Geomicrobiology and occluded O2–CO2–Ar gas analyses provide evidence of microbial respiration in ancient terrestrial ground ice

Lacelle, Denis; Radtke, K.; Clark, Ian D.; Fisher, David; Lauriol, Bernard; Utting, Nicholas; Whyte, Lyle G.

doi:10.1016/j.epsl.2011.03.023

Cited by 26 publications

(28 citation statements)

References 46 publications

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“…Our study suggests a variable water-snow mix as a source of the ice with higher water contribution during the Holocene period. Concurrent with data from Lacelle et al (2011) and St-Jean et al (2011), however, our δ(N 2 /Ar) and δ(O 2 /Ar) results (Fig. 8) indicate an increasing influence of biological processes with the increasing amount of water in the water-snow mix.…”

Section: Iw-28mentioning

confidence: 76%

Stable isotope and gas properties of two climatically contrasting (Pleistocene and Holocene) ice wedges from Cape Mamontov Klyk, Laptev Sea, northern Siberia

et al. 2013

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Abstract. This paper presents and discusses the texture, fabric, water stable isotopes (δ 18 O, δD) and gas properties (total gas content, O 2 , N 2 , Ar, CO 2 , and CH 4 mixing ratios) of two climatically contrasted (Holocene vs. Pleistocene) ice wedges (IW-26 and IW-28) from Cape Mamontov Klyk, Laptev Sea, in northern Siberia. The two ice wedges display contrasting structures: one being of relatively "clean" ice and the other showing clean ice at its centre as well as debris-rich ice on both sides (referred to as "ice-sand wedge"). Our multiparametric approach allows discrimination between three different ice facies with specific signatures, suggesting different climatic and environmental conditions of formation and various intensities and nature of biological activity. More specifically, crystallography, total gas content and gas composition reveal variable levels of meltwater infiltration and contrasting contributions from anaerobic and aerobic conditions to the biological signatures. Stable isotope data are drawn on to discuss changes in paleoenvironmental conditions and in the temporal variation of the different moisture sources for the snow feeding into the ice wedges infillings. Our data set also supports the previous assumption that the ice wedge IW-28 was formed in Pleistocene and the ice wedge IW-26 in Holocene times. This study sheds more light on the conditions of ice wedge growth under changing environmental conditions.

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Section: Iw-28mentioning

confidence: 76%

Stable isotope and gas properties of two climatically contrasting (Pleistocene and Holocene) ice wedges from Cape Mamontov Klyk, Laptev Sea, northern Siberia

et al. 2013

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“…However, our SIP data does not demonstrate a significant reduction in active OTUs at colder temperatures (Supplementary Figure S6). Collectively, this implies that DNA synthesis could occur at temperatures much lower than À 20 1C, where evidence of respiration or metabolic activity has also been observed (Junge et al, 2006;Panikov et al, 2006;Lacelle et al, 2011).…”

Section: Discussionmentioning

confidence: 99%

“…Examples include, but are not limited to the following: measurements of hydrolytic enzyme activity (Gilichinsky et al, 1992); incorporation of isotopic labels/bromodeoxyuridine into macromolecules/ metabolites (Carpenter et al, 2000;Rivkina et al, 2000;Christner 2002;Junge et al, 2006;McMahon et al, 2009;Drotz et al, 2010); respiratory evolution of gases (for example, 14 CO 2 ) (Gilichinsky et al, 2003;Panikov et al, 2006;Steven et al, 2007;Lacelle et al, 2011); and 14 CO 2 incorporation into cells (Panikov and Sizova, 2007;Panikov, 2010 (Review)). Unfortunately, these bulk approaches cannot elucidate which specific microorganisms are growing in subzero environments (for example, native permafrost) or whether different members of the microbial community modulate their responses as a function of changing subzero temperatures.…”

Section: Introductionmentioning

confidence: 99%

Bacterial genome replication at subzero temperatures in permafrost

et al. 2013

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Microbial metabolic activity occurs at subzero temperatures in permafrost, an environment representing B25% of the global soil organic matter. Although much of the observed subzero microbial activity may be due to basal metabolism or macromolecular repair, there is also ample evidence for cellular growth. Unfortunately, most metabolic measurements or culture-based laboratory experiments cannot elucidate the specific microorganisms responsible for metabolic activities in native permafrost, nor, can bulk approaches determine whether different members of the microbial community modulate their responses as a function of changing subzero temperatures. Here, we report on the use of stable isotope probing with 13 C-acetate to demonstrate bacterial genome replication in Alaskan permafrost at temperatures of 0 to À 20 1C. We found that the majority (80%) of operational taxonomic units detected in permafrost microcosms were active and could synthesize 13 C-labeled DNA when supplemented with 13 C-acetate at temperatures of 0 to À 20 1C during a 6-month incubation. The data indicated that some members of the bacterial community were active across all of the experimental temperatures, whereas many others only synthesized DNA within a narrow subzero temperature range. Phylogenetic analysis of 13 C-labeled 16S rRNA genes revealed that the subzero active bacteria were members of the Acidobacteria, Actinobacteria, Chloroflexi, Gemmatimonadetes and Proteobacteria phyla and were distantly related to currently cultivated psychrophiles. These results imply that small subzero temperature changes may lead to changes in the active microbial community, which could have consequences for biogeochemical cycling in permanently frozen systems.

