly alkaline saline soil of the former lake Texcoco (Mexico) following flooding. Extremophiles 13:609–621. doi: 10.1007/s00792-009-0244-4

  • Vartoukian SR Palmer RM Wade WG (2010) Strategies for culture of ‘unculturable’ bacteria. FEMS microbiology letters 309:1–7

  • Vasireddy R Vasireddy S Brown-Elliott BA et al (2016) Mycobacterium arupenseMycobacterium heraklionense and a Newly Proposed Species “Mycobacterium virginiense” sp. nov. but Not Mycobacterium nonchromogenicum as Species of the Mycobacterium terrae Complex Causing Tenosynovitis and Osteomyelitis. J Clin Microbiol 54:1340–1351. doi: 10.1128/JCM.00198-16

  • Wright ES Yilmaz LS Noguera DR (2012) DECIPHER a Search-Based Approach to Chimera Identification for 16S rRNA Sequences. Appl Environ Microbiol 78:717–725. doi: 10.1128/AEM.06516-11

  • Yoon S-H Ha S-M Kwon S et al (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. doi: 10.1099/ijsem.0.001755

  • Zhang X Zhang J Zhang Y et al (2013) Friedmanniella flava sp. nov. a soil actinomycete. Int J Syst Evol Microbiol 63:1771–1775. doi: 10.1099/ijs.0.043984-0

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