Geodermatophilaceae

The Geodermatophilaceae family [Normand 2006], that belongs to the order Actinobacteria, is one of the most common bacterial groups associated to carbonatic stone biodeterioration [Urzì et al. 2001; Urzì & Realini 1999]. These actinobacteria have been found growing upon surfaces of important monuments such as Bari’s cathedral (Italy), ancient walls of the old city of Cagliari (Italy; Figure 1), Herberstein castle (Austria), medieval glasses from Stockkämpen church (Germany), marble surfaces from Ephesus (Turkey), as well as on several of the Unesco world heritage sites such as the Burgos castle (Spain) and the Maya temples (Mexico) [Garcia-Vallés et al., 2000; Gurtner et al., 2000; Ortega-Morales et al., 2005; Rolleke et al., 1999; Urzì et al. 2001]. Geodermatophilaceae have been associated to different stone materials like marbles, dolomites and calcarenites [Urzì et al. 2001] (Figure 1). On these monuments and stones, due to their pigmentations, Geodermatophilaceae provoke alteration of the original color of the stone surface; moreover they are able to damage stones by biopitting deterioration (Figure 1).

The family Geodermatophilaceae comprises three genera: Geodermatophilus [Luedemann, 1968], Blastococcus [Ahrens & Moll, 1970] and the recently discovered Modestobacter [Mevs et al., 2000]. Bacteria belonging to these three genera are Gram positive Actinobacteria, aerobic, chemoorganotrophs, mesophiles with a rudimentary mycelium. Their peptidoglycan contains meso-diaminopimelic acid. The generation time of Modestobacter versicolor is 6.4 – 6.6 hours [Reddy et al., 2007]. Cells belong to two morphological stages [Ishiguro & Wolfe, 1970, 1974]: i) motile short irregular rods called R form, that develop into pairs and form multiseptate short filaments, with rare bud-like cells and ii) irregular coccoid cell clusters named C form that can form extensive biofilms (Figure 2).

The major difference between C- and R-forms is in cell envelope structure. Moreover, short rods are motile by means of flagella, while multicellular structures that tend to be sessile. In stationary liquid cultures, well-developed sheaths may be produced. A variety of mono- and divalent cations can induce a change from the R-form to the C-form and also maintain the organism in the C form: these are NH4+, Li+, Na+, Rb+, K+, Ca2+, Mg2+ and Sr2+ [Ishiguro & Wolfe, 1974]. A variety of organic amines also induce morphogenesis [Ishiguro & Wolfe, 1974]. The uptake of cations is accompanied by extrusion of intracellular protons, causing an increase in intracellular pH [Ishiguro & Wolfe, 1974].

Modestobacter and Blastococcus are found in extreme dry regions such as the Negev, Sonoran, and Sahara deserts [Hungate et al., 1987; Eppard et al., 1996; Garrity, 1996; Rainey et al., 2005]; other strains were isolated from varnish rocks from Rocky Mountains (USA) [Kuhlman et al., 2005a], Mediterranean regions (Italy, Greece, Turkey, Spain, Malta) [Urzì et al. 2001], cold regions (Antarctica, Svalbard Islands, Mount Everest) [Mevs et al., 2000]. However, rare strains affiliated to this family were occasionally retrieved from deep-ocean sediments (Palau, Korea), plant leaves (Japan), sea water (Baltic) [Ahrens & Moll, 1970], temperate or tropical soils (USA, Singapore, China, Australia, Georgia and Japan). Some strains were isolated also from biodeteriorated frescoes in Austria (Herberstein) and Germany (Greene) [Gurtner et al., 2000].

These genera are frequently associated to limestone and carbonatic rock surfaces. On these stones their growth is favored by the intrinsic porosity and discontinuity of the material that is easily fragmented by biological and physico-chemical processes. They grow under very diverse environmental conditions allowing many studies on their physiology and genome regulation. Geodermatophilaceae are strongly colored with pink, orange, brown or black pigments (Figure 3). M. versicolor produces two pigments: a brown eumelanin and a pink carotenoid [Reddy et al., 2005]. Their production seems to be independent of salt concentration, growth phase, illumination conditions and to be enhanced by UV irradiation and by starvation [Kuhlman et al., 2005b].

Various Geodermatophilaceae from Sonoran Desert and a non-arid soil from a Louisiana forest showed high resistance to ionizing gamma-radiation even after a massive dose of 30 kGy, comparable to the maximum doses tolerated by Deinococcus radiodurans [Rainey et al., 2005].

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Eppard et al., 1996. Morphological, physiological, and molecular characterization of actinomycetes isolated from dry soil, rocks, and monument surfaces. Arch. Microbiol. 166:12-22.

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Gurtner et al., 2000. Comparative analyses of the bacterial diversity on two different biodeteriorated wall paintings by DGGE and 16S rDNA sequence analysis. Int. Biodeter. Biodegr. 46:229-239.

Hungate et al., 1987. Characterization of manganese-oxidizing (Mn(II)-Mn(IV)) bacteria from Negev Desert rock varnish-implications in desert varnish formation. Can. J. Microbiol. 33:939-943.

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Luedemann, 1968. Geodermatophilus, a new genus of the Dermatophilaceae (Actinomycetales). J. Bact. 96:1848-1858.

Mevs et al. 2000. Modestobacter multiseptatus gen. nov., sp. nov., a budding actinomycete from soils of the Asgard Range (Transantarctic Mountains). Int. J. Syst. Evol. Microbiol. 50:337-346.

Normand, 2006. Geodermatophilaceae fam. nov., a formal description. Int. J. Syst. Evol. Microbiol. 56:2277-2278.

Ortega-Morales et al., 2005. Characterization of epilithic microbial communities associated with Mayan stone monuments in Yucatan, Mexico. Geomicrobiol J 22:261-268.

Rainey et al., 2005. Extensive diversity of ionizing-radiation-resistant bacteria recovered from Sonoran Desert soil and description of nine new species of the genus Deinococcus obtained from a single soil sample. Appl. Environ. Microbiol. 71:5225–5235.

Reddy et al. 2007. Modestobacter versicolor sp. nov., an actinobacterium from biological soil crusts that produces melanins under oligotrophy, with emended descriptions of the genus Modestobacter and Modestobacter multiseptatus Mevs et al. 2000. Int. J. Syst. Evol. Microbiol. 57:2014-2020.

Rolleke et al., 1999. Analysis of bacterial communities on historical glass by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. J. Microbiol. Meth. 36:107-114.

Urzì et al., 2001. Biodiversity of Geodermatophilaceae isolated from altered stones and monuments in the Mediterranean basin. Env. Microbiol. 3:471-479.

Urzì & Realini, 1998. Colour changes of Noto’s calcareous sandstone as related with its colonization by microorganisms. Int. Biodeter. Biodegr. 42:45-54.