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Glob Change Biol. 2023;00:1–17. wileyonlinelibrary.com/journal/gcb
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1© 2023 John Wiley & Sons Ltd.
Received: 8 May 2022
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Revised: 13 Januar y 2023
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Accepted: 19 Januar y 2023
DOI : 10.1111/gcb .16613
RESEARCH ARTICLE
Microbial necromass in cropland soils: A global meta- analysis
of management effects
Ranran Zhou1 | Yuan Liu2 | Jennifer A. J. Dungait3,4 | Amit Kumar5 |
Jinsong Wang6 | Lisa K. Tiemann2 | Fusuo Zhang1 | Yakov Kuzyakov7 |
Jing Tian1
Ranra n Zhou and Yuan Liu con tribute equa lly to thi s work.
1Key Laborator y of Plant- Soil Interact ions,
Ministry of Education, College of
Resources and Environmental Sciences ,
Nationa l Academy of Agriculture Green
Develop ment, C hina Agricultural
University, Beijing, P.R. Chi na
2Depar tment of Plant, S oil and Mi crobial
Science s, Michigan State Univer sity, Eas t
Lansing, Michigan, USA
3Carbo n Manage ment Centre, SRU C-
Scotlan d's Rural College, Edinbu rgh, UK
4Depar tment of Geography, College
of Life and Environm ental S cience s,
University of E xeter, Exete r, UK
5Depar tment of Biolog y, College of
Science , United A rab Emirates University,
Al Ain, UAE
6Key Laborator y of Ecosys tem Net work
Obser vation and Modeling, I nstitute
of Geogr aphic Sciences and Natural
Resources Research, Chinese Ac ademy of
Science s, Beijing, China
7Depar tment of Soil Science of Temper ate
Ecosystems, Uni versit y of Göt tingen ,
Göttingen, Germany
Correspondence
Jing Tian and Fusuo Zhang, Key
Labor atory of Plant- Soil Interact ions,
Ministry of Education, College of
Resources and Environmental Sciences ,
Nationa l Academy of Agriculture Green
Develop ment, C hina Agricultural
University, 100193 Beijing, P.R. China.
Email: tianj@igsnrr.ac.cn; zhangfs@cau.
edu.cn
Funding information
Nationa l Key R&D Prog ram of Chi na,
Grant /Award Number: 2022YFD1901300 ;
Nationa l Natural Scien ce Foundation of
China, G rant/Award Numbe r: 32071629
Abstract
Microbial necromass is a large and persistent component of soil organic carbon (SOC),
especially under croplands. The effects of cropland management on microbial nec-
romass accumulation and its contribution to SOC have been measured in individual
studies but have not yet been summarized on the global scale. We conducted a meta-
analysis of 481- paired measurements from cropland soils to examine the management
effects on microbial necromass and identify the optimal conditions for its accumula-
tion. Nitrogen fertilization increased total microbial necromass C by 12%, cover crops
by 14%, no or reduced tillage (NT/RT) by 20%, manure by 21%, and straw amendment
by 21%. Microbial necromass accumulation was independent of biochar addition. NT/
RT and straw amendment increased fungal necromass and its contribution to SOC
more than bacterial necromass. Manure increased bacterial necromass higher than
fungal, leading to decreased ratio of fungal- to- bacterial necromass. Greater microbial
necromass increases after straw amendments were common under semi- arid and in
cool climates in soils with pH <8, and were proportional to the amount of straw input.
In contrast, NT/RT increased microbial necromass mainly under warm and humid cli-
mates. Manure application increased microbial necromass irrespective of soil proper-
ties and climate. Management effects were especially strong when applied during
medium (3– 10 years) to long (10+ years) periods to soils with larger initial SOC con-
tents, but were absent in sandy soils. Close positive links between microbial biomass,
necromass and SOC indicate the important role of stabilized microbial products for
C accrual. Microbial necromass contribution to SOC increment (accumulation effi-
ciency) under NT/RT, cover crops, manure and straw amendment ranged from 45%
to 52%, which was 9%– 16% larger than under N fertilization. In summary, long- term
cropland management increases SOC by enhancing microbial necromass accumula-
tion, and optimizing microbial necromass accumulation and its contribution to SOC
sequestration requires site- specific management.
KEYWORDS
amino sugars, cropland management, land use, meta- analysis, microbial necromass, soil carbon
sequestration, soil organic mat ter
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ZHOU et al.
1 | INTRODUC TION
Soils contain the largest pool of terrestrial carbon (C), and small
changes in global soil C content have a strong impact on atmospheric
CO2 and climate change (Davidson & Janssens, 2006; Schmidt
et al., 2011). Loss of soil organic carbon (SOC) is regarded as a key
indicator of soil degradation, and monitoring SOC is recommended
to validate progress towards several UN Sustainable Development
Goals (Toth et al., 2018). Although agriculture covers 38% of the
Earth's land surface, large areas of agricultural land suffer from
medium to strong degradation (Nachtergaele et al., 2011). On the
global scale, agricultural soils have lost one- half to two- thirds of
total SOC compared with natural or uncultivated soils (Lal, 2004).
The estimated global soil C accrual potential varies between 0.4 4
and 0.68 Gt C year−1 through cropland management including fer-
tilization, no- till, and cover crops (Lessmann et al., 2022). Therefore,
there is a large potential for SOC accrual in croplands through prac-
tical management practices, which is particularly important to im-
prove soil health, achieve food security, and mitigate climate change
(Lessmann et al., 2022; Olsson et al., 2019).
Soil microbial community plays a key role in delivering ecosystem
functions, including C sequestration, through the formation of sta-
ble SOC pools via their necromass (Gougoulias et al., 2014). The soil
“microbial carbon pump” concept emphasizes the important role of
microbial anabolism in organic matter formation and turnover (Liang
et al., 2017; Zhu et al., 2020). Microbial residues (i.e., necromass) can
contribute more than 50% SOC in croplands (Liang et al., 2019; Wang
et al., 2021) and constitutes a persistent SOC pool that is protected
either physically within aggregates or chemically via association with
clay minerals and iron (hydr) oxides (Bernard et al., 2022; Cotrufo &
Lavallee, 2022; Kan et al., 2022; Sokol et al., 2022). Therefore, quan-
tifying microbial necromass and it s response to management can in-
crease the persistent SOC pool contributing to C sequestration as a
key ecosystem function of agricultural soils.
