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ABSTRACT Microbes from terrestrial extreme environments enable testing of biosignature production in conditions relevant to astrobiological targets. Mars, which was likely more conducive to life during early warmer and wetter epochs, has inspired missions that search for signs of early life in the surficial rock record, including mineral or organic biosignatures. Microbial iron reduction is a common and ancient metabolism that may have also operated on other rocky celestial bodies. To investigate biosignature production during iron reduction, aShewanellasp. (strain BF02_Schw) isolated from a subglacial discharge known as Blood Falls, Antarctica, was incubated with the electron acceptor ferrihydrite (Fh). Biosignatures associated with Fh reduction were identified using a suite of techniques currently utilized or proposed for Mars missions, including X-ray diffraction and infrared, Mössbauer, and Raman spectroscopy. The biotic origin of features was validated by transcriptional changes observed between treatments with and without Fh and comparison to killed controls. In live treatments, Fh was reduced to magnetite and goethite, both detected in Martian lacustrine basins. Several soluble and volatile metabolites were also detected, including riboflavin and dimethyl sulfide (DMS), which could be astrobiological indicators of active microbial processes. While none of the identified biosignatures individually would serve as definitive proof of life (past or present), detecting concomitant features associated with known terrestrial biotic processes would provide compelling rationale for more targeted life detection missions. Terrestrial extremophiles can support the exploration of astrobiologically relevant microbial processes, validation of life detection instrumentation, and potentially the discovery of new biomarkers.IMPORTANCECulture-based experiments with terrestrial extremophiles can elucidate biosignatures that may be analogous to those produced under extraterrestrial conditions, and thus inform sampling and technology strategies for future missions. Here, we demonstrate the production of several biosignatures under iron-reducing conditions byShewanellasp. BF02_Schw, originally isolated from an Antarctic analog feature. These biosignatures could be detectable using flight-ready instrumentation. Growth experiments with terrestrial extremophiles can identify biosignatures measurable by current methodologies and inform the development and optimization of techniques for detecting extant or extinct life on other worlds. 

Aperiodic discharge of brine at Blood Falls forms a red-tinged fan at the terminus of Taylor Glacier, Antarctica. Samples from this discharge provide an opportunity for mineralogical study at a Martian analogue study site. Environmental samples were collected in the field and analyzed in the laboratory using Fourier transform infrared, Raman, visible to near-infrared, and Mössbauer spectroscopies. Samples were further characterized using microprobe and inductively coupled plasma optical emission spectroscopy for chemistry, and x-ray diffraction, scanning electron microscopy, and transmission electron microscopy for mineralogy, crystallography, and chemistry. The mineralogy of these samples is dominated by the carbonate minerals calcite and aragonite, accompanied by quartz, feldspar, halide, and clay minerals. There is no strong evidence for crystalline iron oxide/hydroxide phases, but compositionally and morphologically diverse iron- and chlorine-rich amorphous nanospheres are found in many of the samples. These results showcase the strengths and weaknesses of different analytical methods and underscore the need for multiple complementary techniques to inform the complicated mineralogy at this locale. These analyses suggest that the red color at Blood Falls arises from oxidation of dissolved Fe 2+ in the subglacial fluid that transforms upon exposure to air to form nanospheres of amorphous hydroxylated mixed-valent iron-containing material, with color also influenced by other ions in those structures. Finally, the results provide a comprehensive mineralogical analysis previously missing from the literature for an analogue site with a well-studied sub-ice microbial community. Thus, this mineral assemblage could indicate a habitable environment if found elsewhere in the Solar System. 

Emiliania huxleyi is a bloom-forming microalga that affects the global sulfur cycle by producing large amounts of dimethylsulfoniopropionate (DMSP) and its volatile metabolic product dimethyl sulfide. Top-down regulation of E. huxleyi blooms has been attributed to viruses and grazers; however, the possible involvement of algicidal bacteria in bloom demise has remained elusive. We demonstrate that a Roseobacter strain, Sulfitobacter D7, that we isolated from a North Atlantic E. huxleyi bloom, exhibited algicidal effects against E. huxleyi upon coculturing. Both the alga and the bacterium were found to co-occur during a natural E. huxleyi bloom, therefore establishing this host-pathogen system as an attractive, ecologically relevant model for studying algal-bacterial interactions in the oceans. During interaction, Sulfitobacter D7 consumed and metabolized algal DMSP to produce high amounts of methanethiol, an alternative product of DMSP catabolism. We revealed a unique strain-specific response, in which E. huxleyi strains that exuded higher amounts of DMSP were more susceptible to Sulfitobacter D7 infection. Intriguingly, exogenous application of DMSP enhanced bacterial virulence and induced susceptibility in an algal strain typically resistant to the bacterial pathogen. This enhanced virulence was highly specific to DMSP compared to addition of propionate and glycerol which had no effect on bacterial virulence. We propose a novel function for DMSP, in addition to its central role in mutualistic interactions among marine organisms, as a mediator of bacterial virulence that may regulate E. huxleyi blooms. 

