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Microbes in thawing permafrost: The unknown variable in the climate change equation


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Considering that 25% of Earth s terrestrial surface is underlain by permafrost (ground that has been continuously frozen for at least 2 years), our understanding of the diversity of microbial life in this extreme habitat is surprisingly limited. Taking into account the total mass of perennially frozen sediment (up to several hundred meters deep), permafrost contains a huge amount of buried, ancient organic carbon (Tarnocai et al., 2009). In addition, permafrost is warming rapidly in response to global climate change (Romanovsky et al., 2010), potentially leading to widespread thaw and a larger, seasonally thawed soil active layer. This concern has prompted the question: will permafrost thawing lead to the release of massive amounts of carbon dioxide (CO2) and methane (CH4) into the atmosphere? This question can only be answered by understanding how the microbes residing in permafrost will respond to thaw, through processes such as respiration, fermentation, methanogenesis and CH4 oxidation (Schuur et al., 2009). Predicting future carbon fluxes is complicated by the diversity of permafrost environments, ranging from high mountains, southern boreal forests, frozen peatlands and Pleistocene ice complexes (yedoma) up to several hundred meters deep, which vary widely in soil composition, soil organic matter (SOM) quality, hydrology and thermal regimes (Figure 1). Permafrost degradation can occur in many forms: thaw can progress downward from seasonally-thawed active layer soils in warming climates or laterally because of changes in surface or groundwater flow paths (Grosse et al., 2011). Permafrost degradation can sometimes lead to dramatic changes in ecosystem structure and function
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Microbes in thawing permafrost: the unknown
variable in the climate change equation
David E Graham, Matthew D Wallenstein, Tatiana A Vishnivetskaya, Mark P Waldrop,
Tommy J Phelps, Susan M Pfiffner, Tullis C Onstott, Lyle G Whyte, Elizaveta M Rivkina,
David A Gilichinsky, Dwayne A Elias, Rachel Mackelprang, Nathan C VerBerkmoes,
Robert L Hettich, Dirk Wagner, Stan D Wullschleger and Janet K Jansson
The ISME Journal (2012) 6, 709–712; doi:10.1038/
ismej.2011.163; published online 17 November 2011
Considering that 25% of Earth’s terrestrial surface
is underlain by permafrost (ground that has
been continuously frozen for at least 2 years), our
understanding of the diversity of microbial life in
this extreme habitat is surprisingly limited. Taking
into account the total mass of perennially frozen
sediment (up to several hundred meters deep),
permafrost contains a huge amount of buried,
ancient organic carbon (Tarnocai et al., 2009). In
addition, permafrost is warming rapidly in response
to global climate change (Romanovsky et al., 2010),
potentially leading to widespread thaw and a larger,
seasonally thawed soil active layer. This concern
has prompted the question: will permafrost thawing
lead to the release of massive amounts of carbon
dioxide (CO
) and methane (CH
) into the atmo-
sphere? This question can only be answered by
understanding how the microbes residing in perma-
frost will respond to thaw, through processes
such as respiration, fermentation, methanogenesis
and CH
oxidation (Schuur et al., 2009).
Predicting future carbon fluxes is complicated by
the diversity of permafrost environments, ranging
from high mountains, southern boreal forests, frozen
peatlands and Pleistocene ice complexes (yedoma)
up to several hundred meters deep, which vary
widely in soil composition, soil organic matter
(SOM) quality, hydrology and thermal regimes
(Figure 1). Permafrost degradation can occur in
many forms: thaw can progress downward from
seasonally-thawed ‘active layer’ soils in warming
climates or laterally because of changes in surface
or groundwater flow paths (Grosse et al., 2011).
Permafrost degradation can sometimes lead to
dramatic changes in ecosystem structure and func-
tion, such as the formation of thermokarst bogs.
Wildfires and other disturbances that remove
vegetation and organic matter warm the ground,
hastening permafrost degradation. The complexity
of the Northern Arctic and Subarctic environments
in terms of geology, vegetation, paleohistory and
climate, suggests that understanding the microbial
ecology in permafrost regions will require numerous
studies throughout the Pan-Arctic.
Frozen conditions in permafrost efficiently
preserve biological material from DNA to wooly
mammoths. Low water potential, reduced protein
flexibility and enzyme activity, limited membrane
fluidity, and ice nucleation and melting are all
potentially lethal, so it was long assumed that
microbes were either dead or dormant when frozen.
