Biosignatures of diverse eukaryotic life from a Snowball Earth analogue environment in Antarctica

Abstract

The ephemeral, supraglacial meltwater ponds of the McMurdo Ice Shelf's undulating ice serve as analogues for refugia where eukaryotic organisms could have thrived during the Cryogenian period. The seafloor sediment and debris lined ponds support the growth of a diverse array of cyanobacterial mat communities and provide habitats for a variety of protists and meiofauna. Here, we show that these eukaryotic assemblages, assessed by steroid biomarker and 18S rRNA gene analyses, inform long-standing questions regarding the diversity of, and controls on, community composition in these environments. Sixteen photosynthetically active microbial mats from meltwater ponds, a 700-year-old relict microbial mat, and a microbial mat from the Bratina Lagoon were analysed for their sterol compositions. These sterols were subjected to simulated diagenesis via catalytic hydrogenation/hydrogenolysis affording their sterane hydrocarbon counterparts, facilitating comparisons with ancient settings. Pond salinity appeared to be a factor influencing the sterol distributions observed. Analyses of 18S rRNA gene sequences conducted on the modern mats independently confirm that the ponds host diverse eukaryotes, including many types of microalgae, protists, and an array of unclassifiable organisms. Our findings support the hypothesis that supraglacial meltwater ponds like those of the McMurdo ice are strong candidates for refugia that sheltered complex life during Snowball Earth episodes.

Fig. 1. Study area and sample location.

A The geographical location of the study vicinity and Bratina Island. B Detailed depiction of the meltwater ponds off the coast of Bratina Island based on satellite imagery. Sites included in this study are outlined in black and coloured in blue. Not shown: Bratina Lagoon, located approximately 1 km west of the area depicted.

Fig. 2. Life around the Bratina meltwater pond landscape.

A Pustular microbial mat section collected from New Pond. B A mound of relict microbial mats. C A fossil sponge on the landscape surface atop pinnacle ice. D A fossil bryozoan. All photos were captured by RES in January 2018.

Fig. 3. Partial gas chromatograms showing compounds identified in ponds Skua, Duet, and Brack.

Sterols identified are numbered; their corresponding peaks are described in Table 2. Peaks labelled A represent carboxylic acids, peaks labelled S represent siloxanes, and the peak labelled U represents an unidentified non-sterol, non-acid compound.

Fig. 4. Ternary diagram depicting C₂₇, C₂₈, and C₂₉ sterane distributions derived from the microbial mats.

Hydrogenated relict microbial mat steranes, noted by 1, are included as well as relict microbial mat steranes without hydrogenation, noted by F. Values were calculated using the relative intensities of ααα20R isomers. Ponds with conductivities >4000 µS/cm are noted with orange squares; ponds with conductivities <4000 µS/cm are noted with blue circles; ponds without conductivity information available are noted with white squares.

Fig. 5. Dynamic multiple reaction monitoring (dMRM) chromatograms showing steranes from Fresh Pond sterol hydrogenation.

Numerically labelled peaks are accompanied by peak identities.

Fig. 6. 18S rRNA gene communities of the undulating ice meltwater ponds and the Bratina Lagoon microbial mats.

Community assemblages are shown as relative abundances. Certain names are abbreviated: Fogg is short for Fogghorne, Cono is short for Conophyton, and Casten is short for Castenholz. Source data are provided as a Source Data file.

Fig. 7. Principal component analysis of meltwater pond microbial mat steranes and 18S rRNA gene communities.

Principal component scores for individual ponds are coloured according to conductivity, while loadings, representing the distributions of A steranes and B 18S rRNA genes, are coloured in dark purple. Certain 18S rRNA gene variables plotted very closely together near the origin and their names are abbreviated. Cr is short for Cryptophyceae, Ce is short for Centrohelida, and Ha is short for Haptophyta.