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“…As anticipated, Phoenix discovered a heterogeneous composition of icy soil just underlying the topsoil (mean depth of 4.6 cm) with similarities to what is found in certain types of terrestrial wedges Smith et al, 2009). On Earth, microorganisms have been isolated from similar ice wedges (Katayama et al, 2007), and cellular respiration is known to occur within the ice matrix of subsurface soil wedges (Lacelle et al, 2011). The confirmation of subsurface ice on Mars and the presence of ice-bound life on Earth are compelling evidence and affirm the need for study of the ecology and physiological capabilities of microbial life in ice wedges and an assessment as to how such a niche might sustain life on Earth or in analogous martian environments.…”

Section: Introductionmentioning

confidence: 97%

“…The microbial communities of a variety of terrestrial cryoenvironments have been studied, such as those found in glacier ice (Skidmore et al, 2000;Miteva et al, 2004), subglacial environments (Yde et al, 2010), cryoconite holes (Sä wströ m et al, 2002), Arctic permafrost soil (Steven et al, 2009;Wilhelm et al, 2011), Antarctic Dry Valley soils and endoliths (Pointing et al, 2009), cryopegs (Gilichinsky, 2002), ice shelves (Bottos et al, 2008), high Arctic saline perennial spring environments (Perreault et al, 2007;Niederberger et al, 2009Niederberger et al, , 2010, and various other ice environments (Lacelle et al, 2011). These studies reveal complex cold-tolerant microbial communities, some of which exhibit active metabolism at in situ temperatures in ice and brine (-5°C) (Niederberger et al, 2010;Bakermans and Skidmore, 2011) and permafrost (-15°C) (Steven et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Life at the Wedge: the Activity and Diversity of Arctic Ice Wedge Microbial Communities

et al. 2012

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The discovery of polygonal terrain on Mars underlain by ice heightens interest in the possibility that this water-bearing habitat may be, or may have been, a suitable habitat for extant life. The possibility is supported by the recurring detection of terrestrial microorganisms in subsurface ice environments, such as ice wedges found beneath tundra polygon features. A characterization of the microbial community of ice wedges from the high Arctic was performed to determine whether this ice environment can sustain actively respiring microorganisms and to assess the ecology of this extreme niche. We found that ice wedge samples contained a relatively abundant number of culturable cells compared to other ice habitats (∼10(5) CFU·mL(-1)). Respiration assays in which radio-labeled acetate and in situ measurement of CO(2) flux were used suggested low levels of microbial activity, though more sensitive techniques are required to confirm these findings. Based on 16S rRNA gene pyrosequencing, bacterial and archaeal ice wedge communities appeared to reflect surrounding soil communities. Two Pseudomonas sp. were the most abundant taxa in the ice wedge bacterial library (∼50%), while taxa related to ammonia-oxidizing Thaumarchaeota occupied 90% of the archaeal library. The tolerance of a variety of isolates to salinity and temperature revealed characteristics of a psychrotolerant, halotolerant community. Our findings support the hypothesis that ice wedges are capable of sustaining a diverse, plausibly active microbial community. As such, ice wedges, compared to other forms of less habitable ground ice, could serve as a reservoir for life on permanently cold, water-scarce, ice-rich extraterrestrial bodies and are therefore of interest to astrobiologists and ecologists alike. .

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Geomicrobiology and occluded O2–CO2–Ar gas analyses provide evidence of microbial respiration in ancient terrestrial ground ice

Cited by 26 publications

References 46 publications

Stable isotope and gas properties of two climatically contrasting (Pleistocene and Holocene) ice wedges from Cape Mamontov Klyk, Laptev Sea, northern Siberia

Stable isotope and gas properties of two climatically contrasting (Pleistocene and Holocene) ice wedges from Cape Mamontov Klyk, Laptev Sea, northern Siberia

Bacterial genome replication at subzero temperatures in permafrost

Life at the Wedge: the Activity and Diversity of Arctic Ice Wedge Microbial Communities

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