However, high ionic strength within pore water
can depress the freezing point and preserve cell
viability. Recent experiments demonstrated that
permafrost microorganisms remain active at extre-
mely low temperatures (Vishnivetskaya et al., 2006;
Gilichinsky and Rivkina, 2011): indigenous bacteria
C-labeled acetate into lipids down to
20 1C, many isolates showed psychroactive growth
at 2.5 1C and acetotrophic methanogenesis contin-
ued between 5 1C and 17 1C. Thus, warming could
induce SOM decomposition even before permafrost
thaws completely. Microbial activity at low tem-
peratures could transform complex organic com-
pounds to soluble metabolites and gases, including
the greenhouse gases (GHG): CO
and N
(Figure 2). Microbial transformations of carbon and
nitrogen compounds in the soil active layer can in
turn affect plant productivity and community
composition, changing animal habitats and affecting
human land use. Although these gas fluxes and
landscape changes can be directly measured, we
need more detailed, mechanistic models that
integrate geochemical and structural parameters
with microbial processes to explain and predict
future changes in permafrost regions. In order to
accurately predict the vulnerability of permafrost
carbon to decomposition and the resulting fluxes of
GHG products, we should understand how Arctic
microbial communities respond to permafrost
thawing. In addition to an increase in the rate of organic
matter decomposition because of warming, there
will most likely be shifts in the microbial commu-
nity composition and in the relative consumption
of different organic constituents.
Here we address how combining information
about microbial identity (from phylotyping) and
The ISME Journal (2012) 6, 709 –712
2012 International Society for Microbial Ecology All rights reserved 1751-7362/12
metabolic potential (from metagenomes) with
information on what genes are expressed and
functioning (from metatranscriptomes and metapro-
teomes) (VerBerkmoes et al., 2009; Jansson, 2011)
has begun to open a new window of opportunity to
map and predict biochemical processes in soils.
They provide the tools to distinguish among
different mechanisms for increased organic matter
decomposition caused by increasing temperature
(Conant et al., 2011). Two potential applications of
this systems biology framework, discussed below,
illustrate how these molecular techniques could be
used to improve our ability to model SOM degrada-
tion rates and mechanisms, and to predict changes
in CH
and CO
emissions from thawing permafrost.
Currently, we cannot predict how microbes will
use SOM released by permafrost thawing, or reliably
estimate the temperature-dependent activities of the
enzymes they produce to degrade this material.
Current biogeochemical models segregate SOM into
conceptual pools with different mean residence
times (Smith et al., 1997). If most organic matter
trapped in permafrost is difficult to degrade because
of its chemical structure (for example, lignin) or its
physical structure (for example, particulates or
mineral complexes), then this humus comprises a
recalcitrant pool that will slowly stimulate micro-
bial growth and GHG production. Alternatively, if
plant litter was rapidly frozen in permafrost, then
microbes could quickly metabolize thawed poly-
mers like cellulose or protein. Although chemical
methods can be used to characterize this SOM, a
complementary approach could use transcriptional
and proteomic measurements of enzyme expression
to analyze the microbial response to this SOM and
infer its properties. Increased temperature may also
cause changes in protein structure and conforma-
tion, protein adsorption, altered protein expression
and shifts in microbial populations, which are not
currently modeled (Waldrop et al., 2010; Wallen-
stein et al., 2011). We might expect soil warming to
select for microbes producing enzymes that degrade
SOM more efficiently at higher temperatures. If
transcriptomic, proteomic and enzymatic analyses
confirm this hypothesis through experiments repli-
cating in situ conditions, then thermal acclimation
of enzymes would need to be incorporated into
models to accurately predict long-term C dynamics
in response to permafrost thaw (Allison et al., 2010).
Predictions of soil GHG flux include increasingly
sophisticated representations of processes in the
subsurface carbon cycle (Figure 2), but these models
are poorly parameterized for permafrost regions
(Riley et al., 2011). 16S rRNA gene sequence data
have identified both hydrogenotrophic and aceto-
trophic (methylotrophic) methanogen phylotypes in
Arctic tundra samples, at substantial abundance
(Wagner and Liebner, 2010). The two groups of
methanogens differ in their substrates, syntrophic
associations and isotopic fractionation of carbon:
it is important to distinguish between the methano-
genic pathways to predict the proportions of
and CO
, as well as fluxes (Walter et al.,
2008). Changes in methanogen abundance could
also confuse estimates of the temperature and pH
response factors. Comparative metagenomics can
identify changes in the abundance of characteristic
methanogen genes required for coenzyme biosynth-
esis and methyl-coenzyme M reductase production,
as well as methanotrophic genes from CH
bacteria. Metaproteomics can measure peptides
from highly abundant signature enzymes in soil
(Chourey et al., 2010), such as methyl-coenzyme M
reductase and CH
monooxygenase. This high-
Figure 1 Several Alaskan permafrost features that affect carbon cycling in northern circumpolar soils. (a) Low-centered polygonal
ground and thaw lakes from the North Slope; (b,c) polygonal tundra in Barrow; (d) thermokarst terrain in tussock tundra near
Council; (e) subsurface core section containing organic matter in permafrost from Fairbanks.
The ISME Journal
resolution portrait will help determine how the CH
flux changes in response to permafrost thawing, new
SOM inputs and increased fermentation by other
community members.
