4. DISCUSSION
In this study, we discovered that distinct variation trends of soil
microbiomes during desertification regulated the changes in
multifunctionality
in
vertical soil profiles. Notably, particular microbial taxa rather than
microbial diversity better predicted the vertical profile variation in
multifunctionality in desert ecosystems. Our results highlight the
significance of deep soil microbiomes for buffering and regulating the
multifunctionality of desert
ecosystems.
4.1 Variation in multifunctionality in desert
ecosystems
Deep
soil multifunctionality was as important as superficial soil
multifunctionality in the desert ecosystems (Fig. 1). The results of
this study confirmed our first hypothesis. Desertification can lead to
the loss of surface soil C, N and P and fine soil particles and
decreases in the water-holding capacity and vegetation cover (D’Odorico
et al., 2013; Ravi et al., 2010; Ward et al., 2018). Soil pores and
water
infiltration
in superficial soil exhibited continuous increases due to the gradual
loss of fine soil particles during desertification (Allington & Valone,
2010; D’Odorico et al., 2007), leading to enhanced nutrient accumulation
in deep soils from plant litter and superficial soil nutrients.
Furthermore, microbiomes play a vital role in regulating soil
multifunctionality by supporting functional processes (i.e., soil
nutrient cycling, litter decomposition, and N mineralization), which
allow the transfer of materials and carbon energy between above- and
belowground communities (Falkowski et al., 2008; Tedersoo et al., 2014).
Thus, the simultaneous changes in and coupling of soil physical
properties and vegetation and microbiomes jointly contributed to the
equivalent multifunctionalities of superficial and deep soils (D’Odorico
et al., 2019; Jiao et al., 2018; Ravi et al., 2010). In addition, soil
nutrients are mainly derived from the decomposition of plant litter and
root in both undisturbed and restored ecosystems (Barber et al., 2017;
Lozano et al., 2014). In this study, the plant litter and root biomass
gradually decreased during desertification (Figure S8), leading to
reduced soil nutrient accumulation from litter and root decomposition,
which was largely responsible for the significant decrease in
multifunctionality in the vertical soil profiles along the
desertification gradient (Fig. 1c).
4.2 Vertical variation in soil microbiomes in desert
ecosystems
Our results showed that the desertification process drove distinct
variation trends of the microbiomes in the vertical soil profiles.
Microbial survival and growth may be severely limited by continuous
abiotic stressors (i.e., limited bioavailability of water and C
substrates), frequent disturbances (i.e., drying-rewetting events), and
heterogeneous distributions of substrates across soil profiles (Fierer,
2017). In desert ecosystems, all these abiotic stressors often
synchronously appear during desertification, which is characterized by
decreasing plant biomass and fluctuating soil nutrients and soil
structure, leading to enhanced environmental stress gradients that
account for the distinct variation in microbiomes in vertical soil
profiles (D’Odorico et al., 2013; D’Odorico et al., 2019; Neilson et
al., 2017). Furthermore, the phyla Actinobacteria, Proteobacteria,
Chloroflexi, Acidobacteria, Ascomycota, Basidiomycota, Thaumarchaeota
and Euryarchaeota were the most abundant microbial taxa with distinct
responses in the desert ecosystems. These phylum-level profiles were
similar to those in other soils and environments (Jiao et al., 2018; Li
et al., 2014; Tedersoo et al., 2014; Upton et al., 2020). We further
found that bacteria are on average more resilient in the face of
disturbances and perturbations because of their relatively fast
intrinsic growth rates (Wardle, 2013), suggesting that they are more
sensitive to the environmental filtering driven by desertification. As
soil depth increased, the bacterial phyla Acidobacteria, Actinobacteria,
and Chloroflexi typically declined, while
Proteobacteria
significantly increased (Figs. S4 and S5). The majority of
Acidobacteria, Actinobacteria,
Proteobacteria, and Chloroflexi have
been suggested to be closely associated with organic substrates
(Goldfarb et al., 2011). Except for the response of Proteobacteria,
these observed changes were further confirmed by the findings of other
studies (Jiao et al., 2018; Li et al., 2014), suggesting that soil pH
and nutrient bioavailability are more likely to be the reasons for the
decreased relative abundance in soil profiles. In this study, Alpha-,
Delta-, and Gammaproteobacteria belonging to the class Proteobacteria
were examined (Figure S2). Alpha- and Deltaproteobacteria have been
suggested to be negatively associated with increased organic substrates,
while Gammaproteobacteria are positively associated with increased
organic substrates (Goldfarb et al., 2011). This contrasting pattern
could reflect divergent ecological niches and microbial synergism, which
are more likely to be the reasons for the enhanced abundance of
Proteobacteria in the vertical soil profiles, as reported by Li et al.
(2014) in farmland ecosystems. In addition, the most abundant fungal
phyla
(Ascomycota
and Basidiomycota) were less mobile in vertical soil profiles than
bacterial and archaeal phyla in the desert ecosystems, similar to
previous findings (Tedersoo et al., 2014), suggesting that the richness
of fungi and functional groups is not associated with plant productivity
and that the plant-soil feedback loop does not typically reshape fungal
diversity in different ecosystems. The archaeal phyla Thaumarchaeota and
Euryarchaeota mainly drive soil N cycling (Haroon et al., 2013;
Leininger et al., 2006). Thus, the gradual decrease in N substrate in
vertical soil profiles is more likely to be the reason for the decreased
relative abundance of Thaumarchaeota and Euryarchaeota.
