In this experiment, we studied the effects of prolonged days conditions in low Earth orbit on a natural community of rock-dwelling phototrophs augmented with A. By using cut-off filters at defined wavelengths, the extraterrestrial UV radiation flux can be used to simulate past UV environments. The early Earth, during the time when life first arose, is thought to have been anoxic. When this flux was reduced to 0.
The sample sizes we studied were small because of logistical constraints in launching organisms into Earth orbit, so caution must be exercised in interpreting the results. For example, we do not know precisely the abundance of cells of each isolate of the natural community on each sample. However, these data show that in a worst-case scenario, early Earth UV fluxes would have been extremely detrimental to surface-dwelling epilithic organisms, particularly those in an inactive state.
The detrimental effects of these UV fluxes are confirmed by the analysis of the surface layer, which showed that the unattenuated UV flux not only killed organisms, but also bleached the chlorophyll and accessory pigments and destroyed carotenoids, as observed by bright-field microscopy and Raman spectroscopy.
The observations are consistent with previous data. For example, a fluence of 5. Although organisms beneath the altered surface layer did not exhibit obvious alteration by bright-field microscopy, the data suggest that the detrimental effects of UV radiation can penetrate to the natural community covered by the augmented cyanobacteria.
UV radiation damage could have been caused either directly to cell components such as DNA, which did not manifest itself as destruction of accessory pigments or carotenoids, or indirectly by the production of damaging radicals in the surface layer that subsequently destroyed the subsurface layers Hansen et al.
The greater survival of organisms in dark controls compared with UV exposure, both in ground-simulation and space exposure experiments, is consistent with data obtained with other organisms such as Bacillus subtilis , which were rapidly killed by extraterrestrial UV radiation, but not when shielded Horneck, ; Rettberg et al. We also observed generally greater survival of organisms in ground-based experiments than in space-exposed samples.
This observation might be explained by the different radiation environments. The quality of the UV fluxes is different in space than the ground-based UV lamp. Extraterrestrial UV fluxes have higher fluxes of short-wavelength UV radiation, which are likely to have been more detrimental to the UV-exposed samples.
However, this does not explain the difference between the dark control samples. One explanation is that the space-exposed samples were affected by ionizing radiation. The lower tolerance of the other components may have contributed to their loss of viability even at the doses received in this experiment, depending upon their dose-response functions.
Despite these results, cells of Chroococcidiopsis did survive under all UV-exposed conditions in ground and space-based experiments. The results are unlikely to be explained by UV radiation resistance alone. In the Atacama study, a small subpopulation of cells survived, which was attributed to self-shielding by clumps of cells in areas of an imperfect monolayer. Self-shielding might have contributed to cell survival in the work reported in this study, suggested by the presence of unbleached cells under the brown altered surface layer.
Other factors may have contributed to survival. Chroococcidiopsis is a polyextremophile, tolerant of multiple combined stressors including desiccation, ionizing radiation and temperature excursions Grilli Caiola et al. Finally, the high cell numbers of Chroococccidiopsis might have contributed. The organism had approximately 25 times greater number of cells than A. Applied to the worst-case UV radiation scenario on the early Earth or similar anoxic planets, the result shows that although UV fluxes would have been detrimental and a strong selection pressure on epilithic communities, some factors would have allowed organisms to survive.
Either individually or in combination, these factors would have allowed the surfaces of rocks to be colonized, despite the destruction of biomolecules in the surface layers. The work reported in this study also revealed new microorganisms of potential use in space exploration. Phototrophs have a number of uses, for example, in oxygen production in life support systems, the amelioration of planetary regolith surface material and the extraction of useful elements from rocks Cockell, The data show that some phototrophs can survive under space conditions, but that high UV fluxes or the combined stressors of space conditions even under dark conditions including temperature fluctuations kill most organisms.
Our experiments also resulted in the identification of two novel algal species, neither of which was isolated in the previous 10 day experiment. One explanation may be heterogeneities in the abundance or presence of the organisms on the rock surface, so that in the 10 day experiment they were either not present on the samples, or their population was not sufficiently abundant for a sub-population of cells to survive.
Nevertheless, our results show that space exposure experiments can result in the identification of novel, potentially useful, eukaryotic fast-growing phototrophs. The two algal species closely affiliate to genera Chlorella and Rosenvingiella , known to have representatives that can tolerate environmental extremes Belcher, ; Broady, ; Rindi et al.
The two novel non-cyanobacterial prokaryotic isolates belong to genera not previously characterized for tolerance to extreme environmental conditions. In conclusion, we have shown that prokaryotic and eukaryotic phototrophs can survive conditions in low Earth orbit for a year and a half and that these conditions act as a selective pressure on communities. However, some organisms could have survived the unattenuated flux in an inactive state for considerable lengths of time.
Future work must investigate the physiological capabilities of the novel extremophiles isolated from the rocks and their potential practical uses. Heterocyst differentiation and cell division in the cyanobacterium Anabaena cylindrica : effect of high light intensity.
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