Until recently, the high microbial diversity of
Arctic soils (Bartram et al., 2011) has hindered
metagenomic studies. New technologies produce
sequences on an unprecedented scale, at a fraction
of the traditional cost. Accordingly, the first meta-
genomic analyses of permafrost are now becoming
available. An analysis of one active layer soil
and two-meter deep permafrost sample from the
Canadian high Arctic identified signature genes for
hydrogenotrophic methanogenesis, CH
by type I methanotrophs, nitrification and carbohy-
drate degradation (Yergeau et al., 2010). Microbial
abundances were 10–100 times lower in the perma-
frost than in the active layer sample, resulting in low
DNA yields and complicating the downstream
analysis. This report illustrates the feasibility and
challenges of large-scale comparative analyses
of metabolic potential in a complex permafrost
microbiome. To improve the analysis of permafrost
metagenomic data, more reference genome seque-
nces should be produced through parallel techniques,
such as genome sequencing of isolated or enriched
microbes and single-cell genome sequencing.
Eventually, microbial activities will dictate
whether permafrost environments will be a net
source or sink of GHG in the coming decades and
whether large-scale feedbacks to regional and global
climate will develop because of increased CO
and CH
emissions and vegetation changes in
the Arctic. The new ‘omics’ techniques of metage-
nomics, metatranscriptomics, metaproteomics and
metabolomics are developing at an opportune time
to provide process-level insights to microbial com-
munities’ responses to rapidly changing environ-
ments. We need this mechanistic understanding to
extrapolate beyond observed events and conse-
quently improve our ability to predict and quantify
GHG flux from different permafrost ecosystems as a
result of global warming. Biomolecular evidence of
key processes in nitrogen and carbon cycling is
essential for prioritizing and interpreting geochem-
ical measurements and representing them in high-
resolution ecosystem models. These detailed mod-
els could in turn help parameterize global climate
models. As a scientific community, we advocate
coordination and integration of our microbiological
data with geochemical measurements to determine
the magnitude and impacts of warming in high
latitude, circumpolar permafrost systems.
We thank Diana Swantek for assistance preparing Figure 2
and Peter Thornton for helpful discussions. This work is
funded in part by the US Department of Energy, Office of
Science, Biological and Environmental Research (BER)
Program. Oak Ridge National Laboratory is managed by
UT Battelle, LLC under Contract No. DE-AC05-00OR22725
for the US Department of Energy. Additional support was
provided by the US Department of Energy under Contract
No. DE-AC02-05CH11231 with the Lawrence Berkeley
National Laboratory.
DE Graham, TA Vishnivetskaya, TJ Phelps and
DA Elias are at Biosciences Division, Oak Ridge
National Laboratory, Oak Ridge, TN, USA;
MD Wallenstein is at Natural Resource Ecology
Laboratory, Colorado State University,
Fort Collins, CO, USA;
TA Vishnivetskaya and SM Pfiffner are at Center for
Figure 2 Key biological processes in the carbon cycle of permafrost environments. Permafrost thawing at the transition zone introduces
previously unavailable organic matter into the expanded active layer of soil. Enzymatic hydrolysis decomposes complex organic matter
into soluble substrates for microbial fermentation, producing a mixture of organic acids, alcohols and microbial biomass. Methanogenic
archaea convert acetate, methylated compounds or H
and CO
into CH
that can be released to the atmosphere through ebullition,
diffusion or aerenchyma. Methanotrophs oxidize some of this CH
, converting it to CO
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Environmental Biotechnology, The University of
Tennessee, Knoxville, TN, USA;
MP Waldrop is at United States Geological Survey,
Geologic Discipline, Menlo Park, CA, USA;
TC Onstott is at Department of Geosciences,
Princeton University, Princeton, NJ, USA;
LG Whyte is at Department of Natural Resource
Sciences, McGill University, Montre
Quebec, Canada;
EM Rivkina and DA Gilichinsky are at
Soil Cryology Laboratory,
Institute of Physicochemical and Biological
Problems in Soil Science, Russian Academy of
Sciences, Pushchino, Russia;
R Mackelprang and JK Jansson are at Department of
Energy, Joint Genome Institute,
Walnut Creek, CA, USA;
R Mackelprang is also at Department of
Biology, California State University Northridge,
Northridge, CA, USA;
NC VerBerkmoes and RL Hettich are at Chemical
Sciences Division, Oak Ridge National Laboratory,
Oak Ridge, TN, USA;
D Wagner is at Alfred Wegener Institute for Polar
and Marine Research, Research Unit Potsdam,
Potsdam, Germany;
SD Wullschleger is at Environmental Sciences
Division, Oak Ridge National Laboratory, Oak Ridge,
TN, USA and
JK Jansson is at Earth Sciences Division, Lawrence
Berkeley National Laboratory, Berkeley, CA, USA and
DoE Joint Bioenergy Institute, Emeryville,
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... However, there are several environmental settings where there is a non-negligible probability of long-dormant organisms being exposed to modern communities. In particular, unprecedented rates of melting of glaciers and permafrost [13,14] are now giving many types of icedormant microorganisms the opportunity to re-emerge [15][16][17][18][19][20][21]. There is also potential for ancient (or de-extinct) microorganisms to leak from laboratory facilities [22]. ...
