Abstract
A polyphasic study was undertaken to establish the taxonomic status of two Modestobacter strains isolated from the surface of deteriorated sandstone of a historic building in Salamanca, Spain. The strains, isolates MDVD1T and MON 3.1T, were found to have chemotaxonomic and morphological properties consistent with their classification in the genus Modestobacter and to form distinct phyletic lines in the Modestobacter 16S rRNA gene tree. Isolate MDVD1T was found to be closely related to the type strain of Modestobacter versicolor (98.7 % similarity) and isolate MON 3.1T to the type strain of Modestobacter multiseptatus (98.6 % similarity). The isolates were distinguished readily from one another and from the Modestobacter type strains by a broad range of phenotypic properties, by qualitative and quantitative differences in fatty acid profiles and by BOX fingerprint patterns. On the basis of these data, it is proposed that the isolates be classified in the genus Modestobacter as Modestobacter lapidis sp. nov. and Modestobacter muralis sp. nov., with isolates MON 3.1T (CECT 8844T = DSM 100206T) and MDVD1T (CECT 8845T = DSM 100205T) as the respective type strains.
Similar content being viewed by others
References
Ahrens R, Moll G (1970) Ein neues knospendes Bakterium aus der Ostsee. Arch Mikrobiol 70:243–263
Carro L, Spröer C, Alonso P, Trujillo ME (2012) Diversity of Micromonospora strains isolated from nitrogen fixing nodules and rhizosphere of Pisum sativum analyzed by multilocus sequence analysis. Syst Appl Microbiol 35:73–80
Chouaia B, Crotti E, Brusetti L et al (2012) Genome sequence of Blastococcus saxobsidens DD2, a stone inhibiting bacterium. J Bacteriol 194:2752–2753
Eppard M, Krumbein WE, Koch C, Rhiel E, Staley JT, Stackebrandt E (1996) Morphological, physiological and molecular characterization of actinomycetes isolated from dry soil, rocks and monument surfaces. Arch Microbiol 166:12–22
Essoussi I, Ghodbane-Gtari F, Amairi H, Sghaier H, Jaouani A, Brusetti L, Daffonchio D, Boudabous A, Gtari M (2010) Esterase as an enzyme signature of Geodermatophilus adaptability to Sahara desert stones and monuments. J Appl Microbiol 108:1723–1732
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 39:383–391
Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416
Gtari M, Essoussi I, Maaoui R, Sghaier H, Boujmil R et al (2012) Contrasted resistance of stone dwelling Geodermatophilaceae species to stresses known to give rise to reactive oxygen species. FEMS Microbiol Ecol 80:566–577
Hasegawa T, Takizawa M, Tamida S (1983) A rapid analysis for chemical grouping of aerobic actinomycetes. J Gen Appl Microbiol 29:319–322
Jones K (1949) Fresh isolates of actinomycetes in which the presence of the sporogenous aerial mycelia is a fluctuating characteristic. J Bacteriol 57:141–145
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
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
Lechevalier MP, De Biévre C, Lechevalier HA (1977) Chemotaxonomy of aerobic actinomycetes: phospholipid composition. Biochem Syst Ecol 5:249–260
Luedemann GM (1968) Geodermatophilus, a new genus of the Dermatophilaceae (Actinomycetes). J Bacteriol 96:1848–1858
Luedemann GM (1971) Micromonospora purpureochromogenes (Waksman and Curtis 1916) comb. Nov. (subjective synonym, Micromonospora fusca Jensen 1932). Int J Syst Bacteriol 21:240–247
Mandel M, Marmur J (1968) Use of ultraviolet absorbance temperature profile for determining the guanine plus cytosine content of DNA. Methods Enzymol 12B:195–206
Meier-Kolthoff JP, Göker M, Spöer C, Klenk H-P (2013) When should a DDH experiment be mandatory in microbial taxonomy? Arch Microbiol 95:413–418
Mevs U, Stackebrandt E, Schumann P, Gallikowski CA, Hirsch P (2000) Modestobacter multiseptatus sp. nov., a budding actinomycete from soils of the Asgard Range (Transantarctic Mountains). Int J Syst Evol Microbiol 50:337–346
Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett JH (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241
Murray PR, Baron EJ, Phaller MA, Ternover JC, Yolkken RJ (1999) Manual of clinical microbiology, 7th edn. ASM Press, Washington DC
Nie G-X, Ming H, Li S, Zhou E-M, Cheng J, Yu TT, Zhang J, Feng H-G, Tang S-K, Li W-J (2012) Geodermatophilus nigrescens sp. nov., isolated from a dry-hot valley. Antonie Van Leeuwenhoek 101:811–817
Normand P (2006) Geodermatophilaceae fam. nov., a formal description. Int J Syst Evol Microbiol 56:2277–2278
