Bacterial Utilisation of Aliphatic Organics: Is the Dwarf Planet Ceres Habitable?

Abstract

The regolith environment and associated organic material on Ceres is analogous to environments that existed on Earth 3-4 billion years ago. This has implications not only for abiogenesis and the theory of transpermia, but it provides context for developing a framework to contrast the limits of Earth's biosphere with extraterrestrial environments of interest. In this study, substrate utilisation by the ice-associated bacterium Colwellia hornerae was examined with respect to three aliphatic organic hydrocarbons that may be present on Ceres: dodecane, isobutyronitrile, and dioctyl-sulphide. Following inoculation into a phyllosilicate regolith spiked with a hydrocarbon (1% or 20% organic concentration wt%), cell density, electron transport activity, oxygen consumption, and the production of ATP, NADPH, and protein in C. hornerae was monitored for a period of 32 days. Microbial growth kinetics were correlated with changes in bioavailable carbon, nitrogen, and sulphur. We provide compelling evidence that C. hornerae can survive and grow by utilising isobutyronitrile and, in particular, dodecane. Cellular growth, electron transport activity, and oxygen consumption increased significantly in dodecane at 20 wt% compared to only minor growth at 1 wt%. Importantly, the reduction in total carbon, nitrogen, and sulphur observed at 20 wt% is attributed to biotic, rather than abiotic, processes. This study illustrates that short-term bacterial incubation studies using exotic substrates provide a useful indicator of habitability. We suggest that replicating the regolith environment of Ceres warrants further study and that this dwarf planet could be a valid target for future exploratory missions.

Keywords: Ceres; Colwellia hornerae; aliphatic hydrocarbons; astrobiology.

Figure 1

Growth curves of Colwellia hornerae grown under Ceres regolith conditions with three organic aliphatic substrates: (a) dodecane, (b) isobutyronitrile, and (c) dioctyl−sulphide; and (d) MMB (positive control) and no organic substrate (negative control). Modified Gompertz growth models (dotted lines) have been fitted to growth curves. Error bars represent the standard error of the mean.

Figure 2

Physiological response of Colwellia hornerae under Ceres regolith conditions when supplied with organic substrates: dodecane (a,e,i,m), isobutyronitrile (b,f,j,n), dioctyl-sulphide (c,g,k,o), and controls (d,h,l,p). (a–d) Proportion of CTC-positive (i.e., metabolically active) cells over time: (e–h) ATP production (mM cell⁻¹), (i–l) NADPH/NADP⁺ ratio, and (m–p) total protein concentration (pg cell⁻¹). Blue lines represent 1 wt% treatment (in aliphatic substrates) and no growth substrate (negative control). Red lines represent 20 wt% treatment (in aliphatic substrates) and MMB (positive control). Error bars represent standard error of the mean.

Figure 3

Relative amount of total oxygen consumed by Colwellia hornerae over the 32-day experimental period when grown under Ceres regolith conditions in different organic aliphatic substrates (dodecane, isobutyronitrile, and dioctyl-sulphide) at two concentrations (1 wt% and 20 wt%), and MMB (positive control) and no organic substrates (negative control). Values are averages of n = 15; errors are standard errors of the mean. Values marked with the same letters are not significantly different from the corresponding factor (Games–Howell multi-comparison test; p > 0.05).

Figure 4

Spearman correlations of total carbon, nitrogen, and sulphur concentrations in Colwellia hornerae under Ceres regolith conditions. Total carbon concentrations (pg cell⁻¹) in (a) dodecane, (b) isobutyronitrile, (c) dioctyl-sulphide, and (d) control substrates. Total nitrogen concentrations (pg cell⁻¹) in (e) isobutyronitrile and (g) control substrates. Total sulphur concentrations (pg cell⁻¹) in (f) dioctyl-sulphide.