Contrasted resistance of stone-dwelling Geodermatophilaceae species to stresses known to give rise to reactive oxygen species

Abstract

Stones in arid environments are inhabited by actinobacteria of the family Geodermatophilaceae like the genera Blastococcus and Modestobacter frequently isolated from altered calcarenites. Their habitat requires adaptation to light-induced and other stresses that generate reactive oxygen species. Here, we show that representative members of the species Blastococcus saxobsidens, Geodermatophilus obscurus, and Modestobacter multiseptatus are differentially adapted to stresses associated with arid environments. Whereas B. saxobsidens was found to be sensitive to gamma radiation (D(10) = 900 Gy; 10% survival at 900 Gy), M. multiseptatus was moderately (D(10) = 6000 Gy) and G. obscurus was highly tolerant (D(10) = 9000 Gy). A difference in resistance to high-frequency (λ value = 254 nm) UV was shown by B. saxobsidens, M. multiseptatus, and G. obscurus, being sensitive, tolerant, and highly tolerant (D(10) of 6, 900, and > 3500 kJ m(-2) , respectively). Tolerance to desiccation, mitomycin C and hydrogen peroxide correlated with the ionizing radiation and UV resistance profiles of the three species and were correlated with the pigments synthesized. Resistance to heavy metals/metalloids did not follow the same pattern, with resistance to Ag(2+) and Pb(2+) being similar for B. saxobsidens, M. multiseptatus, and G. obscurus, whereas resistance to AsO4 3-, Cr(2+) , or Cu(2+) was greater for B. saxobsidens than for the other two species. The stress resistance profiles of M. multiseptatus and B. saxobsidens were reflected in different calcarenite colonization patterns. While M. multiseptatus was predominantly isolated from the first two millimeters of stone surface, B. saxobsidens was predominantly isolated from the deeper part of the stone where it is better protected from sun irradiation, suggesting that the response to light- and desiccation-induced oxidative stress is an important driver for niche colonization in the stone biotope.

Stone-dwelling actinobacteria Blastococcus saxobsidens, Modestobacter marinus and Geodermatophilus obscurus proteogenomes

“…These three genera have a complex life cycle and produce remarkably resistant enzymes such as esterases (Essoussi et al, 2010;Jaouani et al, 2012;Normand et al, 2014). They also have the ability to resist adverse environmental conditions such as ultraviolet light, ionizing radiation, desiccation and heavy metals (Rainey et al, 2005;Gtari et al, 2012;Montero-Calasanz et al, 2014, 2015. This resistance to environmental hazards represents a trait of Terrabacteria, a well-supported phylogenetic group composed of Actinobacteria and four other major lineages of eubacteria (Firmicutes, Cyanobacteria, Chloroflexi and Deinococcus-Thermus) that colonized land 3.05-2.78 Ga (Tunnacliffe and Lapinski, 2003;Battistuzzi et al, 2004;Battistuzzi and Hedges, 2009).…”

Microbial Community Structure of Subalpine Snow in the Sierra Nevada, California

“…For instance, the elevated relative abundance of phylotypes 1110021 and 453616 within the deeper layer of snow may reflect the ability of Geodermaphilaceae to tolerate stressful conditions (Ivanova et al, 2010). Indeed, phylotype 1110021 shared 99.3% similarity with Modestobacter marinus, an isolate that has often been recovered from harsh environments such as deserts and is able to withstand high gamma radiation, UV levels, and desiccation typical of snowpack conditions (Gtari et al, 2012). Similar tolerance for extended periods of extreme desiccation may explain the higher abundance of Actinobacteria and Firmicutes in the deeper snow layer (Connon et al, 2007), and may also account for the commonness of these phyla in other snow-dominated environments (Liu et al, 2007).…”

Community succession of bacteria and eukaryotes in dune ecosystems of Gurbantünggüt Desert, Northwest China

“…Actinobacteria are known to dominate alkaline soils, particularly arid soils, and have been found in abundance in previous surveys of neutral-alkaline soils (Lauber et al 2009), similar to the environment in this study. The most abundant actinobacterial genus was Blastococcus, which is known for its resistance to environmental hazards and has morphological features that facilitate adaptation to dry biotopes, including the formation of spores (Gtari et al 2012). Other actinobacterial genera, such as Cryptosporangium and Friedmanniella, have been derived from arid soil crusts in the Turpan Basin and the Colorado Plateau (Gundlapally and Garcia-Pichel 2006).…”