Abstract
A novel halophilic actinobacterium strain, designated H8T, was isolated from a Saharan soil sample collected in El-Goléa, South Algeria. Strain H8T was identified as representing a new genus using a polyphasic taxonomic approach. Phylogenetic analysis revealed that strain H8T shared the highest degree of 16S rRNA gene sequence similarity with ‘Mzabimyces algeriensis’ DSM 46680T (93.0 %), Saccharopolyspora ghardaiensis DSM 45606T (91.2 %), Halopolyspora alba DSM 45976T (90.8 %) and Actinopolyspora mortivallis DSM 44261T (90.0 %). The strain was found to grow optimally at 28–35 °C, at pH 6.0–7.0, and in the presence of 15–25 % (w/v) NaCl. The substrate mycelium was observed to be well developed and fragmented in liquid medium and on solid medium. The aerial mycelium was observed to be moderately abundant and to form long chains with non-motile, smooth-surfaced and ovoid or spherical spores at maturity. The cell wall of strain H8T was found to contain meso-diaminopimelic acid. The whole-cell hydrolysates were found to mainly contain arabinose and galactose. The diagnostic phospholipid detected was phosphatidylcholine, and MK-9(H4), MK-9(H2) and MK-10(H2) were found to be the predominant menaquinones. The major cellular fatty acids were determined to be anteiso-C17:0 and iso-C15:0. The genomic DNA G+C content of strain H8T was determined to be 71.3 mol%. The genotypic and phenotypic data showed that the strain represents a novel genus and species, for which the name Bounagaea algeriensis gen. nov., sp. nov. is proposed, with the type strain H8T (=DSM 45966T = CECT 8470T).
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References
Becker B, Lechevalier MP, Gordon RE, Lechevalier HA (1964) Rapid differentiation between Nocardia and Streptomyces by paper chromatography of whole-cell hydrolysates. J Appl Microbiol 12:421–423
Bouras N, Meklat A, Zitouni A, Mathieu F, Schumann P, Spröer C, Sabaou N, Klenk HP (2015) Nocardiopsis algeriensis sp. nov., an alkalitolerant actinomycete isolated from Saharan soil. Antonie Van Leeuwenhoek 107:313–320
Chun J, Bae KS, Moon EY, Jung SO, Lee HK, Kim SJ (2000) Nocardiopsis kunsanensis sp. nov., a moderately halophilic actinomycete isolated from a saltern. Int J Syst Evol Microbiol 50:1909–1913
Coenye T, Falsen E, Vancanneyt M, Hoste B, Govan JR, Kersters K, Vandamme P (1999) Classification of Alcaligenes faecalis-like isolates from the environment and human clinical samples as Ralstonia gilardii sp. nov. Int J Syst Bacteriol 49:405–413
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Fitch WM (1977) On the problem of discovering the most parsimonious tree. Am Nat 111:223–257
Goodfellow M (1971) Numerical taxonomy of some nocardioform bacteria. J Gen Microbiol 69:33–90
Goodfellow M, Trujillo ME (2012) Family I. Actinopolysporaceae. In: Goodfellow M, Kämpfer P, Busse H-J, Trujillo ME, Suzuki K-I, Ludwig W, Whitman WB (eds) Bergey’s manual of systematic bacteriology, vol 5. Springer, New York, pp 163–170
Gordon RE, Barnett DA (1977) Resistance to rifampicin and lysozyme of strains of some species of Mycobacterium and Nocardia as a taxonomic tool. Int J Syst Bacteriol 27:176–178
Gordon RE, Barnett DA, Handerhan JE, Pang CHN (1974) Nocardia coeliaca, Nocardia autotrophica, and the nocardin strain. Int J Syst Bacteriol 24:54–63
Hamedi J, Mohammadipanah F, Ventosa A (2013) Systematic and biotechnological aspects of halophilic and halotolerant actinomycetes. Antonie Van Leeuwenhoek 17:1–13
Jang KH, Nam SJ, Locke JB, Kauffman CA, Beatty DS, Paul LA, Fenical W (2013) Anthracimycin, a potent anthrax antibiotic from a marine-derived actinomycete. Angew Chem Int Ed Engl 52:7822–7824
Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism, vol 3. Academic Press, New York, pp 21–132
