Introduction
High-latitude tundra is one of the most vulnerable ecosystems to climate
warming (Myers-Smith et al., 2015), wherein permafrost thawing and
changes of vegetation patterns have been observed during past decades
(Schuur, Crummer, Vogel, & Mack, 2007; Sturm, Racine, & Tape, 2001;
Xue et al., 2016). Given the fact that permafrost soil of high-latitude
tundra contains up to half of the global soil carbon (C) storage
(Tarnocai et al., 2009),
warming-induced permafrost C loss
to atmosphere could be one of the most severe concerns for accelerating
climate warming by greenhouse gas effects (Natali et al. 2011; Schuur et
al. 2009). In a warmer world, vast C may be released to the atmosphere
as a result of stimulated microbial activities to accelerate permafrost
C degradation (Mann et al., 2015; Zhou et al., 2012).
As
the major soil C decomposers, fungi may affect the C stability of
high-latitude tundra considerably (Christiansen et al., 2016).
For
instance, saprotrophic fungi are important regulators of soil nutrient
cycling via organic C decomposition, especially lignin (Buckeridge,
Banerjee, Siciliano, & Grogan, 2013; Yuste et al., 2011). In winter,
fungi are the largest proportion of soil microbial biomass and
predominantly affect wintertime C degradation (Buckeridge et al., 2013;
Schadt, Martin, Lipson, & Schmidt, 2003). Additionally, mycorrhizal
fungi form mutually beneficial associations to facilitate the growth of
arctic plants, especially those warming-responsive plant species such asSalix spp., and Betula nana (Clemmensen, Michelsen,
Jonasson, & Shaver, 2006), and thus can regulate C stability by
affecting primary productivity.
Therefore, responses of fungal
communities to climate warming would be determinative for the C fate in
tundra ecosystems.
Using
PCR-based marker gene sequencing, several in situ field studies
have demonstrated that experimental warming changes taxonomic
composition and environmental group abundances of fungal communities in
tundra soil, with increased diversity of saprotrophic fungi but
decreased diversity of ectomycorrhizal fungi (Morgado et al., 2016;
Mundra et al., 2016; Semenova et al., 2016). However, such taxonomic
information provides little insight into the relationship between fungal
functions and ecological processes.
Functional
gene analysis has been applied to quantify functional genes responsible
for key ecosystem processes. The main findings of previous studies
(Levy-Booth, Prescott, & Grayston, 2014; Yergeau, Kang, He, Zhou, &
Kowalchuk, 2007), i.e., close relationships between functional gene
abundances and ecosystem processes, have provided important insights on
the roles of microbial communities in ecosystem functioning.
In
addition to taxonomic composition, it is possible that fungal functional
genes, serving as markers of potential functional capacities, are
sensitive to climate warming. The justification includes 1) Temperature
affects the syntheses of cryoprotective compounds essential for
maintaining fungal growth and functions in cold environments (Weinstein,
Montiel, & Johnstone, 2000); 2) Temperature sensitivity of soil
heterotrophic respiration (measured as Q10) is
widespread (Malcolm, Lopez-Gutierrez, Koide, & Eissenstat, 2008),
implying that C degradation capacities of soil microorganisms including
fungi are variable; and 3) Plant litter input would be higher under
warming (Rinnan, Michelsen, Baath, & Jonasson, 2007), which may
stimulate fungi-mediated C degradation.
As the change of functional gene
composition can inevitably affect interactions among microbial members,
it is important to elucidate complex interactions among microbial
functional genes or species containing these genes in order to
understand ecosystem functioning (Wu et al., 2016). However, it remains
challenging due to myriad members in microbial communities and
difficulties in cultivating individual species. In recent years, network
analysis has been widely used to reveal potential interactions among
co-existing microbial members (Banerjee et al., 2016; Banerjee,
Schlaeppi, & van der Heijden, 2018; de Vries et al.,
2018).
Accumulating
evidence shows that network properties can reflect responses of
microbial communities to environmental disturbances (de Vries et al.,
2018; De Vries et al., 2012), as drought treatment in grassland
mesocosms led to higher connectivity and lower modularity of soil
bacterial networks than fungal networks, which suggested lower stability
of bacteria than fungi under drought (de Vries et al., 2018).
In the present work, we analyzed
the effects of winter warming on fungal communities in the active layer
of the Alaskan tundra, via 28S gene amplicon sequencing and GeoChip
technologies. Through installing snow fences to increase snow cover thus
winter soil temperature, we tested the following hypotheses: 1) Warming
would affect fungal community composition and potential interactions; 2)
Fungal C degradation capacities, represented by the abundances of C
degradation genes, would be increased by warming; 3)
Increased fungal C degradation
capacities could explain the increase of ecosystem respiration
(R eco), as recently witnessed in several studies
(Liu et al., 2015; Trivedi et al., 2016; Zhao et al., 2014).