... Speculation has so far dominated the discussion of the potential threats ancient re-emerging organisms will have on modern communities [16][17][18][19][20][21]38]. For the first time, we have taken advantage of the flexibility and realism of in silico evolution to provide an extensive exploration of the ecological risk of time-travelling pathogens. ...
Full-text available
Permafrost thawing and the potential ‘lab leak’ of ancient microorganisms generate risks of biological invasions for today’s ecological communities, including threats to human health via exposure to emergent pathogens. Whether and how such ‘time-travelling’ invaders could establish in modern communities is unclear, and existing data are too scarce to test hypotheses. To quantify the risks of time-travelling invasions, we isolated digital virus-like pathogens from the past records of coevolved artificial life communities and studied their simulated invasion into future states of the community. We then investigated how invasions affected diversity of the free-living bacteria-like organisms (i.e., host) in recipient communities compared to controls where no invasion occurred (and control invasions of contemporary pathogens). Invading pathogens could often survive and continue evolving, and in a few cases (3.1%) became exceptionally dominant in the invaded community. Even so, invaders often had negligible effects on the invaded community composition; however, in a few, highly unpredictable cases (1.1%), invaders precipitated either substantial losses (up to -32%) or gains (up to +12%) in the total richness of free-living species compared to controls. Given the sheer abundance of ancient microorganisms regularly released into modern communities, such a low probability of outbreak events still presents substantial risks. Our findings therefore suggest that unpredictable threats so far confined to science fiction and conjecture could in fact be powerful drivers of ecological change.
... Both gradual and abrupt thaw introduces novel stressors to permafrost ecosystems where microbial life persists in thin brine channels of liquid water, slowly metabolizing and transforming organic matter over millennia ( Fig. 1) (Graham et al., 2012;Ward et al., 2017;Miner et al., 2021). Gradual thaw describes a steady downward movement of nearsurface permafrost. ...
Full-text available
Permafrost is important from an exobiology and climate change perspective. It serves as an analog for extraplanetary exploration, and it threatens to emit globally significant amounts of greenhouse gases as it thaws due to climate change. Viable microbes survive in Earth's permafrost, slowly metabolizing and transforming organic matter through geologic time. Ancient permafrost microbial communities represent a crucial resource for gaining novel insights into survival strategies adopted by extremotolerant organisms in extraplanetary analogs. We present a proof-of-concept study on ∼22 Kya permafrost to determine the potential for coupling Raman and fluorescence biosignature detection technology from the NASA Mars Perseverance rover with microbial community characterization in frozen soils, which could be expanded to other Earth and off-Earth locations. Besides the well-known utility for biosignature detection and identification, our results indicate that spectral mapping of permafrost could be used to rapidly characterize organic carbon characteristics. Coupled with microbial community analyses, this method has the potential to enhance our understanding of carbon degradation and emissions in thawing permafrost. Further, spectroscopy can be accomplished in situ to mitigate sample transport challenges and in assessing and prioritizing frozen soils for further investigation. This method has broad-range applicability to understanding microbial communities and their associations with biosignatures and soil carbon and mineralogic characteristics relevant to climate science and astrobiology.
... Persistent and widespread permafrost warming and thawing result in enhanced degradation and mineralization of the large organic carbon pool in permafrost active layer by these diverse microorganisms [8,9], contributing to a major positive feedback between climate warming and atmospheric carbon dioxide rise [2,10]. Thus, microbial variables have attracted growing attention to be incorporated into models to accurately predict future changes of permafrost carbon dynamics due to their importance in influencing biogeochemical processes [10][11][12]. However, comparing to our understanding of bacterial and archaeal communities in permafrost [13][14][15], we know much less about microbial eukaryotic communities in permafrost. ...
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Permafrost active layer soils are harsh environments with thaw/freeze cycles and sub-zero temperatures, harboring diverse microorganisms. However, the distribution patterns, assembly mechanism, and driving forces of soil microeukaryotes in permafrost remain largely unknown. In this study, we investigated microeukaryotes in permafrost active layer across the Qinghai-Tibet Plateau (QTP) using 18S rRNA gene sequencing. The results showed that the microbial eukaryotic communities were dominated by Nematozoa, Ciliophora, Ascomycota, Cercozoa, Arthropoda, and Basidiomycota in terms of relative abundance and operational taxonomic unit (OTU) richness. Nematozoa had the highest relative abundance, while Ciliophora had the highest OTU richness. These phyla had strong interactions between each other. Their alpha diversity and community structure were differently influenced by the factors associated to location, climate, and soil properties, particularly the soil properties. Significant but weak distance-decay relationships with different slopes were established for the communities of these dominant phyla, except for Basidiomycota. According to the null model, community assemblies of Nematozoa and Cercozoa were dominated by heterogeneous selection, Ciliophora and Ascomycota were dominated by dispersal limitation, while Arthropoda and Basidiomycota were highly dominated by non-dominant processes. The assembly mechanisms can be jointly explained by biotic interactions, organism treats, and environmental influences. Modules in the co-occurrence network of the microeukaryotes were composed by members from different taxonomic groups. These modules also had interactions and responded to different environmental factors, within which, soil properties had strong influences on these modules. The results suggested the importance of biological interactions and soil properties in structuring microbial eukaryotic communities in permafrost active layer soil across the QTP.