Growing interest in the ef fect s of cropland management on
microbial necromass dynamics is increasing (Hu, Huang, Zhou,
Liu, et al., 2022; Rui et al., 2022). Nitrogen (N) fertilization accel-
erates SOC dynamics by modifying microbial turnover and necro-
mass accumulation (Ni et al., 2021). Positive (Hu, Huang, Zhou, Liu,
et al., 2022), neutral (Chen et al., 2018), and negative ef fects (Liang
& Balser, 2012) of N fertilization on microbial necromass have been
observed. Long- term straw or manure applications increased mi-
crobial necromass accumulation (Xia et al., 2021; Ye et al., 2019).
However, the change direction and magnitudes varied substantially
among different field experiments. For example, manure amend-
ment increased fungal necromass after 27 years in upland Ultisols
(Ye et al., 20 19), but induced a higher increase of bacterial relative
to fungal necromass at a 31- year paddy soil trial (Xia et al., 2021).
Climate- smart agricultural practices, such as no tillage or reduced
tillage, cover crops and biochar application also increased SOC se-
questration directly or indirectly through their effects on plant
productivity and microbial necromass (Bai et al., 2019; Murugan
et al., 2013). Cover crops (especially legumes; Li et al., 2019; Liang
et al., 20 17; Liu et al., 2019) provide diverse substrates with low
C/N ratio that accelerate microbial anabolism, thereby may con-
tinuously form microbial necromass and stable SOC by entombing
effects. However, cover crops (winter rye) do not increase microbial
necromass contributions to SOC in another continuous corn silage
field experiment (West et al., 2020). Our limited understanding of
the factors driving the variable responses of microbial necromass to
cropland management reported in above studies across the world
currently restricts the development of appropriate management
strategies to optimize the potential of microbial necromass to con-
tribute to global C sequestration.
Soil microbial necromass accumulation is determined by the bal-
ance of necromass production, recycling rates and efficiency, and
stabilization processes (Buckeridge et al., 2022; Wang et al., 2022).
Inconsistency in the reported effects of cropland management on
soil microbial necromass accumulation may be ascribed to the com-
bined effects of management practices and site- specific edaphic
and climatic factors (Angst et al., 2021; Arndt et al., 2022; Liang &
Zhu, 2021). For instance, soil texture is one of the governing factors
regulating SOC stability (Ni et al., 2022) and large contents of silt- and
clay- sized minerals provide more favorable conditions for microbial
necromass stabilization (Angst et al., 2021; Wang et al., 2022). Soil
pH is another fac tors strongly affecting microbial necromass con-
tributions to SOC (Jones et al., 2019). Selec tion pressures of soil pH
on the microbial community are evident, in which bacteria are less
environmentally filtered than fungi (Chen et al., 2019; Finlay, 2002)
resulting in their divergent contributions to microbial necromass
accumulation in acidic and alkaline soils (Chen et al., 2018; Liang &
Balser, 2012). Climate can also affect the microbial necromass accu-
mulation in soil. Microbial necromass decreased sharply where arid-
ity indexes were greater than 0.77 and soil C- to- N ratios were above
9.6 (Hao et al., 2021). A significant increase in the amounts of mi-
crobial necromass was observed when the temperature was raised
approximately 1.3– 2.2°C in a 9- year field trial (Ma et al., 2022). Using
the combined outcomes of these experiments under various crop-
land management, edaphic and climatic conditions could help to
identify the optimal scenarios for microbial necromass accumulation,
and thereby encourage stable SOC formation and C sequestration.
The effects of cropland management on microbial necromass
accumulation and thus, contributing to SOC has been evaluated
in many individual studies, but not yet summarized at the global
scale. Microbial necromass usually is measured by quantifying
amino sugars, which are major components of microbial cell walls
and therefore, is used as biomarkers of bacterial and fungal nec-
romass in soils (Zhang & Amelung, 1996). Therefore, we collec ted
amino sugars data published in report s of experiments in global
cropland soils with paired management practices (N and manure
fertilization, straw and biochar amendment, NT/RT, cover crops)
to reveal the factors governing microbial necromass accumula-
tion globally. This study aims to (i) characterize the response of
microbial necromass, its contribution for SOC and accumulation
efficiency (i.e., the increase in microbial necromass C per unit of
soil C) to cropland management, and (ii) identify and elucidate
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ZHOU et al.
environmental factors (e.g., climatic and edaphic conditions) af-
fecting microbial necromass accumulation depending on manage-
ment. We hypothesize that globally: (1) necromass accumulation
from increased bacterial or fungal abundance in relation to man-
agement is mediated by edaphic (e.g. soil pH and initial SOC level)
and climatic factors; (2) cropland management that increases mi-
crobial biomass also increases necromass accumulation; and (3) mi-
crobial necromass accumulation efficiency is especially increased
under cropland management that promote fungal necromass.
2 | MATERIALS AND METHODS
2.1 | Data collection
Data were collected using the Web of Science (WoS, h t t p: //
apps.webof knowl edge.com/) and China National Knowledge
Infrastructure (CNKI, https://www.cnki.net/) to search peer-
reviewed research article s pu blished pri or to August 2022 that re -
port ed the ef fec ts of cro pland man ag em ent pra ctices on microbial
necromass or amino sugars. We focused on the impact of experi-
ments that investigated the effect of common cropland manage-
ment practices on microbial necromass accumulation, including
N fer tilization (mineral N), manure application (pig manure, cat tle
manure, poultry manure, and farmyard manure, etc.), straw (maize
straw, wheat straw, rice straw, peanut and radish residues, etc.)
and biocha r am endme nts, NT/RT, and cove r cr ops. Other manage-
ment practices were not included due to the lack of studies with
quantitative data. Various keyword combinations were used for
searching, including (management OR biochar OR straw return OR
crop straw OR crop residues OR manure OR nitrogen addition OR
nitrogen fertilization OR nitrogen enrichment OR nitrogen deposi-
tion OR tillage OR cover crops) AND (microbial/fungal/bacterial
necromass/residues OR amino sugars OR glucosamine OR mu-
ramic acid).
