The identification of sulfide oxidation as potential metabolism driving primary production on late Noachian Mars

Macey, Michael C; Fox-Powell, Mark; Ramkissoon, Nisha K; Baharier, Bea; Oliver, James A W; Stephens, Ben; Schwenzer, Susanne P; Pearson, Victoria K; Cousins, Claire R and Olsson-Francis, Karen (2020). The identification of sulfide oxidation as potential metabolism driving primary production on late Noachian Mars. In: 52nd Lunar and Planetary Science Conference, 15-19 Mar 2020 (Virtual), Houston, USA.



The surface of Mars cannot sus-tain liquid water today, but there is evidence for the extended presence of liquid water during the Noa-chian era [1-2]. The transition of the martian cli-mate from the wet Noachian to the dry, late Hespe-rian would have resulted in saline and sulfur-rich surface waters [1-4]. Terrestrial analogue environ-ments that possess a similar chemistry to these pro-posed waters can be used to develop an understand-ing of the diversity of organisms that could have persisted under such conditions. Combining this with laboratory simulation experiments, which ena-ble a greater level of accuracy regarding the chemi-cal environment, allows for concepts regarding di-versity and function to be developed. Here we present the chemistry and microbial community of the highly reducing sediment of the springs of Colour Peak, a sulfidic and saline spring system located within the Canadian High Arctic [2]. We also present details of the viability of this mi-crobial community when grown in defined, simulat-ed martian fluid chemistries based on the chemistry of Rocknest at Gale crater in combination with ba-saltic and iron enriched martian simulants.

In this study, the elemental com-position of the fluids and sediment porewater of Colour Peak was determined by ICP-OES. This data was compared with a range of fluid chemistries, including those from other analogue environments and martian brines, the composition of which were determined based on the chemistry of the “Rock-nest” sand sample at Yellowknife Bay, Gale crater (Mars) by thermochemical modelling [5]. The fluid chemistry derived from the thermochemical model-ling was used to calculate Gibbs energy values to identify metabolic pathways that could be energeti-cally feasible. Molecular techniques were also used to investigate the microbial community of the sedi-ment of the Colour Peak Springs. Both DNA and RNA were extracted from the microbes in the sedi-ment using a novel extraction technique that was developed to overcome issues associated with low biomass and the high concentrations of inhibitory substances (e.g. salt and sulfide). The microbial community was characterised by the amplification and sequencing of 16S rRNA gene amplicons pro-duced from the extracted nucleic acids. The ability of the microbial community to grow under defined martian chemical conditions was tested using the modelled fluid chemistry in combination with sim-ulants representative of either a general martian chemistry (OUCM-1, also based on the chemistry of Rocknest) or an iron enriched chemistry (OUHR-1, based on the chemistry of Haematite Slope) [6]. Enrichments were incubated at 10 °C for 28 days with a headspace of H2/CO2 (80:20) at one bar pres-sure. Growth was monitored using microscopy with Live/Dead staining and the enriched communities were characterised by sequencing of 16S rRNA gene amplicons produced from the extracted DNA.

Results and Discussion:
Analysis of the chemis-tries of the Colour Peak fluids confirmed a chemical composition that was similar to the thermochemi-cally modelled fluid derived from in-situ measure-ments of the chemistry of Gale crater sediments (Figure 1). This similarity in elemental composition confirms the classification of Colour Peak as an appropriate analogue environment to investigate the habitability of former martian aqueous environ-ments.
16S rRNA gene profiling of the Colour Peak mi-crobial community (Figure 2) revealed it was domi-nated by bacteria associated with the oxidation of reduced sulfur species and the fixation of carbon dioxide (autotrophy). Gibbs energy values demon-strated that the oxidation of reduced sulfur species was a viable metabolism in this chemical environ-ment under both oxic (using modern day concentra-tions of oxygen in the martian atmosphere [7]) and anoxic (denitrification-enabled [8]) conditions. The enrichments performed under simulated martian chemical conditions confirmed that the Colour Peak Spring sediment contained microbes that were via-ble under reconstructed martian chemical condi-tions. However, whilst sulfide oxidising bacteria were viable in the enrichments, sulfate reducing bacteria dominated the enriched communities.
In the unenriched community, non-autotrophic, fermentative bacteria were also detected as being active. Given the low concentration of carbon in the sediment and the persistence of bacteria that are dependent on an exogenous supply of organic car-bon, the community profile suggests that the sulfur oxidising bacteria may be driving primary produc-tion in this environment. The simulation experi-ments support the possible role of primary produc-ers supporting the persistence of additional diversi-ty, with the enrichments comprising clades of bacte-ria associated with autotrophy and additional het-erotrophic bacteria. The potential for the auto-trophic sulfur-cycling bacteria to enable the surviv-al of heterotrophic bacteria within the sediment has implications for the viability of metabolisms on Mars, since syntrophy may facilitate a greater di-versity of metabolisms.

This study highlights the potential role of oxidation of reduced sulfur species as a me-tabolism on Mars using either oxygen or nitrate as an electron acceptor. This needs further characteri-sation with regards to its viability in a martian con-text. It also shows the importance of community dynamics and the role of syntrophy when consider-ing the viability of metabolisms under terrestrial and martian chemical conditions.

Acknowledgments: We would like to acknowledge Hugo Moors from the Belgian Nuclear Research Center for his advice on handling nucleic acids extracted from saline environments. We would like to thank Gordon Osinski from Western University, Ontario for leading the sampling trip to Axel Heiberg island in 2017. We would like to acknowledge funding from the Science and Technology Facilities Council, Leverhulme Trust for funding and the Polar Continental Shelf Program (Natural Resources Cana-da) for logistical field support in Nunavut.

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