Discussion
Biogeographic Patterns of Microbial
Properties
We found significant biogeographic patterns of fungi, bacteria and their
balance in topsoil along latitude, climate (MAP and MAT), plant (NPP and
Croot), soil microclimate (SM and ST), and edaphic
factors (SOC, TN, C:N ratio, soil pH, soil texture, and bulk density)
(Fig. S2-6 ). Some of those have been reported in previous
studies (Fierer et al. 2009; Waring et al. 2013; Chenet al. 2016; Bahram et al. 2018). For example, Bahramet al. (2018) also reported the inverse unimodal trend of BBC and
positive linear trend of F:B ratio along latitude and significant
positive linear trend of F:B ratio along MAP and MAT, Fierer et
al. (2009) reported significant controls of plant NPP and microbial
biomass, Waring et al. (2013) showed that F:B ratio decreased
with low level C:N ratio, and increased at high C:N ratio, and de Vrieset al. (2012) found that finely textured soils tend to have
higher fungal and bacterial biomass.
In addition, we did find different results compared with previous
studies. Specifically, in contrast to the inverse unimodal trend of FBC
along latitude, Bahram et al. (2018) found the significant
positive linear relationships between FBC and latitude. Also, we
observed the inverse unimodal relationship between F:B ratio and soil
pH, with lowest F:B ratio at soil pH of 6.3, while Chen et al.(2015) reported a significant positive relationship between F:B ratio
and soil pH in Mongolian Plateau and Eskelinen et al. (2009)
found a negative relationship between F:B ratio and soil pH in the
alpine tundra of northern Europe. These discrepancies may result from
two reasons. First, the difference in sample size may lead to the
variations in the relationships obtained among studies. Dataset in
Bahram et al. (2018) was built based on the globally selective
sampling plots (145 topsoil samples), while the dataset of this study is
a comprehensive meta-analysis dataset with 1323 data points
(Fig. 1 ). Second, the difference in spatial scales of research
is responsible for the plausible distinction. Chen et al. (2015)
covered soil pH>6.5, while Eskelinen et al. (2009)
contained sampling sites of soil pH ranging from 4.7 to 7.0. Merging the
negative and positive relationships between F:B ratio and soil pH found
by Chen et al. (2015) and Eskelinen et al. (2009) reach
the similar results as reported in this study.
FBC and BBC were largely distinct among biomes, but we observed
generally similar patterns for FBC and BBC among biomes (Table
1 ). Consistent with our results, Xu et al. (2013) also found the
highest soil microbial biomass in tundra among biomes, and soil
microbial biomass was significantly higher in boreal forests than that
in temperate forests and tropical/subtropical forests. Both Fiereret al. (2009) and Xu et al. (2013) reported lowest soil
microbial biomass in deserts, the low SOC concentration may result in
low FBC and BBC in deserts (Fig. S6 ). However, this study
generated slightly different results from previous studies. Among forest
biomes, Fierer et al. (2009) reported the higher soil microbial
biomass in temperate and tropical forests than that in boreal forests,
which exhibited opposite patterns with this study. In addition, soil
microbial biomass in temperate forests was significantly higher than
that in tropical/subtropical forests reported by Xu et al.(2013), while both FBC and BBC were significantly higher in
tropical/subtropical forests than that in temperate forests in this
study (Table 1 ). The seasonality of FBC and BBC could be a
source for the inconsistency. Microbial biomass showed strong seasonal
dynamics, samples taken in growing and non-growing seasons are expected
to have distinct microbial biomass concentrations (Lipson et al.2002).
Our results also showed that F:B ratio was distinct among biomes, with
the smallest F:B ratio in savanna and the highest in tundra
(Table 1 ). Similar to our findings, Bahram et al. (2018)
found significantly higher F:B ratio in boreal-arctic biomes (e.g.,
tundra and boreal forests) and temperate biomes (e.g., temperate forests
and grassland) than that in tropical biomes (e.g., savanna and
tropical/subtropical forests). Additionally, we found significantly
higher F:B ratio in grasslands than that in pastures, which is
consistent with de Vries et al. (2012), suggesting that
management practices enhance the dominance of bacteria.
We estimated FBC and BBC storage in topsoil as 12.56 Pg C and 4.34 Pg C,
respectively (Table 2 ). This result is consistent with overall
terrestrial biomass estimates of FBC and BBC storage of 12 Pg C and 7 Pg
C, respectively, in Bar-On et al. (2018). Differences in methods
probably account for most of the differences between the results
reported in these studies. Fungi are more sensitive to anoxic
conditions, and bacteria and archaea are important components in deep
soils such as subsurface environments (Bar-On et al. 2018). It is
likely that the differences in the soil depths between this study (0-30
cm) and Bar-On et al. (2018) (entire soil profile) might underpin
the discrepancy in estimated global budget of BBC.