To reduce publication bias, articles were screened to determine
whether the study met the following criteria. First, the content of
fungal and bacterial necromass coul d be directly retrieved from art i-
cles, or glucosamine (GluN) and muramic acid (MurA) were reported
to calculate microbial necromass based on empirical conversion fac-
tors (Zhu et al., 2020). Those containing only total necromass content
without its partitioning into fungal and bacterial necromass were
excluded. Second, the experiment was implemented with a pair-
wise design, including control and treatment. We considered con-
ventional tillage as the control for NT and RT. Likewise, “no N”, “no
manure”, “no straw”, “no biochar”, and “no cover crops” were treated
as control conditions relative to N, manure, straw, biochar, and cover
crops, respectively (Bai et al., 2019). Third, we only collected data
from agricultural ecosystems, and excluded studies in grassland and
forest ecosystems. Incubation studies using field soil were included
in our database. Fourth, when the same result s were presented in
different publications of the same research group, these data were
only included once. Finally, only the means, standard deviation (SD),
and replication number of selected variables could be obtained from
the ar ticles. If only standard error (SE) was presented for amino sug-
ars and soil variables in a study, SD was calculated as SE*
√n
.
Additional information was also collected including experiment
location (e.g., longitude, latitude, and altitude), climatic conditions
(e.g., mean annual air temperature [MAT], mean annual precipita-
tion [MAP]), soil properties (e.g., initial soil pH, SOC, total N [TN],
C/N, microbial biomass C and N [MBC; MBN], sand, silt and clay
content), and experimental details (e.g., resource input type and
application rate, and experimental type and duration). Data pre-
sented only in figures within the ar ticles were extracted by the free
software GETDATA GRAPH DIGITIZER (h t t p : / / g e t d a t a - g r a p h - d i g i t
izer.com). Data presented in supplementar y materials accompany-
ing the article or other articles by the same research group were
also included. The Aridity index is calculated as the ratio of mean
annual precipitation and mean annual evapotranspiration (MAP/
MAE) (Zomer et al., 2007), an d wa s ob taine d fr om the Gl ob al Aridit y
and PET Database (https://cgiar csi.commu nity/data/globa l- aridi ty-
and- pet- database). Since experiments in hype r arid and arid climati c
conditions were rare in our dataset, we grouped data into two cate-
gories according to the ar idity index, either semi- ar id (≤0.65; inc lud-
ing semi- a ri d and dry sub- humid) or hum id (>0.65) (Hao et al., 2021).
Data were also grouped into two climate zones by study site MAT,
cool (temperate and Mediterranean climates) and warm (subtropi-
cal and tropical climates; Bai et al., 2019). Data were also grouped
by initial SOC content into poor/low (<12 g C kg−1) or moderate/
rich (>12 g C kg−1 ) categories, and by the initial soil pH into acidic
(≤6), neutral (6– 8), or alkaline (>8) groups (Du et al., 2020). Soil tex-
ture was classified based on the USDA soil texture classification
system (USDA, 2017). For field experiments, we grouped data by
experimental duration including short- term (≤3 years), medium- term
(3– 10 years), and long- term (>10 years) (Du et al., 2020). The N re-
source input rate presented as g kg−1 soil in laboratory incubations
was conver ted to kg ha−1 year after correcting for soil bulk density.
Implementing these criteria, 61 published articles were selected
(Appendix S1). We collected a total of 481 paired observations
that reported the effects of management on microbial necromass
accumulation for fur ther analyses (Dataset S1). Most studies were
concentrated in thre e areas: East Asia, North Amer ic a, and Western
Europe (Figure 1).
2.2 | Microbial necromass calculation
Fungal and bacterial necromass were calculated from GluN and
MurA content s. MurA exclusively originates from bacteria, whereas
GluN occurs in either fungal or bacterial cell walls. Assuming GluN
and MurA occur on average at a 2:1 molar ratio in bacterial cells, fun-
gal GluN can be calculated (Joergensen, 2018), the ba c te ria l an d fun -
gal necromass C were calculated using the following formula based
on previously established stoichiometric conversion factors:
Bacterial necromass C =MurA ×45,
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4
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ZHOU et al.
where 45 is the conversion factor from MurA to bacterial necromass
C; 9 is the conversion factor from GluN to fungal necromass C; and,
251.23 and 179.17 are the molecular weights of MurA and GluN, re-
spectively (Zhu et al., 2020).
The total microbial necromass was estimated as the sum of fun-
gal and bacterial necromass. The ratios of fungal- to- bacterial nec-
romass were used to evaluate the relative accumulation of fungal
and bac terial necromass. The corresponding SOC contents were ex-
tracted from the studies to evaluate the contributions of microbial-
derived necromass to SOC by dividing the microbial necromass by
total SOC , as follows:
Contributions of microbial- derived C to SOC depending on treat-
ments (or management practices) relative to control was calculated
by dividing the treatment induced change in microbial necromass C
(ΔMNC) by the treatment induced change in SOC (ΔSOC) as follow:
where the subscript T represented treatment groups and Cont rep-
resented control groups. This metric, which represents the change
in microbial necromass C per unit change in SOC depending on man-
agement, reflecting actual contribution of microbial necromass to the
increment of SOC, can be considered a quantitative representation of
necromass accumulation efficiency.
2.3 | Meta- analysis
A random- effects model was used to evaluate the effects of crop-
land management on microbial necromass and its contribution to
SOC (Hedges et al., 1999). The natural log of the response ratio (RR)
was calculated as the ef fect size, representing the management
effects:
Fungal necromass C
=
(
GluN
179.17 −2×MurA
251.23
)
×179.17 ×
9,
Contribution of necromass C to SOC
=
Microbial necromass C
SOC
Δ
MNC
Δ
SOC =
Microbial necromass C
T
−Microbial necromass C
Cont
SOC
T−
SOC
Cont
,
RR
=ln
XT
X
Cont
=ln
XT
−ln
XCont
,
FIGURE 1 Distribution of experiment al sites used in the meta- analysis of microbial necromass accumulation. The distribution of
experiments on cropland management (a). Numbers in brackets are the number of samples under the management practices. NT/RT: no-
tillage or reduced- tillage. The distribution of the sites according to ecosystem types (b).
