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Review
, 64 (3), 548-72

Resistance of Bacillus Endospores to Extreme Terrestrial and Extraterrestrial Environments

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Review

Resistance of Bacillus Endospores to Extreme Terrestrial and Extraterrestrial Environments

W L Nicholson et al. Microbiol Mol Biol Rev.

Abstract

Endospores of Bacillus spp., especially Bacillus subtilis, have served as experimental models for exploring the molecular mechanisms underlying the incredible longevity of spores and their resistance to environmental insults. In this review we summarize the molecular laboratory model of spore resistance mechanisms and attempt to use the model as a basis for exploration of the resistance of spores to environmental extremes both on Earth and during postulated interplanetary transfer through space as a result of natural impact processes.

Figures

FIG. 1
FIG. 1
Survival times (D values; decimal reduction time) for spores of B. subtilis strain 5230 exposed to wet and dry heat. (Data are modified from reference .)
FIG. 2
FIG. 2
Structures of a single pair of adjacent thymines on the same DNA strand (left), a cis-syn cyclobutyl thymine-thymine dimer (center), and SP (right). dRib, d-ribose.
FIG. 3
FIG. 3
UV resistance of spores and vegetative cells of B. subtilis DNA repair mutants. All strains were derivatives of the prototype laboratory strain 168. The average UV dose required to kill 90% of the population (LD90 value) is given for vegetative cells (open bars) and spores (solid bars). LD90 values are averages of values reported in the literature; the number of reports from which each value was derived is listed on the top of each bar. Data are from references , , , , , , , , , , , , and and from P. Fajardo-Cavazos (unpublished data).
FIG. 4
FIG. 4
Comparison of amino acid regions forming [4Fe-4S] clusters in the SplB amino acid sequences from Bacillus anthracis (B.an), B. amyloliquefaciens (B.am), B. stearothermophilus (B.st), B. subtilis (B.su), Clostridium acetobutylicum (C.ac), and C. difficile (C.di) with the [4Fe-4S] clusters of: the activating subunits of ribonucleotide reductase (NrdG) and pyruvate-formate lyase (Act) from Escherichia coli (E.co), phage T4 (T4), and Haemophilus influenzae (H.in) and the [4Fe-4S] clusters from lysine-2,3-aminomutase (KamA) from Clostridium subterminale (C.su), biotin synthase (BioB) from B. subtilis, and the probable lipoic acid synthase (YutB) from B. subtilis. Highly conserved residues are in bold, and invariant cysteines are marked with an asterisk.
FIG. 5
FIG. 5
Solar spectrum in space (thin line) and on Earth's surface (thick line). Below the spectrum is an expansion of the UV portion, showing the approximate boundaries between UV-C, UV-B, and UV-A. Also shown is the UV wavelength commonly used in the laboratory (254 nm) and the UV wavelengths incident on the Earth's surface (290 nm and longer). vis, visible; IR, infrared.
FIG. 6
FIG. 6
Cross-section of a spore of B. subtilis. The DNA is contained in the nucleoid (electron-light regions) within the spore core. The core is surrounded by the protective cortex and the lamellar inner spore coat and electron-dense outer spore coat. The long axis of the spore is 1.2 μm; the core area is 0.25 μm2. (The electron micrograph was kindly provided by S. Pankratz.)
FIG. 7
FIG. 7
Increase in biologically effective UV irradiance (biologically effective dose) with decreasing simulated ozone column thickness as measured by the spore biofilm technique in a space experiment. (A) Extraterrestrial solar spectral irradiances filtered through a quartz (7 mm) plate (H) or additionally through cutoff filters simulating different ozone column thicknesses with a progressive simulated ozone depletion from curves A to G. (B) Biofilm data of biologically effective solar irradiance for the different ozone column thicknesses, given in Dobson units (DU) (A to G), the extraterrestrial UV spectrum (H), and ground control (GC, Cologne). The dashed line shows the corresponding curve for DNA damage calculated by Madronich (95). (Data are modified from reference .)
FIG. 8
FIG. 8
Action spectrum of extraterrestrial solar UV inactivation of B. subtilis spores from three space experiments on board the missions Spacelab (SL) 1 (triangles), D2 (squares), and EURECA (circles). Using an optical filtering system, dry layers of spores were exposed to defined wavelengths and intensities of extraterrestrial solar UV radiation during periods when the samples were pointing towards the sun. The spores were either kept at atmospheric pressure in argon (solid symbols) or exposed to the vacuum of space during the whole mission (open symbols). (Data are modified from reference .)
FIG. 9
FIG. 9
Biostack experiment, a method to study the biological effects of single heavy ions of cosmic radiation. (A) The complete Biostack experiment package (about 10 × 10 × 10 cm in size) accommodated in a hermetically sealed aluminum container was stowed inside the spacecraft during several space missions (Apollo and Spacelab) and exposed to cosmic radiation. (B) The Biostack consists of a sandwich of monolayers of biological objects in a resting state (in this example, B. subtilis spores) mounted on a particle track detector. After irradiation and processing of the track detector, the biological effect on individual spores was investigated and correlated to impact parameter, i.e., the distance from the particle's trajectory (C) (17). CN, cellulose nitrate; PC, polycarbonate; PVA, polyvinyl alcohol.
FIG. 10
FIG. 10
Frequency of inactivated spores of B. subtilis as a function of the impact parameter. During several space missions, spores were exposed to the HZE particles of cosmic radiation in a Biostack experiment, and the viability of each spore in the vicinity of the trajectory of an HZE particle was analyzed separately under the microscope after micromanipulation and incubation in small incubation chambers. Data are based on the analysis of 121 HZE particle tracks, 919 spores from the target area, and 580 control spores. (Data modified from reference .)
FIG. 11
FIG. 11
Shielding of bacterial spores against galactic cosmic radiation by meteorite material. The dashed line gives the annual dose profile (in Grays per year), which increases for the outer 10 cm due to secondary radiation and then decreases. The solid line gives the exposure time for a survival rate of 10−6 (survival of 100 spores from an initial population of 108 spores). (Data from reference .)
FIG. 12
FIG. 12
Survival of B. subtilis spores on the LDEF experiment after nearly 6 years in space. The spores in multilayers were either exposed under a perforated dome to the full environment of space or shielded either by a quartz window 2 mm thick, which allowed access of solar UV radiation (λ > 170 nm), or an aluminum cover of 2 mm. (Graph drawn from data in reference .)

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