Kelly KL, Judd DB (1976) Color. Universal language and dictionary of names (National Bureau of Standards special publication 440). US Department of Commerce, Washington
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 data-base with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721
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
Kroppenstedt RM (1982) Separation of bacterial menaquinones by HPLC using reverse phase (RP18) and a silver loaded ion exchanger as stationary phases. J Liq Chromatogr 5:2359–2367
Kroppenstedt RM (1985) Fatty acid and menaquinone analysis of actinomycetes and related organisms. In: Goodfellow M, Minnikin DE (eds) Chemical methods in bacterial systematics. Academic Press, London, pp 173–179
Labeda DP, Goodfellow M (2012) Family I. Pseudonocardiaceae. In: Goodfellow M, Kämpfer P, Busse H-J, Trujillo ME, Suzuki K-I, Ludwig W, Whitman WB (eds) Bergey’s manual of systematic bacteriology, vol 5. Springer, New York, Dordrecht, Heidelberg, London, pp 1302–1445
Lai H, Wei X, Jiang Y, Chen X, Li Q, Jiang Y, Jiang C, Gillerman L (2014) Halopolyspora alba gen. nov., sp. nov., isolated from sediment. Int J Syst Evol Microbiol 64:2775–2780
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) CLUSTAL W and CLUSTAL X version 2. Bioinformatics 23:2947–2948
Lechevalier MP, Lechevalier HA (1970) Chemical composition as a criterion in the classification of aerobic actinomycetes. Int J Syst Bacteriol 34:435–444
Lechevalier MP, de Bièvre C, Lechevalier HA (1977) Chemotaxonomy of aerobic actinomycetes: phospholipid composition. Biochem Syst Ecol 5:249–260
Liu D, Coloe S, Baird R, Pedersen J (2000) Rapid mini-preparation of fungal DNA for PCR. J Clin Microbiol 38:471
Mao J, Wang J, Dai H-Q, Zhang Z-D, Tang Q-Y, Ren B, Yang N, Goodfellow M, Zhang L-X, Liu Z-H (2011) Yuhushiella deserti gen. nov., sp. nov., a new member of the suborder Pseudonocardineae. Int J Syst Evol Microbiol 61:621–630
Marchal N, Bourdon JL, Richard CL (1987) Les milieux de culture pour l’isolement et l’identification biochimique des bactéries. Doin Press, Paris
Meklat A, Bouras N, Zitouni A, Mathieu F, Lebrihi A, Schumann P, Spröer C, Klenk HP, Sabaou N (2012) Actinopolyspora algeriensis sp. nov., a novel halophilic actinomycete isolated from a Saharan soil. Extremophiles 16:771–776
Meklat A, Bouras N, Zitouni A, Mathieu F, Lebrihi A, Schumann P, Spröer C, Klenk HP, Sabaou N (2013a) Actinopolyspora saharensis sp. nov., a novel halophilic actinomycete isolated from a Saharan soil of Algeria. Antonie Van Leeuwenhoek 103:771–776
Meklat A, Bouras N, Zitouni A, Mathieu F, Lebrihi A, Schumann P, Spröer C, Klenk HP, Sabaou N (2013b) Actinopolyspora mzabensis sp. nov., a halophilic actinomycete isolated from an Algerian Saharan soil. Int J Syst Evol Microbiol 63:3787–3792
Meklat A, Bouras N, Zitouni A, Mathieu F, Lebrihi A, Schumann P, Spröer C, Klenk HP, Sabaou N (2013c) Actinopolyspora righensis sp. nov., a novel halophilic actinomycete isolated from Saharan soil in Algeria. Antonie Van Leeuwenhoek 104:301–307
Meklat A, Bouras N, Zitouni A, Sabaou N, Mathieu F, Schumann P, Spröer C, Klenk HP (2014a) Saccharopolyspora ghardaiensis sp. nov., an extremely halophilic actinomycete isolated from Algerian Saharan soil. J Antibiotics 67:299–303
Meklat A, Bouras N, Riba A, Zitouni A, Mathieu F, Rhode M, Schumann P, Spröer C, Klenk HP, Sabaou N (2014b) Streptomonospora algeriensis sp. nov., a halophilic actinomycete isolated from soil in Algeria. Antonie Van Leeuwenhoek 106:287–292
Mesbah M, Premachandran U, Whitman WB (1989) Precise measurement of the G+C content of deoxyribonucleic acid by high-performance liquid chromatography. Int J Syst Bacteriol 39:159–167
Minnikin DE, Patel PV, Alshamaony L, Goodfellow M (1977) Polar lipid composition in the classification of Nocardia and related bacteria. Int J Syst Bacteriol 27:104–117