Normand P, Benson DR (2012) Family IV. Geodermatophilaceae 2006, 2277VP (Effective publication: Normand, Orso, Jeannin, Chapelon, Dawson, Evtuschenko and Misra, 1996, 8). In: Goodfellow M, Kämpfer P, Busse H-J, Trujillo MR, Suzuki K-I, Ludwig W, Whitman WB (eds) Bergey’s manual of systematic bacteriology, Part A, vol 5, 2nd edn. Springer, New York, p 528
Qin S, Bian G-K, Zhang Y-J, Ying K, Cao C-L, Liu C-H, Dai C-C, Jiang J-H (2013) Modestobacter roseus sp. nov., an endophytic actinomycete isolated from the coastal halophyte Salicornia europea Linn, and emended description of the genus Modestobacter. Int J Syst Microbiol 63:2197–2202
Reddy GSN, Potrafka RM, Garcia-Pichel F (2007) Modestobacter versicolor sp. nov., an actinobacterium from biological soil crusts that produce melanins under oligotrophy, with emended descriptions of the genus Modestobacter and Modestobacter multiseptatus Mevs et al. 2000. Int J Syst Evol Microbiol 57:2000–2014
Rohde A (2011) Microscopy. Methods Microbiol 38:61–100
Saitou N, Nei M (1987) The neighbour-joining method: a new method for constructing phylogenetic trees. Mol Biol Evol 4:406–425
Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. MIDI technical note 101, MIDI Inc., Newark
Sen A, Daubin E, Abbro D, Gifford I, Berry AM, Normand P (2014) Phylogeny of the class Actinobacteria revisited in light of complete genomes. The orders ‘Frankiales’ and Micrococcales should be split into coherent entities: proposal of Frankiales ord. nov., Geodermatophilales ord. nov, Acidothermales ord. nov. and Nakamurellales ord. nov. Int J Syst Evol Microbiol 64:3821–3832
Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340
Sierra G (1957) A simple method for the detection of lipolytic activity of microorganisms and some observations on the influence of contact between cells and fatty substrates. Antonie Van Leeuwenhoek 23:15–22
Staneck JL, Roberts GD (1974) Simplified approach to the identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 28:226–231
Tamura K, Peterson D, Peterson N, Stecker G, Nei M, Kumar S (2011) MEGA 5: molecular evolution genetics analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Trujillo ME, Alonso-Vega P, Rodriguez R, Carro L, Cerda E, Alonso P, Martinez-Molina E (2010) The genus Micromonospora is widespread in legume root nodules: the example of Lupinus angustifolius. ISME J 4:1265–1281
Urzi C, Brusetti P, Salamone C, Sorlini F, Stackebrandt E, Daffenchio D (2001) Biodiversity of Geodermatophilaceae isolated from altered stones and monuments in the Mediterranean basin. Environ Microbiol 3:471–479
Urzi C, La Cono V, Stackebrandt E (2004) Design and application of two oligonucleotide probes in the identification of Geodermatophilaceae strains using fluorescence in situ hybridization. Environ Microbiol 6:678–685
Versalovic J, Scheider M, De Bruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol 5:25–40
Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O et al (1987) International Committee on Systematic Bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464
Xiao J, Luo Y, Yu J, Xie J (2011) Modestobacter marinus sp. nov., a psychrotolerant actinobacterium from deep-sea, and emended description of the genus Modestobacter. Int J Syst Evol Microbiol 61:1704–17010
Acknowledgments
Kanungnid Bukarasam is grateful for a scholarship from the Thai Royal Government and Michael Goodfellow for an Emeritus Fellowship from The Leverhulme Trust. ME Trujillo was financed by the Junta de Castilla and Leon (SA100A7) and Universidad de Salamanca, (Programa 1, 18KAZG/463AC01).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
10482_2015_482_MOESM1_ESM.pptx
Figure S1. Two-dimensional thin-layer chromatography of polar lipids of strains MDVD1T (a, b, c) and MON 3.1T (d, e, f) stained with ninhydrin, molybdophosphoric acid and anisaldehyde, respectively. Abbrevations: DPG, diphosphatidylglycerol; PE, phosphatidylethanolamine; PG, phosphatidylglycerol; PI, phosphatidylinositol; PIM, phosphatidylinositol mannoside; PL1 and PL2, polar lipids (PPTX 1314 kb)
Rights and permissions
About this article
Cite this article
Trujillo, M.E., Goodfellow, M., Busarakam, K. et al. Modestobacter lapidis sp. nov. and Modestobacter muralis sp. nov., isolated from a deteriorated sandstone historic building in Salamanca, Spain. Antonie van Leeuwenhoek 108, 311–320 (2015). https://doi.org/10.1007/s10482-015-0482-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-015-0482-7