Mechanisms for the Microbial
Biogeography
We demonstrated that different factors underpin the biogeographic
patterns of FBC, BBC, and F:B ratio in topsoil. These patterns can be
related to the different nutrient stoichiometry of the microbial groups
and their ecological tolerance. First, saprotrophic fungi have more
efficient enzymatic machinery than bacteria to obtain C from complex
organic material with high C:N ratio (de Vries et al. 2012; Chenet al. 2015). Second, highly carbon-rich soils usually display
low soil pH that is relatively more difficult to cope with for bacteria
compared with fungi (Eskelinen et al. 2009; Rousk et al.2010). These two interacting mechanisms may favor fungi-dominated
ecosystem C and nutrient cycling in tundra and boreal forest ecosystems
that exhibits particularly high F:B ratio. Third, fungi were more
adapted to low‐temperature conditions and more heat-tolerant than
bacteria (Pietikäinen et al. 2005). Meanwhile, fungi dominate
early stages of litter decomposition that is more common in
high-latitude than low-latitude (Steidinger et al. 2019). In
concordance, we also found significantly higher F:B ratio in boreal
forest and temperate forest than that in tropical/subtropical forest
(Table 1 ). Grasslands feature significantly higher F:B ratio
than pasture, indicating that management practices might enhance the
dominance of bacteria as shown by de Vries et al. (2012). Natural
wetland has F:B ratio comparable to unvegetated ground, desert, and
shrub, which might be relevant to the low availability of oxygen that
inhibits the growth of fungi and most soil bacteria (Lin et al.2012).
Edaphic properties rather than climatic variables determine much of the
variation in FBC and BBC globally (Fig. 2a-b), which is consistent with
Chen et al. (2016). This result indicates that FBC and BBC
variations are driven by soil pH, SOC, nutrients (e.g., nitrogen and
phosphorus), and soil texture (clay, silt, and sand) that control the
availability of C energy, nutrients and oxygen – all determinants of
fungal and bacterial growth (Brockett et al. 2012; de Vrieset al. 2012). Edaphic properties determine the nutrient and water
availabilities, and even shelter from predation (Chapin et al.2011). Specifically, soil pH strongly influences abiotic factors, such
as C availability (Andersson et al. 2000), nutrient availability
(Pietri & Brookes 2008), and the solubility of metals (Firestoneet al. 1983).
In striking contrast to bacterial and fungal biomass, our results
suggest that climate is the most important factor governing the F:B
ratio (Fig. 2c ). Climate has a principal effect on soil
properties and vegetation activities that control soil microbial
composition (Classen et al. 2015; Bahram et al. 2018).
Although the tight association between plant community and soil
microbial community structure has been reported (Bardgett et al.1998), we observed negligible effects of plant productivity (NPP and
Croot) on topsoil microbial community structure. It is
likely due to two reasons: 1) we used plant productivity to represent
the effect of plants in this study, while growing evidence points to
plant functional traits as drivers of soil biological processes at a
range of spatial scales (Bardgett & Wardle 2010); 2) vegetation
distribution and functional traits are largely determined by climate
(Aerts 1997), the inclusion of both climate and plants into the model
may result in the dominant role of climate in deciding soil microbial
community.
Implications for Global Carbon
Cycle
We estimated the ratio of FBC and BBC to SOC as 1.8% and 0.6%,
respectively, which agrees with the findings that microbial biomass C
(MBC) generally comprises 0.5-5% of SOC (Insam 1990). Soil microbes,
the living fraction of soil organic matter, have a much faster turnover
rate than soil organic carbon (Xu et al. 2017); meanwhile, the
BBC bas faster turnover rate than FBC (Bååth 1998; Rousk & Bååth
2007b). The changes in the MBC:SOC ratio indicates the integrated
effects of soil organic matter input, soil microbial C use and C losses,
and mineral protection of SOC; therefore, MBC:SOC ratio has been
suggested as a useful and meaningful indicator of changes in soil
organic matter status (Powlson & Jenkinson 1981; Sparling 1992).
However, MBC:SOC ratio was not constant. In addition to the natural
variations due to the seasonal dynamics of MBC, MBC:SOC ratio is
affected by climate, and land use change, soil texture, soil mineralogy,
and SOC (Sparling 1992). For example, managed ecosystems such as
croplands and pastures tend to have broad MBC:SOC ratio and high MBC,
the increasing MBC will enhance the release of carbon dioxide from soil
to atmosphere due to the facilitated microbial breakdown of soil organic
matter. The acceleration of such processes by soil microbes could
significantly exacerbate the soil C cycle; therefore, soil microbial
community change is expected to have profound influence on global C
cycle.
Limitations and Prospects
A few limitations need to be recognized when interpreting the results.
First, we assumed that all samples were taken from surface soil
representing 0-30 cm soil profile; while the sampling depth varies
between 0 and 30 cm in this study, and 76% of soil samples were taken
for topsoil of 0-15 cm. Considering the vertical distribution of
microbial biomass C (Xu et al. 2013), this bias might lead to a
trivial overestimate to the summarized BBC and FBC in our estimates.
Second, the disproportion of the number of data points from each biome
to its land area might lead to bias in spatial extrapolation. For
example, the data points from forest, grassland, and cropland contribute
approximately 80% of the dataset, while the land area of these biomes
is approximately 50% of the global land area (Table 2 ). Third,
the sampling date might be another reason for uncertainty; the data
points were taken from various seasons and we assume the average across
season represent the annual mean. In this aspect, future studies on
seasonal variation of soil FBC and BBC would bring in improvements to
our knowledge. Fourth, actinobacteria was categorized as bacteria in a
portion of studies but not in others (Andersen et al. 2010;
Royer-Tardif et al. 2010). This difference in classification may
introduce minor uncertainties in simulating the relationships between
FBC and BBC.