Alpha-diversity can characterize the number of microbial taxa within
sample sites, while beta diversity can describe the variation trend of
microbial composition across sample sites (de Carvalho et al., 2016;
Legendre & De Cáceres, 2013). Previous work has suggested that the
alpha-diversity (i.e., Shannon and OTU richness indexes) of bacteria and
fungi decreases while archaeal diversity typically increases with
increasing soil depth in different systems (i.e., grassland, forest and
farmland) (Eilers et al., 2012; Jiao et al., 2018). Our results further
indicated that bacterial diversity decreased, archaeal diversity
increased, and fungal diversity fluctuated with increasing soil depth
along a desertification gradient (Fig. 2). These discordant patterns of
soil microbiomes were due to their distinct ecological niches and
differences in oxygen tolerance,
showing that bacteria and fungi are mainly aerobic, while archaea are
mainly anaerobic (Haroon et al., 2013; Upton et al., 2020). The oxygen
content gradually decreased with soil depth in the desert ecosystems,
given the increasing water content with increasing depth resulting from
high soil water infiltration (D’Odorico et al., 2007). In addition,
ecological restoration characterized by increased availability of soil C
and N significantly enhanced the alpha- and beta-diversity of bacteria
and archaea but not fungi (Barber et al., 2017; Jiao et al., 2018;
Lozano et al., 2014). In contrast to ecological restoration,
desertification is characterized by decreasing soil C and N, which may
be the reason for the decreased alpha- and beta-diversity of bacteria
and archaea in the vertical soil profiles as desertification proceeded.
In this study, the indistinctive alpha- and beta-diversity of fungi
suggested the stable performance of fungal communities in desert
ecosystems (Figs. 2 and 3). Fungi are heterotrophic microorganisms that
play fundamental ecological roles as decomposers, such as the
decomposition of litter and senescence or death of roots (Tedersoo et
al., 2014). In this study, the litter and root supplies decreased as
desertification progressed, and this unfavourable and variable habitat
was ineffective in completely restraining the growth and enrichment of
fungi. The fungal kingdom contains a large proportion of various niche
strategies ranging from saprotrophy through mutualism to parasitism
across trophic levels (Nilsson et al., 2019). In addition, fungal
communities with filamentous growth
may show different interactions because of dispersal limitation and
greater tolerance of desiccation (Austin et al., 2004; Fukami et al.,
2010; Powell et al., 2015), leading to their co-enrichment and distinct
vertical distributions.
4.3 Main predictors of ecosystem multifunctionality in
desert
ecosystems
Our results indicated that particular microbial phyla rather than total
microbial diversity better predicted and explained the vertical profile
variation in soil multifunctionality in desert ecosystems. The results
of this study confirmed our second hypothesis. Experiments at the
microcosm and global scales showed that microbial diversity variables
(i.e., Shannon and phylogenetic diversity indexes and OTU richness) are
important predictors of multifunctionality and are positively linked to
superficial soil multifunctionality (Delgado-Baquerizo et al., 2016; Li
et al., 2019; Wagg et al., 2014; Zheng et al., 2019), suggesting that
microbial communities with higher richness perform better under varying
conditions and better protect against the loss of taxa. However, our
knowledge is largely based on microbial diversity and dominance in
superficial soil, and less attention has been paid to deep soils of
desert ecosystems. Our results suggested that individual bacterial and
archaeal species are more important predictors of multifunctionality in
desert soils, especially in deep soils (20-100 cm). These individual
bacterial and archaeal species in deep soils may play a leading role in
driving soil multifunctionality, which to some extent could explain why
the process of desertification significantly decreased soil
multifunctionality (Fig. 1) and dominant bacterial and fungal phyla
maintained synchronous positive feedbacks (Figures. S3, S4, and S5). In
contrast to those of bacterial and archaeal taxa, the links between
individual species of fungi and ecosystem function are dependent on the
presence of other species and a result of multiple interactions (i.e.,
positive and negative as well as direct and indirect) between the
various species that as a whole regulate potential ecosystem functions
(Tedersoo et al., 2014; Wagg et al., 2019).
Intriguingly, our results showed a disproportionate role of individual
species (i.e., Acidobacteria or their strategic alliances) in
multifunctionality, which seems counter-intuitive given their higher
than expected ecological importance in soil microbial communities (Figs.
4 and 5). Acidobacteria in soil habitats are considered ubiquitous and
physiologically active but are rarely cultured and consequently remain a
poorly studied phylum (Goldfarb et al., 2011; Naether et al., 2012). The
phylogenetic diversity and relative abundance of Acidobacteria in
diverse habitats have suggested their vital role in driving
biogeochemical processes and diverse metabolic functions (Naether et
al., 2012). High C bioavailability is negatively associated with
acidobacterial abundance in various soils (Fierer et al., 2007; Goldfarb
et al., 2011), suggesting that Acidobacteria are adapted to habitats
with poor substrates and often slow-growing oligotrophs. Indeed, the
acidobacterial community can be energetically adapted to C-limited soils
and may be predominant in oligotrophic habitats, where decreasing plant
biomass results in a decrease in the availability of plant-derived C
sources (Castro et al., 2010).
Microbial diversity can maintain and regulate multifunctionality in a
variety of ways, suggesting that microbial communities with higher total
richness perform better in progressively developed and
less-stressed
soils (i.e., forest, cropland, and wetland soils) (Delgado-Baquerizo et
al., 2016; Jiao et al., 2018; Li et al., 2019; Wagg et al., 2014).
Conversely, multifunctionality may be controlled by particular microbial
taxa (relative abundance of phylotypes) but not the total richness and
abundance of microbial communities in dryland soils (Delgado-Baquerizo
et al., 2017). Interestingly, our results further support the notion
that particular microbial phyla (microbial species index in Figs. 4 and
5) rather than total microbial diversity best predict and explain the
vertical profile variation in soil multifunctionality in desert
ecosystems.