... The vulnerability of permafrost carbon to decomposition and subsequent greenhouse gas release can be dictated by the microbial community response to thaw (Feng et al., 2020). This alteration of bacterial and archaeal communities in thawing permafrost has generally been associated with an increase in greenhouse gas production (Graham et al., 2012). Bacteria and archaea in thawing permafrost accelerate carbon and nutrient cycling processes, including denitrification (Marushchak et al., 2021), ferrous iron reduction (Patzner et al., 2020), hydrogenotrophic and acetoclastic methanogenesis (McCalley et al., 2014), methanotrophy (Singleton et al., 2018), mercury methylation (Tarbier et al., 2021), sulfate reduction (Hultman et al., 2015;Mackelprang et al., 2016), and fermentation (Wu et al., 2022). ...
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In recent decades the habitat of North American beaver (Castor canadensis) has expanded from boreal forests into Arctic tundra ecosystems. Beaver ponds in Arctic watersheds are known to alter stream biogeochemistry, which is likely coupled with changes in the activity and composition of microbial communities inhabiting beaver pond sediments. We investigated bacterial, archaeal, and fungal communities in beaver pond sediments along tundra streams in northwestern Alaska (AK), USA and compared them to those of tundra lakes and streams in north‐central Alaska that are unimpacted by beavers. β‐glucosidase activity assays indicated higher cellulose degradation potential in beaver ponds than in unimpacted streams and lakes within a watershed absent of beavers. Beta diversity analyses showed that dominant lineages of bacteria and archaea in beaver ponds differed from those in tundra lakes and streams, but dominant fungal lineages did not differ between these sample types. Beaver pond sediments displayed lower relative abundances of Crenarchaeota and Euryarchaeota archaea and of bacteria from typically anaerobic taxonomic groups, suggesting differences in rates of fermentative organic matter (OM) breakdown, syntrophy, and methane generation. Beaver ponds also displayed low relative abundances of Chytridiomycota (putative non‐symbiotic) fungi and high relative abundances of ectomycorrhizal (plant symbionts) Basidiomycota fungi, suggesting differences in the occurrence of plant and fungi mutualistic interactions. Beaver ponds also featured microbes with taxonomic identities typically associated with the cycling of nitrogen and sulfur compounds in higher relative abundances than tundra lakes and streams. These findings help clarify the microbiological implications of beavers expanding into high latitude regions.
... Permafrost collapse greatly affects total nitrogen distribution and soil organic carbon stabilization (Mu et al. 2020). Moreover, permafrost collapse could regulate soil microbial functions and microbially mediated biogeochemical cycles (Graham et al. 2012;Liu et al. 2020). Waldrop et al. (2021) found that the youngest collapse-scar bog had the highest CH 4 production potential from soil incubation and higher summer in situ rates of respiration compared to permafrost plateaus or older collapsed scar swamps. ...
Full-text available
Due to ongoing climate change, permafrost collapse has become widely distributed across the Qinghai-Tibet Plateau (QTP). However, it is not yet understood how soil microbial composition changes after the development of permafrost collapse. In this study, evaluations were conducted on three stages (the collapsed areas, the collapsing area and the control areas) of the permafrost collapse. The composition and biomass of the soil microorganisms were quantified by the phospholipid fatty acid (PLFA) method. The results showed that the permafrost collapse stages affected the soil microbial communities. The PCA suggested that the soil microbial communities were separated into 3 groups, i.e., the control areas, collapsing areas and collapsed areas. The contents of total PLFAs, gram-negative (GN) bacteria, total bacteria and fungi in the collapsed areas and the collapsing areas were significantly lower than those in the control areas. Soils in the collapsing areas had higher abundance of GN bacteria, total bacteria, total PLFAs and gram-positive bacteria to gram-negative (GP/GN) ratio than those in the collapsed areas. The collapsed areas had a higher ratio of GP/GN among the three stages. The soil microbial communities did not change significantly with increasing soil depth. The contents of GN bacteria, actinomycetes and total PLFAs had a significant positive correlation with pH. The contents of GP bacteria and the GP/GN ratio were positively correlated with soil water content (SWC). Soil microbial biomass decreased significantly during the permafrost collapse development. The inherent characteristics of soil physicochemical properties, especially soil pH and SWC, are the main factors affecting changes in microbial communities after the development of permafrost collapse.
