Novel sulfur‐oxidizing streamers thriving in perennial cold saline springs of the Canadian high Arctic

Abstract

SummaryThe perennial springs at Gypsum Hill (GH) and Colour Peak (CP), situated at nearly 80°N on Axel Heiberg Island in the Canadian high Arctic, are one of the few known examples of cold springs in thick permafrost on Earth. The springs emanate from deep saline aquifers and discharge cold anoxic brines rich in both sulfide and sulfate. Grey-coloured microbial streamers form during the winter months in snow-covered regions of the GH spring run-off channels (-1.3°C to 6.9°C,~7.5% NaCl, 0-20 p.p.m. dissolved sulfide, 1 p.p.m. dissolved oxygen) but disappear during the Arctic summer. Culture-and molecular-based analyses of the 16S rRNA gene (FISH, DGGE and clone libraries) indicated that the streamers were uniquely dominated by chemolithoautotrophic sulfur-oxidizing Thiomicrospira species. The streamers oxidized both sulfide and thiosulfate and fixed CO 2 under in situ conditions and a Thiomicrospira strain isolated from the streamers also actively oxidized sulfide and thiosulfate and fixed CO2 under cold, saline conditions. Overall, the snow-covered spring channels appear to represent a unique polar saline microhabitat that protects and allows Thiomicrospira streamers to form and flourish via chemolithoautrophic, phototrophicindependent metabolism in a high Arctic winter environment characterized by air temperatures commonly below -40°C and with an annual average air temperature of -15°C. These results broaden our knowledge of the physical and chemical boundaries that define life on Earth and have astrobiological implications for the possibility of life existing under similar Martian conditions.

Microbial characterization of a subzero, hypersaline methane seep in the Canadian High Arctic

“…Further work identified culturable microbes from the spring sediments with autotrophic and sulfur-oxidation activities (Perreault et al, 2008), and the small amounts of hydrocarbons in gases exsolving from these springs were compositionally and isotopically consistent with microbial methanogenesis and possible methanotrophy (Perreault et al, 2007). Niederberger et al (2009) characterized gray-colored microbial streamers that form during the winter months in the snow-covered regions of the GH spring runoff channels. Culture, molecular and microscopicbased analysis of the 16S rRNA gene indicated that the streamers were dominated by chemolithoautotrophic sulfur-oxidizing Thiomicrospira species that oxidized both sulfide and thiosulfate and fixed CO 2 under in situ conditions (Niederberger et al, 2009).…”

“…These springs are among the only known cold springs in thick permafrost on Earth (Andersen et al, 2002) and the geomorphology, chemistry, thermal environment and microbiology of two sets of moderately cold, saline springs (Gypsum Hill (GH), Colour Peak (CP)) located at Expedition Fiord on AHI have been extensively studied (Pollard et al, 1999;Andersen et al, 2002;Perreault et al, 2007Perreault et al, , 2008Niederberger et al, 2009). These springs flow throughout the entire year with constant discharge temperatures ranging from À0.5 to 6.9 1C, and discharge waters that are moderately saline (7.5-15.8% salts), anoxic (mean oxido-reduction potential (ORP) of À325 mV), near-neutral (pH 6.9-7.5), rich in both sulfate (2300-3724 mg l À1 ) and sulfide (25-100 p.p.m.)…”

“…Niederberger et al (2009) characterized gray-colored microbial streamers that form during the winter months in the snow-covered regions of the GH spring runoff channels. Culture, molecular and microscopicbased analysis of the 16S rRNA gene indicated that the streamers were dominated by chemolithoautotrophic sulfur-oxidizing Thiomicrospira species that oxidized both sulfide and thiosulfate and fixed CO 2 under in situ conditions (Niederberger et al, 2009). These collective studies indicate that the utilization and cycling of sulfur compounds may have a major role in the energy production and maintenance of microbial communities in the GH and CP spring environments (Perreault et al, 2007;Niederberger et al, 2009).…”

“…Culture, molecular and microscopicbased analysis of the 16S rRNA gene indicated that the streamers were dominated by chemolithoautotrophic sulfur-oxidizing Thiomicrospira species that oxidized both sulfide and thiosulfate and fixed CO 2 under in situ conditions (Niederberger et al, 2009). These collective studies indicate that the utilization and cycling of sulfur compounds may have a major role in the energy production and maintenance of microbial communities in the GH and CP spring environments (Perreault et al, 2007;Niederberger et al, 2009). These cold saline springs are regarded as analogues to possible Martian liquid water habitats (Andersen et al, 2002).…”

Mineralogy of saline perennial cold springs on Axel Heiberg Island, Nunavut, Canada and implications for spring deposits on Mars

“…Lay et al (2012) also reported phylotypes related to methanogenesis, methanotrophy, sulfur reduction and oxidation Average perennial water temperature at outlets À5.9 to À4.7°C (Lay et al, 2012) 3.6°C (Pollard et al, 1999) 3.9°C (Pollard et al, 1999) Salinity 22-26% (Lay et al, 2012), 22.4% (this study) 16-17% (Pollard et al, 1999), 16.6% (this study) 8-9% (Pollard et al, 1999) (Perreault et al, 2007;Omelon et al, 2006) 27.92 g/L Na, 2.11 g/L Ca, 44.21 g/L Cl (Perreault et al, 2007;Omelon et al, 2006) Discharging gases (bubbles) 50% thermogenic CH 4 , 35% N 2 , 10% CO 2 , <5% He, H 2 , other hydrocarbons (Niederberger et al, 2010) >98% N 2 , <1% CH 4 , <1% CO 2 , minor O 2 (Pollard et al, 1999) >98% N 2 , <1% CH 4 , <1% CO 2 , minor O 2 (Pollard et al, 1999) Microbiology Low microbial diversity compared to similar cryo-environments Psychrophilic obligately chemolithoautotrophic S oxidizing bacteria; anaerobic S and SO 4 reducing bacteria (Perreault et al, 2007) Anaerobic heterotrophic, and aerobic autotrophic S oxidizing bacteria; anaerobic S and SO 4 reducing bacteria; methanogens; possible methanotrophs. Streamers: S-oxidizing bacteria (Perreault et al, 2007(Perreault et al, , 2008Niederberger et al, 2009) Anaerobic methanotrophs; methanogens; S oxidizing bacteria; ammonia-oxidizers; possible SO 4 reducing archaea (Niederberger et al, 2010;Lay et al, 2012) and an archaeal community dominated by phylotypes most closely related to ammonia-oxidation. Although some authors have referred to this site as the ''Lost Hammer spring'', it was mapped by Harrison and Jackson (2008) as ''Wolf spring''.…”