7HPSHUDWXUH
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7H PSHUDWHVHDVRQDOIRUHVW
7H PSHUDWHUDLQIRUHVW
7URSLFDOUDLQIRUHVW
7URSLFDOVHDVRQDOIRUHVWVDYDQQD
6XEWURSLFDOGHVHUW
7H PSHUDWHJUDVVODQGGHVHUW
:RRGODQGVKUXEODQG
&
±
(a)
(b)
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5
ZHOU et al.
where XT and XCont represent the mean of the treatment under man-
agement practice and control groups for variable X, respectively. The
variance of RR was calculated as:
where SDT and SDCont represent the standard deviations of the treat-
ment and control, respectively, and nT and nCont represent the sample
si ze of th e trea tme nt and cont r ol, resp e c tiv ely. Th e n, to ass ign a grea ter
weight to the ent r y with lo wer var ia nce to im prove the precis io n of ou r
analysis, the weighted ef fect size was calculated as:
where
wi
is the weighting factor of the ith experiment in the grou p, an d
was calculated as follows:
To identify significant differences in the effect sizes, the stan-
dard error of RR++ and 95% confidence intervals (CI) was calculated
as follows:
If the 95% confidence intervals did not overlap with zero, the
effects of management on variables were considered significant
(Hedges et al., 1999). We then calculated the percent change depend-
ing on management practices using the equation:
(
e
RR
++ −1
)
×100
%
for all variables, including total, bacterial and fungal necromass C;
contributions of total, bacterial, and fungal necromass C to SOC;
ratio of fungal- to- bacterial necromass C; SOC, TN, and MBC and
MBN.
2.4 | Statistical analysis
The meta- analysis was conducted in R software (version 4.1.1, R
Core Team, 2019) using the “rma.va” function in “metafor” package
version 3.0– 2 (Viechtbauer, 2010). Egger's regression test and Fail-
Safe analysis with Rosenberg method were used to test publication
bias in the studies (Egger et al., 1997; Rosenberg, 20 05). If p values
were >.05 in Egger's regression test, or coefficients >5 N + 10 in the
Fail- Safe analysis (N is the sampling size in this study), then the ef-
fect sizes of variables are considered statistically significant, and the
observed pattern indic ated no sign of publication bias (Table S1).
Linear regressions were used to estimate whether RRs of
necromass C correspond significantly with manure, straw, and N
input levels. The links between living microbial biomass, necro-
mass- C and SOC depending on management also were analyzed
by linear regressions. Prediction of the response of microbial
necromass C to management by environmental variables (e.g.,
MAT, MAP, aridity index, SOC content, TN, soil C: N, soil pH,
and clay content) was implemented using Random Forest mod-
els. The analysis was performed using the “randomForest” pack-
age and was evaluated by using the “A3” package in R 4.1.1 (Hao
et al., 2021). We analyzed the significance of each predictor's
importance to total/bacterial/fungal necromass C in N, manure,
straw, and NT/RT practices, but not cover crops due to the lack
of quantitative data.
Structural equation modeling (SEM) analysis was performed to
test the hypothesized path model inferring management influence
microbial necromass accumulation. The most parsimonious model
was identified by the chi- squared test (χ2; the model has a good
fit when 0 ≤ χ2/df ≤2 and .05 < p ≤ 1.0 0), high Comparative Fit Index
(CFI ≥0.90), and low Root Mean Square Error of Approximation index
(RMSEA ≤0.1). The SEM analysis was conducted with AMOS 21.0
(spss, IBM).
3 | RESULTS
3.1 | Effects of cropland management on microbial
necromass
All investigated management practices except biochar addition
increased total microbial necromass C in cropland by 12%– 21%
(Figure 2a). Straw and manure amendment increased total micro-
bial necromass C by 21% (both p < .0 01), followed by NT/RT (20%,
p < .001), cover crops (14%, p < .05), and N fertilization (12%, p < .05,
Figure 2a).
Bacterial and fungal necromass C were increased by 11%– 29%
and 12%– 26%, respectively (both p < .05, Figure 2b,c), whereas the
effect size on bacterial and fungal necromass C was dependent
on management. Bacterial necromass C was greatest with manure
application (29%, Figure 2b), while fungal necromass C increased
the most under straw application (26%, Figure 2c). The ratio of
fungal- to- bacterial necromass C decreased with manure application
(p < .05, Figure 2d). The effects of cropland management practices
on muramic acid and glucosamine followed similar patterns with the
response of bacterial and fungal necromass C to management prac-
tices, respectively (Figure S1).
Only straw amendment and NT/RT practices increased the
contributions of total microbial necromass C to SOC (both p < .05,
Figure 2e), or more specifically, increased the contribution of fun-
gal but not bacterial necromass C to SOC (both p < .01, Figure 2f, g).
Manure increased the contribution of bacterial necromass to SOC,
but the contribution of total microbial necromass C to SOC remained
unaffected (Figure 2e,f). Biochar application decreased the ratio of
total necromass C- to- SOC while increasing SOC content (p < .001,
Figure 2e and Figure S2a).
v
=SD
2
T
nTX2
T
+SD
2
Cont
n
Cont
X2
Cont
,
RR
++ =Σ
(
wi×RRi
)
Σ
w
i
,
w
i=
1
v
i
.
s
RR
++
=
1∕Σwi
,
95
%CI =RR
++
±1.96 ×s
(
RR
++).
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6
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ZHOU et al.
3.2 | Response of microbial necromass
accumulation to management depending on
climate and soil properties
The responses of microbial necromass C to management de-
pended on climatic conditions (Figure 3 and Figure S3). N fertili-
zation and straw amendment increased total microbial necromass
C by 12% and 24% in semi- arid site (p < .01, Figure 3a), and by
12% and 22% in cool climates (p < .01, Figure 3e), respectively.
These effects were similar for bacterial and fungal necromass C
(Figure 3b,c,f,g). In contrast, NT/RT and cover crops increased
total microbial necromass C in humid (p < .05, Figure 3a) and warm
areas (p < .05, Figure 3e). Manure application increased microbial
necromass C irrespective of climate and increased total microbial
necromass C by 25% in semi- arid (Figure 3a) and 28% in humid cli-
mates (Figure 3e), respectively. Manure- induced total necromass
C ac cum ula te d in coo l and wa rm cli ma tes , espe cia lly in warm (42 % ,
p < .001, Figure 3 e - g ).
The management effects on microbial necromass C accumu-
lation were influenced by soil properties (Figure 4 and Figure S3).
Random Forest analysis showed that initial SOC content and soil
pH were important factors modif ying the management effects
(Figure S3). Manure and straw amendment increased total mi-
crobial necromass C when initial SOC content was moderate
or high (SOC >12 g kg−1, both p < .001), while the effects were
weaker when initial SOC content was low (SOC <12 g kg−1 , p < .05,
Figure 4a). Furthermore, the ratio of fungal- to- bacterial necro-
mass C decreased after manure application when initial SOC con-
tent was large (p < .01; Figure 4d). Soil pH was the most impor tant
factor determining microbial necromass C accumulation after N
fertilization (Figure S3). The N fer tilization effect was only signifi-
cant in alkaline soils, but not in acid and neutral soils (Figure 4e,f).