Minnikin DE, Hutchinson IG, Caldicott AB, Goodfellow M (1980) Thin layer chromatography of methanolysates of mycolic acid-containing bacteria. J Chromatogr A 188:221–233
Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett JH (1984) An integrated procedure for the extraction of isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241
Rainey FA, Ward-Rainey N, Kroppenstedt RM, Stackebrandt E (1996) The genus Nocardiopsis represents a phylogenetically coherent taxon and a distinct actinomycete lineage: proposal of Nocardiopsaceae fam. nov. Int J Syst Bacteriol 46:1088–1092
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Saker R, Bouras N, Zitouni A, Ghoul M, Rohde M, Schumann P, Spröer C, Sabaou N, Klenk HP (2014) Mzabimyces algeriensis gen. nov., sp. nov., a halophilic filamentous actinobacterium isolated from a Saharan soil, and proposal of Mzabimycetaceae fam. nov. Antonie Van Leeuwenhoek 106:1021–1030
Saker R, Bouras N, Meklat A, Zitouni A, Schumann P, Spröer C, Klenk HP, Sabaou N (2015) Actinopolyspora biskrensis sp. nov., a novel halophilic actinomycete isolated from northern Sahara. Curr Microbiol 70:423–428
Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. Technical note 101. Microbial ID, Newark
Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tian SZ, Pu X, Luo G, Zhao LX, Xu LH, Li WJ, Luo Y (2013) Isolation and characterization of new p-Terphenyls with antifungal, antibacterial, and antioxidant activities from halophilic actinomycete Nocardiopsis gilva YIM 90087. J Agric Food Chem 61:3006–3012
Tian S, Yang Y, Liu K, Xiong Z, Xu L, Zhao L (2014) Antimicrobial metabolites from a novel halophilic actinomycete Nocardiopsis terrae YIM 90022. Nat Prod Res 28:344–346
Waksman SA (1961) Classification, identification, and descriptions of genera and species. The actinomycetes, vol 2. Williams & Wilkins, Baltimore, pp 331–332
Yoshida M, Matsubara K, Kudo T, Horikoshi K (1991) Actinopolyspora mortivallis sp. nov., a moderately halophilic actinomycete. Int J Syst Bacteriol 41:15–20
Zhao LX, Huang SX, Tang SK, Jiang CL, Duan Y, Beutler JA, Henrich CJ, McMahon JB, Schmid T, Blees JS, Colburn NH, Rajski SR, Shen B (2011) Actinopolysporins A-C and tubercidin as a Pdcd4 stabilizer from the halophilic actinomycete Actinopolyspora erythraea YIM 90600. J Nat Prod 74:1990–1995
Zhi XY, Li WJ, Stackebrandt E (2009) An update of the structure and 16S rRNA gene sequence-based definition of higher ranks of the class Actinobacteria, with the proposal of two new suborders and four new families and emended descriptions of the existing higher taxa. Int J Syst Evol Microbiol 59:589–608
Acknowledgments
The authors are grateful to Gabriele Pötter (DSMZ) for growing Bounagaea algeriensis cultures and for assistance with chemotaxonomic analyses.
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The authors declare that there are no conflicts of interest to declare.
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This article does not contain any studies with human participants and/or animals performed by any of the authors. The formal consent is not required in this study.
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This work was supported by the Ministère de l’Enseignement Supérieur et de la Recherche Scientifique (MESRS) of Algeria. The funder had no role in study design, data collection and analyses, preparation of the manuscript or decision to publish.
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Meklat, A., Bouras, N., Mokrane, S. et al. Bounagaea algeriensis gen. nov., sp. nov., an extremely halophilic actinobacterium isolated from a Saharan soil of Algeria. Antonie van Leeuwenhoek 108, 473–482 (2015). https://doi.org/10.1007/s10482-015-0500-9
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DOI: https://doi.org/10.1007/s10482-015-0500-9