Environmental contextCobalamin, or vitamin B12, is receiving increased attention as a critical trace nutrient in the growth and metabolic processes of oceanic phytoplankton and bacterial communities. We present evidence that indicates B12 has a more significant role in the biogeochemical cycling of the climatically important compounds dimethylsulfide and dimethylsulfoniopropionate than previously understood. Several possible mechanisms are examined that link cellular-level processes involving B12 to global-scale biogeochemical processes involving the oceanic cycling of dimethylsulfoniopropionate and dimethylsulfide.AbstractEvidence is presented showing that dissolved dimethylsulfoniopropionate (DMSPd) and dimethylsulfide (DMS) concentrations are influenced by the availability of vitamin B12 in two oceanographically distinct regions with different DMS production capacities, the central equatorial Pacific Ocean and the Ross Sea, Antarctica. In both locations, addition of B12 to incubation experiments resulted in decreases in DMS and, in some cases, DMSPd concentrations relative to unamended controls. In no case did increasing iron availability significantly (α=0.1) alter DMS concentrations relative to controls. The relative decreases in DMS between B12 addition and control experiments were significant (α=0.1) in five of seven experiments conducted at ambient iron levels. Overall, DMS concentrations were on average 33.4% (±15.1%; 1 standard deviation) lower, relative to unamended controls, by the end of incubation experiments when B12 was added. Declines in DMSPd were observed in three of five experiments. Similar trends were observed when B12 was added to iron-supplemented bottle incubation experiments (30.4±10.4% lower final DMS concentrations in +B12Fe treatments relative to +Fe treatments). Several possible molecular-level explanations exist for this link between B12 and DMS production, including potential B12 dependence of methyltransferase enzymes involved in both DMS and DMSP degradation. Although the enzymology of these reactions remains unclear, the relationships described here provide evidence for plausible mechanisms behind the microbial modulation of oceanic DMS. 

Environmental contextDimethylsulfoniopropionate (DMSP), a small sulfur compound biosynthesised by algae, plays an important role in global climate, particularly in polar regions. We investigated salinity effects on DMSP levels, and provide the first experimental measurements of DMSP and associated physiological changes in a polar diatom across to a range of gradual salinity shifts representative of sea-ice conditions. Quantitative estimates of DMSP in polar diatoms following salinity changes will facilitate new mathematical models to predict seasonal responses and reactions to climate change.AbstractAlthough extreme environmental gradients within sea-ice have been proposed to stimulate dimethylsulfoniopropionate (DMSP) accumulation in diatoms, a taxa whose temperate counterparts show relatively low concentrations, this has yet to be experimentally validated across a range of salinities representative of sea-ice conditions. The present study examined changes in DMSP concentrations in the widespread polar diatom Fragilariopsis cylindrus in response to gradual salinity shifts representative of those encountered during sea-ice formation and melt. DMSP concentrations were elevated up to 127% in 70-salinity cultures. Low-salinity shifts decreased intracellular DMSP concentrations in a gradient-dependent manner that suggests DMSP recycling rather than release under milder hyposalinity shifts. Permeable membranes were detected in ~45% of 10-salinity cells; therefore, loss of membrane integrity may only partially explain DMSP release in the lowest-salinity group. Growth rates, photosynthetic efficiency of photosystem II and reactive oxygen species detection indicated only partial impairment by salinity stress in this organism. Thus, experimental evidence supports the role of DMSP as a compatible solute in the acclimation of a sea-ice diatom across large salinity gradients and measurements of associated physiological changes will improve interpretation of environmental measurements. 

Abstract As the annual expanse of Arctic summer ice‐cover steadily decreases, concomitant biogeochemical and ecological changes in this region are likely to occur. Because the Central Arctic Ocean is often nutrient and light limited, it is essential to understand how environmental changes will affect productivity, phytoplankton species composition, and ensuing changes in biogeochemistry in the region. During the transition from late summer to early autumn, water column sampling of various biogeochemical parameters was conducted along an ice‐floe drift station near the North Pole. Our results show that as the upper water column stratification weakened during the late summer–early autumn transition, nutrient concentrations, particulate dimethylsulfoniopropionate (DMSP_p) levels, photosynthetic efficiency, and biological productivity, as estimated by ΔO₂/Ar ratios, all decreased. Chemotaxonomic (CHEMTAX) analysis of phytoplankton pigments revealed a taxonomically diverse picoautotrophic community, with chlorophyll (Chl)c₃‐containing flagellates and the prasinophyte,Pyramimonasspp., as the most abundant groups, comprising ~ 30% and 20% of the total Chla(TChla) biomass, respectively. In contrast to previous studies, the picoprasinophyte,Micromonasspp., represented only 5% to 10% of the TChlabiomass. Of the nine taxonomic groups identified, DMSP_pwas most closely associated withPyramimonasspp., a Chlb‐containing species not usually considered a high DMSP producer. As the extent and duration of open, ice‐free waters in the Central Arctic Ocean progressively increases, we suggest that enhanced light transmission could potentially expand the ecological niche ofPyramimonasspp. in the region.