In contrast, straw amendment induced microbial necromass accu-
mulation in soils with pH <8 (both p < .01). Straw amendment in
neutral soils also increased the contribution of microbial necro-
mass C to SOC (p < .0 01, Figure S 5 d – f ). Manure increased total mi-
crobial necromass C regardless of soil pH (p < .01) (Figure 4e). The
ratio of fungal- to- bacterial necromass C decreased with manure
application in neutral soils ( p < .05, Figure 4h).
The management effects were also depending on soil texture,
and were more pronounced mainly in loamy and clay soils (Figure 5).
The N fertilization effec ts on microbial necromass C increased with
soil clay content (p < .05, Figure 5a and Figure S7). Specifically, there
was no response to management in sandy soils (Figure 5).
FIGURE 2 Management ef fects on microbial necromass C (a– c), necromass contribution to soil organic C (e– g), and ratio of fungal-
derived to bacterial- derived necromass (d) in the global cropland ecosystems. All results are presented as effects size in percent of the
control soil (without respec tive amendment or practice). Error bars represent 95% confidence intervals. TNC, tot al necromass C; BNC,
bacterial necromass C; FNC , fungal necromass C; SOC , soil organic carbon; FNC/BNC, the ratio of fungal- derived to bacterial- derived
necromass C; NT/RT, no- tillage or reduced- tillage. The number in parentheses represents the number of obser vations. The closed and open
symbols indicate significant and non- significant effec ts, respectively.
(a) (b) (c) (d)
(e) (f) (g)
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|
7
ZHOU et al.
3.3 | Experimental conditions affecting microbial
necromass accumulation
The interactive effects of management and experiment duration af-
fected microbial necromass C accumulation (Figure 6). Significant
effects on microbial necromass accumulation were absent in short-
term (≤3 years) experiments except under manure application. The
effects of manure application on bacterial necromass were more
pronounced in long- term experiments (>10 years), and decreased the
ratio of fungal- to- bacterial necromass C (p < .0 01; Figure 6a,b,d). N
fertilization and straw amendment increased the total and bacterial
necromass in the medium- to long- term experiments (Figure 6a,b).
Fungal necromass C was increased by 27% after N fertilization in
long- term experiments, but was increased by 24% after straw
amendment in the short- term experiments (both p < .001, Figure 6c).
The amount of straw input increased proportionally total (R2 = .62,
p < .001), bacterial (R2 = .4 3, p < .001) and fungal necromass (R2 = .35,
p < .001, Figure S9). The microbial necromass response, however,
were independent on applied amounts of manure or N fertilizers.
3.4 | Contribution of microbial necromass C to
SOC sequestration depending on management
Regression and SEM analysis were used to link microbial traits (mi-
crobial biomass and necromass) with SOC sequestration depending
FIGURE 3 Management ef fects on microbial necromass C depending on climate (a– d: the climate zones were divided by aridity index;
e– h: the climate zones were divided by mean annual temperature). All results are presented as ef fect s size in percent of the control soil
(without respective amendment or practice). Error bars represent 95% confidence inter vals. TNC, total necromass C; BNC, bacterial
necromass C; FNC, fungal necromass C; FNC/BNC , the ratio of fungal- derived to bacterial- derived necromass C; NT/RT, no- tillage or
reduced- tillage. The number in parentheses represents the number of observations. The closed and open symbols indicate signific ant and
nonsignificant effects, respectively. Biochar and cover crops depending on aridity index and mean annual temperature, respectively, were
not included because the data were not grouped.
(a) (b) (c) (d)
(e) (f) (g) (h)
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8
|
ZHOU et al.
on management (Figures 7 and 8). The SEM provided the best fit of
the data and validate that management affected microbial biomass,
subsequently influenced the production of microbial necromass, and
further SOC accumulation by entombing effects (Figure 8). There
was corresponding direct positive effect of microbial biomass on
necromass accumulation (Figure 8). Regression analysis further
showed that the RR of total microbial necromass C increased as the
RR of MB C increased under N fertilization (R2 = .36 , p < .01), manure
(R2 = .23, p < .001), straw (R2 = .41, p < .001), and NT/RT (R2 = .42,
p < .001) treatments (Figure 7a). Furthermore, microbial necromass
exerted strong direct effect on SOC variance under management
(Figure 8), especially under NT/RT (Figure 7a).
To assess the magnitude of the relationship between microbial
necromass C accumulation and SOC accrual depending on man-
agement, we calculated the microbial necromass accumulation ef-
ficiency (estimated by the ratio of ΔMNC to ΔSOC). The necromass
accumulation efficiency was from 36% to 52% depending on man-
agement: NT/RT were the most efficient (52%), followed by cover
FIGURE 4 Management ef fects on microbial necromass C depending on soil properties, initial soil SOC content (a– d) and pH (e– h). All
results are presented as effects size in percent (%) of the control soil (without respective amendment or practice). SOC < 12 (g kg−1) indicates
the initial SOC content is low and SOC > 12 (g kg−1 ) indicates the initial SOC content is moderate or high. The soil pH was classified as acidic
(<6), neutral (6– 8), or alkaline (>8). Error bars represent 95% confidence intervals. TNC, total necromass C; BNC , bacterial necromass
C; FNC, fungal necromass C; SOC, soil organic carbon; FNC/BNC, the ratio of fungal- derived to bacterial- derived necromass C; NT/RT,
no- tillage or reduced- tillage. The number in parentheses represents the number of observations. The closed and open symbols indicate
significant and nonsignificant effect s, respectively.
(a) (b) (c) (d)
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|
9
ZHOU et al.
crops (48%), straw (47%), and manure application (45%), while N fer-
tilization had the smallest accumulation efficiency (36%, Figure 7b).
Fungal necromass C (23%– 45%) consistently contributed more
to SOC accru al than that bacterial necromass C (7%– 18%) in all man-
agement practices (Figures 7b and 8). The accumulation efficiency
of fungal necromass was about 6.4 times that of bacterial un der NT/
RT, followed by cover crops (2.9 times), straw and N fer tilization (1.8
time s), and manu re application (1.5 times, Figure 7b and Figure S10).