... It is well known that heter otr ophic bacteria and fungi are fundamental in driving soil carbon decomposition and stabilization (e.g. Graham et al. 2012, Deng et al. 2015, Altshuler et al. 2017, Feng et al. 2020. In response to increased temperature and alter ed pr ecipitation r egimes, micr obial mediated miner alization of SOM stored in Arctic soils is expected to be one of the most important feedback effects on the global climate system (Schuur et al. 2015 ). ...
The Arctic soil communities play a vital role in stabilizing and decomposing soil carbon, which affects the global carbon cycling. Studying the food web structure is critical for understanding biotic interactions and the functioning of these ecosystems. Here we studied the trophic relationships of (microscopic) soil biota of two different Arctic spots in Ny-Ålesund, Svalbard, within a natural soil moisture gradient by combining DNA analysis with stable isotopes as trophic tracers. The results of our study suggested that the soil moisture strongly influenced the diversity of soil biota, with the wetter soil, having a higher organic matter content, hosting a more diverse community. Based on a Bayesian mixing model, the community of wet soil formed a more complex food web, in which bacterivorous and detritivorous pathways were important in supplying carbon and energy to the upper trophic levels. In contrast, the drier soil showed a less diverse community, lower trophic complexity, with the green food web (via unicellular green algae and gatherer organisms) playing a more important role in channelling energy to higher trophic levels. These findings are important to better understand the soil communities inhabiting the Arctic, and for predicting how the ecosystem will respond to the forthcoming changes in precipitation regimes.
... Near-surface permafrost-up to 3 m deep-contains around 10 12 tons of C globally, or about 33% of the total soil pool [3]. Climate change driven permafrost thaw may generate substantial climate feedbacks, as carbon dioxide and methane released by thawing permafrost contribute to further warming [4]. Permafrost thaw can also alter surface geomorphologic processes and affect surface water chemistry [5,6]. ...
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Understanding how soil microbes respond to permafrost thaw is critical to predicting the implications of climate change for soil processes. However, our knowledge of microbial responses to warming is mainly based on laboratory thaw experiments, and field sampling in warmer months when sites are more accessible. In this study, we sample a depth profile through seasonally thawed active layer and permafrost in the Imnavait Creek Watershed, Alaska, USA over the growing season from summer to late fall. Amplicon sequencing showed that bacterial and fungal communities differed in composition across both sampling depths and sampling months. Surface communities were most variable, while those from the deepest samples, which remained frozen throughout our sampling period, showed little to no variation over time. However, community variation was not explained by trace metal concentrations, soil nutrient content, pH, or soil condition (frozen/thawed), except insofar as those measurements were correlated with depth. Our results highlight the importance of collecting samples at multiple times throughout the year to capture temporal variation, and suggest that data from across the annual freeze-thaw cycle might help predict microbial responses to permafrost thaw.
... As key decomposers of organic C in permafrost (Falkowski et al., 2008;Jansson and Tas, 2014), soil microorganisms can regulate the ecosystem C balance in permafrost-affected regions under warm climate conditions (Graham et al., 2012;Crowther et al., 2019). Therefore, understanding the quantitative information regarding soil communities that drive elemental cycling as well as the environmental conditions that regulate their activity in permafrost-affected regions is important for accurately predicting the permafrost C feedback (Mondav et al., 2014;Monteux et al., 2018;Crowther et al., 2019). ...
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Under warm climate conditions, permafrost thawing results in the substantial release of carbon (C) into the atmosphere and potentially triggers strong positive feedback to global warming. Soil microorganisms play an important role in decomposing organic C in permafrost, thus potentially regulating the ecosystem C balance in permafrost-affected regions. Soil microbial community and biomass are mainly affected by soil organic carbon (SOC) content and soil texture. Most studies have focused on acidic permafrost soil (pH < 7), whereas few examined alkaline permafrost-affected soil (pH > 7). In this study, we analyzed soil microbial communities and biomass in the alpine desert and steppe on the Tibetan plateau, where the soil pH values were approximately 8.7 ± 0.2 and 8.5 ± 0.1, respectively. Our results revealed that microbial biomass was significantly associated with mean grain size (MGS) and SOC content in alkaline permafrost-affected soils (p < 0.05). In particular, bacterial and fungal biomasses were affected by SOC content in the alpine steppe, whereas bacterial and fungal biomasses were mainly affected by MGS and SOC content, respectively, in the alpine desert. Combined with the results of the structural equation model, those findings suggest that SOC content affects soil texture under high pH-value (pH 8–9) and that soil microbial biomass is indirectly affected. Soils in the alpine steppe and desert are dominated by plagioclase, which provides colonization sites for bacterial communities. This study aimed to highlight the importance of soil texture in managing soil microbial biomass and demonstrate the differential impacts of soil texture on fungal and bacterial communities in alkaline permafrost-affected regions.
