Extra-terrestrial fullerenes as a food source for microorganisms on the early Earth

Abstract

The search for extra-terrestrial life is an ever-evolving field of research that seeks to identify and understand life elsewhere in the universe. In order to narrow down this expansive search it is necessary to establish a set of parameters pertaining to habitability. It is therefore of significant interest for astrobiologists to study the conditions extra-terrestrial life may need to arise. Earth is the only planet currently known to host life and therefore provides an excellent model system as a case study for astrobiologists seeking to search for and understand life on distant planets. Very little is currently known about primitive terrestrial microorganisms, particularly with regard to their energetic processes and metabolism. It is well established that the origin of terrestrial life occurred simultaneously with the Late Heavy Bombardment, during which time a massive amount of organic-rich meteoritic material was accreted. This likely resulted in the accumulation of a large reservoir of extra-terrestrial carbon on the early Earth around the time primitive microorganisms were evolving more advanced metabolic processes. While it was previously assumed early life must have been purely autotrophic, the presence of potentially biologically accessible organics in the early Earth environment introduces the possibility that primitive microbes may have evolved to exploit these resources and develop early heterotrophic mechanisms much earlier than is currently postulated.

Fullerenes are found in abundance in carbonaceous chondrites and were therefore almost certainly present in relatively high amounts on the early Earth. Very little is known about the effect of fullerenes and their naturally occurring water-soluble derivatives, fullerols, on microorganisms, particularly in anoxic environments, and therefore very limited conclusions can be drawn for their potential effects on primitive microbes. Furthermore, the effects of the extreme early Earth environmental conditions, such as short-wave UV exposure, on the chemical properties of fullerenes and their derivatives are yet to be characterised; yet investigating this is critical in understanding how fullerenes may have fulfilled an important ecological niche.

In this thesis, I will explore the effect of fullerenes C60 and C70 and their fullerol derivatives on microorganisms and their potential as carbon sources for heterotrophic metabolism. An anaerobic community was studied as an analogue of a primitive microbial system, with an isolate derived from this community used for further, more comprehensive analyses of biological fullerene interactions. Furthermore, the effect of fullerenes and fullerols on select aerobic environmental isolates and model species E. coli was examined. With these microbiology studies, I show that fullerene response is highly species-specific and closely linked to the growth environment. It is demonstrated that fullerene C60, while inaccessible in its native form, can be converted to a highly accessible carbon source for anaerobic microorganisms when exposed to the high UV and anoxic conditions found on early Earth. To further understand the biodegradation pathways involved in C60 utilisation and the mechanism of toxicity to aerobic species, a comprehensive metabolomics study was carried out in which I present a novel set of results describing the innate biological effect of fullerenes on both an aerobic and anaerobic microorganism. The results presented in this thesis in their entirety give a clearer picture of how fullerenes on the early Earth and other habitable planets could provide primitive microbes with a previously undescribed source of carbon and energy.