4 | DISCUSSION
4.1 | Cropland management affect microbial
necromass accumulation
As important precursors for SOC formation, microbial necromass is
crucial for long- term C sequestration and stabilization (Buckeridge
et al., 2022; Liang et al., 2 017). Microbial necromass increased with
all management practices (except for biochar) (Figure 2a). Overall,
N fertilization increased total microbial necromass C (Figure 2a), be-
cause N availability increased microbial CUE (Hu, Huang, Zhou, &
Kuzyakov, 2022) and further raised C retention in the soil microbial
biomas s. Manure provid es a ran ge of org anic co mpounds of various
availability, which supports microbial proliferation, leading to larger
microbial biomass (Figure S2c) and consequently an increased mi-
crobial necromass (Figure 2a) (observed as the positive relationship
between microbial necromass C and biomass C; Figure 7a). This in-
cludes manure- derived microorganisms and microbial residues (Jost
et al., 2011) that directly and indirectly augments microbial biomass
C and microbial necromass in soil as both are sources of amino sug-
ars and substrates for biosynthesis (Gillespie et al., 2013). Bacterial
necromass increases with manure addition to a lager extent than
fungal, thus leading to a decrease of ratio of fungal- to- bacterial
necromass (Figure 2b– d). High soil fertility and nutrient availability
favors bacteria over fungi (Thoms & Gleixner, 2013; Xia et al., 2021),
thu s increasing the bac te rial necromass and its con tributi on to SOC
(Figure 2b,f). By contrast, the high C/N ratios of straw (80– 100:1)
stimulates fungal growth, leading to more fungal necromass C pro-
duction (Figure 2c) as widely reported (e.g., Rousk & Bååth, 2007).
Conser vation tillage, for example, no tillage or reduced tillage
(NT/RT), decreases soil disturbance, facilit ates the formation of
macroaggregates and preserves fungal hyphae leading to fungal
necromass accumulation and increasing its contribution to SOC
(Figure 2a,g; Murugan et al., 2013; Yang et al., 2022). Regardless of
whether straw amendment or NT/RT was used, the proportions of
total necromass to SOC increased by enhancing fungal necromass
FIGURE 5 Management ef fects on microbial necromass C depending on soil texture. All results are presented as ef fect s size in percent
of the control soil (without respective amendment or practice). Error bars represent 95% confidence intervals. TNC, total necromass C; BNC,
bacterial necromass C; FNC , fungal necromass C; FNC/BNC, the ratio of fungal- derived to bacterial- derived necromass C; NT/RT, no- tillage
or reduced- tillage. The number in parentheses represents the number of observations. The closed and open symbols indicate significant and
nonsignificant effects, respectively.
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10
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ZHOU et al.
(Figure 2e,g). Th er efore, fungal ne cromass is preferenti al ly accumu-
lated during SOC sequestration by straw addition and reduced or
no- tillage. The supply of diverse microbial substrates through lit-
ter, root exudates and rhizodeposits under continuous veget ation
under cover crops (Li et al., 2019 ; Liu et al., 2019) as well as soil pro-
tection by the plant canopy that benefits the entire food web, sup-
ports increased soil microbial activity and/or growth (Baumhardt &
Blanco- Canqui, 2014) leading to intensified production of microbial
necromass (Figure 2).
Biochar incorporation increased microbial biomass C (Figure S2)
because its high surfaces and pores provided habitat for microor-
ganisms as well as increased water holding capacity and cation ex-
change capacity for nutrient accumulation (Pokharel et al., 2020)
but did not affect microbial necromass accumulation (Figure 2).
Biochar is intended to contribute to the stable SOC pool as a
chemically recalcitrant C with a very slow decomposition and has
a high C/N ratio (Wang et al., 2015). This can increase soil total
and organic C content but provides little bioavailable C (an im-
portant precursor for formation of microbial necromass via the
microbial C pump; Chagas et al., 2022; Liang et al., 2017), and,
consequently, biochar does not increase microbial necromass
(Figure 2). Additionally, as an organic material with high C/N ratio,
biochar may divert metabolic resources for additional enzyme pro-
duction to alleviate C and nutrient limitation, for example, N lim-
itation (Gao et al., 2019), leading to lower CUE and high energy
investment (Gunina & Kuzyakov, 2022; Malik et al., 2020; Spohn
et al., 2016) and thus low microbial necromass for matio n (ob served
here, Figure 2). Overall, except for biochar, all tested management
practices increase microbial biomass, and thus promotes the for-
mation and accumulation of necromass C.
4.2 | Climate and edaphic controls on microbial
necromass accumulation depending on management
The dynamic balance of microbial necromass depends on a variety
of factors, such as climate, quality and quantity of C input, and soil
proper ties (Luo et al., 2017).
4.2.1 | Climatic conditions
Climatic conditions (e.g., temperature and precipitation) are domi-
nant environment al factors that not only affect soil microbial com-
munity composition but also control microbial necromass recycling
and turnover, and therefore necromass accumulation (Donhauser
et al., 2021; Hao et al., 2021; Tian et al., 2021). Under N fertili-
zation, microbial necromass accumulation was increased in semi-
arid and cool environments, but not in humid and warm climates
(Figure 3). Generally, high temperature and moisture accelerates
soil organic matter (SOM) decomposition and aggravate N limita-
tion (Mason et al., 2022). N fer tilization may further trigger SOM
and microbial biomass decomposition because of the stimulating of
C- degrading enzyme activities (Allison et al., 2008), thus resulting
in lower necromass accumulation. Similarly, straw increased micro-
bial necromass accumulation under semi- arid conditions, whereas
FIGURE 6 Effects of experiment duration on microbial necromass C (a– c) and ratio of fungal- derived to bacterial- derived necromass (d).
All results are presented as effects size in percent of the control soil (without respective amendment or practice). Error bars represent 95%
confidence intervals. TNC, total necromass C; BNC, bacterial necromass C; FNC, fungal necromass C; FNC/BNC, the ratio of fungal- derived
to bacterial- derived necromass C; NT/RT, no- tillage or reduced- tillage. The numbers <3, 3– 10, >10 reflect the years of the experiments. The
number in parentheses represents the number of observations. The closed and open symbols indicate significant and nonsignificant effects,
respectively.