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Soil viruses are highly abundant and have important roles in the regulation of host dynamics and soil ecology. Climate change is resulting in unprecedented changes to soil ecosystems and the life forms that reside there, including viruses. In this Review, we explore our current understanding of soil viral diversity and ecology, and we discuss how climate change (such as extended and extreme drought events or more flooding and altered precipitation patterns) is influencing soil viruses. Finally, we provide our perspective on future research needs to better understand how climate change will impact soil viral ecology. Soil viruses are highly abundant and have important roles in the regulation of host dynamics and soil ecology. In this Review, Jansson and Wu explore our current understanding of soil viral diversity and ecology, and how climate change (such as extended and extreme drought events or more flooding and altered precipitation patterns) is influencing soil viruses.
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Terrestrial net CH<sub>4</sub> surface fluxes often represent the difference between much larger gross production and consumption fluxes and depend on multiple physical, biological, and chemical mechanisms that are poorly understood and represented in regional- and global-scale biogeochemical models. To characterize uncertainties, study feedbacks between CH<sub>4</sub> fluxes and climate, and to guide future model development and experimentation, we developed and tested a new CH<sub>4</sub> biogeochemistry model (CLM4Me) integrated in the land component (Community Land Model; CLM4) of the Community Earth System Model (CESM1). CLM4Me includes representations of CH<sub>4</sub> production, oxidation, aerenchyma transport, ebullition, aqueous and gaseous diffusion, and fractional inundation. As with most global models, CLM4 lacks important features for predicting current and future CH<sub>4</sub> fluxes, including: vertical representation of soil organic matter, accurate subgrid scale hydrology, realistic representation of inundated system vegetation, anaerobic decomposition, thermokarst dynamics, and aqueous chemistry. We compared the seasonality and magnitude of predicted CH<sub>4</sub> emissions to observations from 18 sites and three global atmospheric inversions. Simulated net CH<sub>4</sub> emissions using our baseline parameter set were 270, 160, 50, and 70 Tg CH<sub>4</sub> yr<sup>−1</sup> globally, in the tropics, in the temperate zone, and north of 45° N, respectively; these values are within the range of previous estimates. We then used the model to characterize the sensitivity of regional and global CH<sub>4</sub> emission estimates to uncertainties in model parameterizations. Of the parameters we tested, the temperature sensitivity of CH<sub>4</sub> production, oxidation parameters, and aerenchyma properties had the largest impacts on net CH<sub>4</sub> emissions, up to a factor of 4 and 10 at the regional and gridcell scales, respectively. In spite of these uncertainties, we were able to demonstrate that emissions from dissolved CH<sub>4</sub> in the transpiration stream are small (<1 Tg CH<sub>4</sub> yr<sup>−1</sup>) and that uncertainty in CH<sub>4</sub> emissions from anoxic microsite production is significant. In a 21st century scenario, we found that predicted declines in high-latitude inundation may limit increases in high-latitude CH<sub>4</sub> emissions. Due to the high level of remaining uncertainty, we outline observations and experiments that would facilitate improvement of regional and global CH<sub>4</sub> biogeochemical models.
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From a microbiological perspective, soil is largely unexplored even though we know it has a rich diversity of microbial life. Depending on its physical and chemical properties, soil can contain 109-1010 microbial cells per gram, including tens of thousands of different bacterial, archaeal, and fungal species, plus viruses and protists.
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This synthesis addresses the vulnerability of the North American high-latitude soil organic carbon (SOC) pool to climate change. Disturbances caused by climate warming in arctic, subarctic, and boreal environments can result in significant redistribution of C among major reservoirs with potential global impacts. We divide the current northern high-latitude SOC pools into (1) near-surface soils where SOC is affected by seasonal freeze-thaw processes and changes in moisture status, and (2) deeper permafrost and peatland strata down to several tens of meters depth where SOC is usually not affected by short-term changes. We address key factors (permafrost, vegetation, hydrology, paleoenvironmental history) and processes (C input, storage, decomposition, and output) responsible for the formation of the large high-latitude SOC pool in North America and highlight how climate-related disturbances could alter this pool's character and size. Press disturbances of relatively slow but persistent nature such as top-down thawing of permafrost, and changes in hydrology, microbiological communities, pedological processes, and vegetation types, as well as pulse disturbances of relatively rapid and local nature such as wildfires and thermokarst, could substantially impact SOC stocks. Ongoing climate warming in the North American high-latitude region could result in crossing environmental thresholds, thereby accelerating press disturbances and increasingly triggering pulse disturbances and eventually affecting the C source/sink net character of northern high-latitude soils. Finally, we assess postdisturbance feedbacks, models, and predictions for the northern high-latitude SOC pool, and discuss data and research gaps to be addressed by future research.
