Seeding Biochemistry on Other Worlds: Enceladus as a Case Study

Abstract

The Solar System is becoming increasingly accessible to exploration by robotic missions to search for life. However, astrobiologists currently lack well-defined frameworks to quantitatively assess the chemical space accessible to life in these alien environments. Such frameworks will be critical for developing concrete predictions needed for future mission planning, both to determine the potential viability of life on other worlds and to anticipate the molecular biosignatures that life could produce. Here, we describe how uniting existing methods provides a framework to study the accessibility of biochemical space across diverse planetary environments. Our approach combines observational data from planetary missions with genomic data catalogued from across Earth and analyzed using computational methods from network theory. To demonstrate this, we use 307 biochemical networks generated from genomic data collected across Earth and "seed" these networks with molecules confirmed to be present on Saturn's moon Enceladus. By expanding through known biochemical reaction space starting from these seed compounds, we are able to determine which products of Earth's biochemistry are, in principle, reachable from compounds available in the environment on Enceladus, and how this varies across different examples of life from Earth (organisms, ecosystems, planetary-scale biochemistry). While we find that none of the 307 prokaryotes analyzed meet the threshold for viability, the reaction space covered by this process can provide a map of possible targets for detection of Earth-like life on Enceladus, as well as targets for synthetic biology approaches to seed life on Enceladus. In cases where biochemistry is not viable because key compounds are missing, we identify the environmental precursors required to make it viable, thus providing a set of compounds to prioritize for detection in future planetary exploration missions aimed at assessing the ability of Enceladus to sustain Earth-like life or directed panspermia.

Keywords: Biochemical networks; Enceladus; Habitability; Life as a planetary process; Metabolic networks; Panspermia; Planetary protection.

FIG. 1.

Compounds in the Enceladus seed set and biological targets for the viability of life on Enceladus. (A) A subset of the compounds reported to be present in the ocean of Enceladus, which are also catalogued in KEGG, a database of biochemically utilized compounds. These compounds, along with 20 others not shown, are included in our “seed set” for network expansion. We add phosphate to this seed set to test whether its presence makes a difference for the viability of diverse biochemical systems. A full list of the 38 compounds in our Enceladus seed set can be found in Supplementary Table S2 (Postberg et al., ; Waite Jr et al., ; Magee and Waite, ; Waite et al., ; Postberg et al., 2018). (B) An overview of the types of compounds that the target set is composed of. A listing of the specific 65 possible target compounds can be found in Supplementary Table S3 (based on the target set from Freilich et al., 2009). KEGG, Kyoto Encyclopedia of Genes and Genomes. Color images are available online.

FIG. 3.

Properties of KEGG networks expanded using subsets of the Enceladus seed set. (A) Distribution of sizes of network scopes, expanded from size 10 seed sets, drawn from the 38 Enceladus seed compounds. Expansions were calculated when keeping the top five most abundant compounds fixed (according to Magee and Waite, 2017), and when varying all 10 seeds, drawn from a flat distribution. The y axis shows the number of occurrences of expanded networks within a given bin-size (bins are 100 compounds large). (B) Number of target compounds produced by randomized seed sets. No randomized sets produced between 1 and 14 target compounds, and none produced the number of compounds, which are produced with the full set of 38 Enceladus seed compounds (18 target compounds). (C) Of the networks that expanded to include at least 500 compounds, the percentage of expanded networks containing compounds is listed. Even though sulfur compounds cannot be produced without the hydrogen sulfide seed, hydrogen sulfide is not overly represented among the most largely expanded networks (those more than 500 compounds). Color images are available online.

FIG. 2.

The fraction of possible scope compounds reached by the analyzed prokaryotes using the Enceladus seed set. Each bar represents an organism (orange for archaea, blue for bacteria). Bar height indicates the fraction of the maximum theoretical size of networks (if scopes were able to take advantage of full organismal reaction networks) reached using only the Enceladus seed set (A subset of which are shown in Fig. 1A). The gray addition shows how the scope size changes for all organisms when adding phosphate to the seed set. In neither case do any target compounds get produced for any organisms. The inset shows histograms for the maximum theoretical sizes of archaeal and bacterial networks, if scopes were able to take advantage of full organismal reaction networks. Color images are available online.

FIG. 4.

Characteristics of irreducible seed sets that produce target metabolites. Blue boxes show results of bacteria expansions, and orange boxes show properties of archaea expansions. The left column shows the molecular weights of all seeds in all irreducible seed sets, by the size of the seed sets they are a part of (i.e., the number of compounds in the seed set). The right column also shows the molecular weights of all seeds in all irreducible seed sets, but by the number of seed compounds required to be added to the Enceladus seed compounds. The top row (A, B) shows distributions of molecular weights from all expansions. The middle row (C, D) shows the distributions of molecular weights only from seed sets with the fewest number of compounds from each organism. The bottom row (E, F) shows the distributions of molecular weights only from seed sets with the lowest mean molecular weight from each organism. The black dashed lines show the size and average molecular weight values for the 38 Enceladus seed set compounds. The box plot whiskers extend 1.5 times the IQR above and below the IQR. IQR, interquartile range. Color images are available online.

FIG. 5.

The rank ordered mean Jaccard index is shown for all 100 irreducible seed sets we calculated for each organism. Bacteria are shown in blue, and archaea are shown in orange. (A) Similarity is calculated using all seed compounds in all seed sets within each organism. (B) Similarity is calculated using only the seed compounds required to be added to the Enceladus seed compounds in all seed sets within each organism. The box plot whiskers extend 1.5 times the IQR above and below the IQR. Species names shown below each box may be difficult to read, so they are additionally provided in Supplementary Table S4. Color images are available online.

FIG. 6.

The similarity of seed sets between organisms. The clusters of two methods of organism comparisons are shown. (A) We take the union of all 100 seed sets within each organism and compare them with one another using the Jaccard index. (B) We take the irreducible seed set of the smallest mean molecular weight of all 100 seed sets within each organism and compare them with one another using the Jaccard index. In both cases, the clustering separates out the domains fairly well but is more effective when using the union of all organismal seed sets. The domain of each organism is shown as blue squares for bacteria and orange squares for archaea above and to the left of the clustermap. The scale for the heat map can be found between (A) and (B). Color images are available online.

FIG. 7.

The top 100 most common seed compounds. (A) Rank ordered and showing the proportion of archaea (orange) and bacteria (blue) seed sets that the compounds are found in. (B) The molecular weights of each of the top 100 most common seed compounds. Compound names are shown in (A) (truncated if prohibitively long), whereas KEGG compound IDs are shown in (B), in the same order. Tick labels are bold if they are part of the 38 Enceladus seed compounds and are colored raspberry if they are part of the target compound set. Color images are available online.