(a) (b) (c) (d)
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|
11
ZHOU et al.
total necromass was preserved under cold temperatures that re-
duce decomposition rates. In contrast, NT/RT and cover crops in-
creased total microbial necromass accumulation in humid and warm
climates. Microbial necromass accumulation was stimulated due
to plant litter input under high moisture availability that supports
increased microbial growth (Prommer et al., 2020). The formation
of soil aggregates is increased by fungal hyphae under humid con-
ditions that physically protec ts microbial necromass from decom-
position (Liu et al., 2014). However, manure application increased
microbial necromass accumulation irrespective of climatic condi-
tions (Figure 3), particularly through the accumulation of bacterial
necromass. Live and dead bacteria from the digestive tract form
a large proportion of dung biomass thereby directly increasing
the proportion of bacterial residues in soil (Dungait et al., 2005).
Due to differences in cell structure, physiological trait s, and inter-
species interactions, bacteria generally have lower sensitivity to
temperature or precipitation compared to fungi (He et al., 2017).
Therefore, this may lead to manure- induced effects independent
of climate. Overall, the meta- analysis indicates that N fertilization
and straw amendment increased microbial necromass accumulation
under semi- arid and cool climate s, while NT/RT and cove r cro ps are
more effec ti ve unde r humid rather than semi- arid climates . Manur e
FIGURE 7 Relations among the response ratio of total necromass C (TNC), the response ratio of MBC, and the response ratio of SOC
(a); Contribution of microbially- derived necromass C to soil organic C increment (
ΔMNC
ΔSOC
) depending on management (b). Only the regression
lines significant at least at p < .05 are presented in (a). TNC, total necromass C; BNC, bacterial necromass C; FNC, fungal necromass C; NT/
RT, no- tillage or reduced- tillage. The white points indicate medians and the black box indicate the 25th and 75th percentiles. The number
with % indicate means of the increase of necromass contribution to SOC increment. The number in parentheses represents the number of
observations for SOC increment.
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13652486, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.16613 by China Agricultural University, Wiley Online Library on [08/02/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
12
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ZHOU et al.
application increases microbial necromass accumulation irrespec-
tive of climate.
4.2.2 | Duration and C input rate of
management practices
All management practices except straw amendment increased mi-
crobial necromass accumulation with experimental duration, and the
largest response appeared after 10 years (i.e., long term experiment;
Figure 6), suggesting slow and progressive accumulation. Microbial
necromass accumulation generally increased with the straw input
rate (Figure S9). Cumulative straw C input over longer periods in-
creases the supply of organic materials to soil microorganisms (Liu
et al., 2014), thereby increasing microbial necromass and SOC se-
questration. In contrast, the necromass response was not associated
with manure application (Figure S9), sug gesting the ‘entombing’ ef-
fect of the microbial carbon pump, that is, the coupling of organic
compounds to their long- term stabilization was only active under
straw amendment (Liang et al., 2017; Liu et al., 2019). Microbial
necromass formation was compensated by accelerated SOC de com-
position through a priming effect or the recycling of the necromass
under manure application (Bernard et al., 2022). Similarly, N ap-
plication amount had no significant effect on microbial necromass
accumulation (Figure S9). Larger N amendment may increase C in-
puts by boosting crop yields and root growth; but higher N rates
may also decrease microbial growth due to soil acidification (Jones
et al., 2019) and faster microbial turnover (Wang et al., 2018). In par-
ticular, chronic N fertilization decreases fungal biomass and diversity
(Zhou et al., 2016).
4.2.3 | Initial soil properties (pH, SOC and texture)
Changes in the microbial necromass induced by management also
are affec ted by initial soil properties (Clayton et al., 2021). The
microbial necromass accumulation was more pronounced in soils
with larger initial SOC content s, especially for bacterial necromass
FIGURE 8 Meta- analysis results of the responses of necromass C to cropland management and model outcome of expected causal
relationships obtained through structural equation modeling. NT/RT, no- tillage or reduced- tillage; An upward red arrow indicates an
increase of contribution, a downward blue arrow indicates a decrease of contribution, and a short green line indicates no significant effects.
SOC increment (ΔSOC), SOC T– S O C Cont. Contribution of bacterial, fungal and other C sources are presented as pie diagram, bac terial C to SOC
increment (
ΔBNC
ΔSOC
),
BNC
T
−BNCCont
SOC
T
−SOC
Cont
; contribution of fungal C to SOC increment (
ΔFNC
ΔSOC
),
FNC
T
−FNC
Cont
SOCT
−SOC
Cont
. The other C sources (beside bacterial and fungal
necromass) include plant litter and organic fer tilizer residues. Fitting paths of c ausality obtained through structural equation modeling
(χ2 = 1.134, df = 1, p = .287, RMSEA = 0.028, CFI = 0.999, n = 174). Figures on the yellow arrows indicate standardized path coefficients and
asterisks mark their significance; ** < .01; *** < .001.
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|
13
ZHOU et al.
(Figure 4). When the SOC content is less than 1%, C sequestration
is inefficient because soil microorganisms maintain high respiratory
losses to acquire limiting nutrients (Clayton et al., 2021) decreas-
ing the growth for resource acquisition (Kumar & Pausch, 2022;
Malik et al., 2 019). Conversely, the turnover rate of living biomass
and the retention rate of microbial necromass may be higher in SOC-
rich soils. More fertile soil increases bacterial dominance, especially
under ruminant manure application (Walsh et al., 2012), leading to
higher bacterial necromass accumulation and low fungal- to- bacterial
necromass ratio (Figure 4d).
Soil type and texture controls the potential for microbial necro-
mass stabilization through organo- mineral complexes (Ni et al., 2022)
and aggregate size and stability (Ye et al., 2019). The re sponse of mi-
crobial necromass accumulation to management strongly depended
on texture and were absent in sandy soils (Figure 5). In the clay- rich
soils, larger content s of silt- and clay- sized mineral particles stabilize
microbial necromass C by physico- chemical protection, unlike sandy
soils (Angst et al., 2021; Wang et al., 2022). Greater microbial nec-
romass accumulation under manure, straw, NT/RT and cover crops
were found in loamy or clay loamy soils, rather than in clay soils,
which may be related to soil type- , climatic- , and soil management-
specific interactions. In general, the higher microbial CUE in the
higher clay content soil resulted in a more efficient litter utilization
and concurrently higher amounts of microbial necromass finally re-
tained in soil with less mineralization (Cotrufo et al., 2013).