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1] This study reports an atmospheric methane (CH 4) source term previously uncharacterized regarding strength and isotopic composition. Methane emissions from 14 Siberian lakes and 9 Alaskan lakes were characterized using stable isotopes (13 C and D) and radiocarbon (14 C) analyses. We classified ebullition (bubbling) into three categories (background, point sources, and hot spots) on the basis of fluxes, major gas concentrations, and isotopic composition. Point sources and hot spots had a strong association with thermokarst (thaw) erosion because permafrost degradation along lake margins releases ancient organic matter into anaerobic lake bottoms, fueling methanogenesis. With increasing ebullition rate, we observed increasing CH 4 concentration of greater radiocarbon age, depletion of 13 C CH4 , and decreasing bubble N 2 content. Microbial oxidation of methane was observed in bubbles that became trapped below and later within winter lake ice; however, oxidation appeared insignificant in bubbles sampled immediately after release from sediments. Methanogenic pathways differed among the bubble sources: CO 2 reduction supported point source and hot spot ebullition to a large degree, while acetate fermentation appeared to contribute to background bubbling. To provide annual whole-lake and regional CH 4 isofluxes for the Siberian lakes, we combined maps of bubble source distributions with long-term, continuous flux measurements and isotopic composition. In contrast to typical values used in inverse models of atmospheric CH 4 for northern wetland sources (d 13 C CH4 = À58%, 14 C age modern), which have not included northern lake ebullition as a source, we show that this large, new source of high-latitude CH 4 from lakes is isotopically distinct (d 13 C CH4 = À70%, 14 C age 16,500 years, for North Siberian lakes).
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1] The Northern Circumpolar Soil Carbon Database was developed in order to determine carbon pools in soils of the northern circumpolar permafrost region. The area of all soils in the northern permafrost region is approximately 18,782 Â 10 3 km 2 , or approximately 16% of the global soil area. In the northern permafrost region, organic soils (peatlands) and cryoturbated permafrost-affected mineral soils have the highest mean soil organic carbon contents (32.2–69.6 kg m À2). Here we report a new estimate of the carbon pools in soils of the northern permafrost region, including deeper layers and pools not accounted for in previous analyses. Carbon pools were estimated to be 191.29 Pg for the 0–30 cm depth, 495.80 Pg for the 0–100 cm depth, and 1024.00 Pg for the 0–300 cm depth. Our estimate for the first meter of soil alone is about double that reported for this region in previous analyses. Carbon pools in layers deeper than 300 cm were estimated to be 407 Pg in yedoma deposits and 241 Pg in deltaic deposits. In total, the northern permafrost region contains approximately 1672 Pg of organic carbon, of which approximately 1466 Pg, or 88%, occurs in perennially frozen soils and deposits. This 1672 Pg of organic carbon would account for approximately 50% of the estimated global belowground organic carbon pool.
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The response of soil organic matter (OM) decomposition to increasing temperature is a critical aspect of ecosystem responses to global change. The impacts of climate warming on decomposition dynamics have not been resolved due to apparently contradictory results from field and lab experiments, most of which has focused on labile carbon with short turnover times. But the majority of total soil carbon stocks are comprised of organic carbon with turnover times of decades to centuries. Understanding the response of these carbon pools to climate change is essential for forecasting longer-term changes in soil carbon storage. Herein, we briefly synthesize information from recent studies that have been conducted using a wide variety of approaches. In our effort to understand research to-date, we derive a new conceptual model that explicitly identifies the processes controlling soil OM availability for decomposition and allows a more explicit description of the factors regulating OM decomposition under different circumstances. It explicitly defines resistance of soil OM to decomposition as being due either to its chemical conformation (quality) or its physico-chemical protection from decomposition. The former is embodied in the depolymerization process, the latter by adsorption/desorption and aggregate turnover. We hypothesize a strong role for variation in temperature sensitivity as a function of reaction rates for both. We conclude that important advances in understanding the temperature response of the processes that control substrate availability, depolymerization, microbial efficiency, and enzyme production will be needed to predict the fate of soil carbon stocks in a warmer world.
In polar regions, huge layers of frozen ground, termed permafrost, are formed. Permafrost covers more than 25% of the land surface and significant parts of the coastal sea shelves. Permafrost habitats are controlled by extreme climate and terrain conditions. Particularly, the seasonal freezing and thawing in the upper active layer of permafrost leads to distinct gradients in temperature and geochemistry. Methanogenic archaea in permafrost environments have to survive extremely cold temperatures, freeze-thaw cycles, desiccation and starvation under long-lasting background radiation over geological time scales. Although the biology of permafrost microorganisms remains relatively unexplored, recent findings show that methanogenic communities in this extreme environment are composed by members of the major phyla of the methanogenic archaea (Methanobrevibacter, Methanobacterium, Methanosaeta, Methanosarcina, Methanolobus/Methanohalophylus/Methanococcoides, Methanoculleus/Methanogenium), with a total biomass comparable to temperate soil ecosystems. Currently, methanogenic archaea were the object of particular attention in permafrost studies, because of their key role in the Arctic methane cycle and consequently of their significance for the global methane budget.