Soil pH is a dominant factor controlling microbial community
functioning and the SOM decomposition (Malik et al., 2018). N
fertilization increased microbial necromass only in alkaline soils
(Figure S3 and Figure 4e). Lon g- ter m N fer tiliz at i on of cro pla nds gen -
erally leads to soil acidification, which reduces microbial abundance
and CUE (Jones et al., 2 019). Higher initial soil pH in calcareous soils
buffers the adverse effects of acidification (Guo et al., 2021), and al-
leviates acidification through liming, while the judicious use of N fer-
tilizers provides potential solutions to alleviate low pH. In contrast,
straw amendment increased microbial necromass in soils with pH <8
(Figure 4e). The contribution of fungal necromass to SOC peaked
at neutral soil pH (Figure S5), as a lower or higher pH reduces crop
residue decomposition thereby decreasing necromass formation
(Wang et al., 2017). In general, apart from climatic and management
controls, necromass accumulation also depends on initial SOC con-
tent, soil texture and pH. Consequently, site- specific management is
required to maximize necromass accumulation.
4.3 | Microbial necromass as the SOC source under
cropland management
Microbial necromass C was positively correlated with MBC and SOC
(Figures 7a and 8), which indicates the vital roles of microbial biomass
and turnover, and their necromass accumulation for C sequestration
(Ni et al., 2020). Previous studies reported that microbial necro-
mass accounted for 51% (Wang et al., 2021) or 56% of SOC (Liang
et al., 2019), which is similar to our analysis (52%, not displayed). We
further calculated the increase of microbial necromass C per unit
increase of SOC (i.e., microbial necromass accumulation efficiency)
to assess the differences between management effect s on microbial
necromass as key sources of SOC in global cropla nds . Microbial ne c-
romass C contributed around 50% of the SOC increment under NT/
RT, cover crops, straw, and manure management, which was greater
than that un de r N fe r ti liza ti on (Figures 7b and 8). SOC was increased
by 13%– 24% under these management practices (Figure S2a), sug-
gesting that microbial- derived C increased SOC by 7.0%– 12%. In
contrast, biochar application did not increase microbial necromass
(Figure 2) but caused the largest SOC content increment (up to 40%,
Figure S2a). This confirms that biochar will not be utilized by micro-
organisms, at least note within 3– 10 years of experiment durations
and the slow biochar decomposition led to poor necromass accumu-
lation efficiency.
The contribution of fungal and bacterial necromass to SOC ac-
crual depended on management (Figure 7), which may reflect differ-
ences in microbial community composition in response to practices
(Luo et al., 2021). Overall, fungi play a predominant role in stable SOC
(necromass) accrual. We found that fungal necromass accumulation
efficiency was 1.8 or 6.4 times greater than bacterial necromass ac-
cumulation efficiency under straw amendment and NT/RT (Figure 7
and Figure S10), corresponding to the larger fungal necromass con-
tent under these management types (Figure 2). Management prac-
tices that encourage the proliferation of fungi, for example, straw
amendment and NT/RT practices, increase the contribution of fun-
gal necromass C to SOC. Overall, fungal necromass had a higher ac-
cumulation efficiency compared to bacterial necromass. Therefore,
optimization of management strategies on fungal development lead
to fungal necromass accumulation and rapidly increase C sequestra-
tion (Hannula & Morriën, 2022).
5 | CONCLUSIONS
All commonly used management prac tices (N fertilization , manure
application, straw amendment, NT/RT, and cover crops) increased
microbial necromass accumulation in soil. The exception was bio-
char application that did not increase microbial necromass accu-
mu l ati o n. The in t ens i tie s of ma n age m ent ef fec t s we re si te- s pec i f ic
and depended on environmental conditions, soil properties (pH,
SOC and text ure) and experimental duration. Microbi al nec ro mass
accumulation was more pronounced in semi- arid or cool climates
and in alkaline soils under N fertilization. Straw amendment and
NT/RT preferentially increased most strongly the fungal nec-
romass accumulation. Straw amendment was more effective in
semi- arid and cool climates in soils with pH <8, which increased
microbial necromass accumulation in proportion with increasing
straw C input. Microbial necromass accumulation was more effec-
tive in soils under NT/RT and cover crops management in humid
conditions. In contrast, manure addition mainly increased bacte-
rial necromass accumulation irrespective of climatic and edaphic
conditions. The accumulation efficiency of fungal necromass was
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14
|
ZHOU et al.
much higher than that of bacterial necromass. Overall, microbial
necromass accumulation was closely connected with living mi-
croorganisms and increased with SOC content s. Consequently,
optimal cropland management increases microbial biomass and
enhances necromass formation and accumulation, and therefore
SOC accrual. In general, microbial necromass accumulation effi-
ciency was 9 %– 16% higher in soil unde r NT/RT, cover c rop s, s traw
amendment and manure application compared to N fertilization. In
summary, management practices considering site- specific climatic
and edaphic conditions could favor microbial growth and necro-
mass accumulation to increase stable soil C formation and accrual
in agroecosystems.
ACKNOWLEDGMENTS
This study was suppor ted by the National Key R&D Program of
China (2022YFD190130 0), National Natural Science Foundation of
China (grant nos. 32071629), the 2115 Talent Development Program
of China Agricultural University and Beijing Advanced Disciplines,
and the RUDN Universit y Strategic Academic Leadership Program
for their support. The contribution of Amit Kumar is supported by
the German Ministry of Education and Research (BMBF) within the
INPLAMINT project (#031B0508- F). Yuan Liu and Lisa Tiemann
are supported by MMPRNT projec t, funded by the Department of
Energy (DOE) Biological and Environmental Research (BER), Office
of Science award DE- SC0014108.
CONFLICT OF INTEREST STATEMENT
The authors declare no conflict of interest.
DATA AVA ILAB ILITY STATE MEN T
The data that support the findings of this study are openly available
in zenodo at https://doi.org/10.5281/zenodo.7556217
ORCID
Ranran Zhou https://orcid.org/0000-0003-2114-8373
Yuan Liu https://orcid.org/0000-0001-8350-5773
Jennifer A. J. Dungait https://orcid.org/0000-0001-9074-4174
Amit Kumar https://orcid.org/0000-0003-4590-1825
Jinsong Wang https://orcid.org/0000-0002-3425-7387
Lisa K. Tiemann https://orcid.org/0000-0003-0514-6503
Fusuo Zhang https://orcid.org/0000-0001-8971-0129
Yakov Kuzyakov https://orcid.org/0000-0002-9863-8461
Jing Tian https://orcid.org/0000-0002-8116-8520
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