Journal of Integrative Agriculture 2019, 18(6): 1360–1368

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RESEARCH ARTICLE

Effects of salinity on the soil microbial community and soil fertility

ZHANG Wen-wen1, 2, 3, WANG Chong1, 2, 3, XUE Rui1, 2, 3, WANG Li-jie1, 2, 3

1
College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, P.R.China
2
Beijing Key Laboratory of Biodiversity and Organic Farming, China Agricultural University, Beijing 100193, P.R.China
3
Key Laboratory of Plant-Soil Interactions, Ministry of Education, Beijing 100193, P.R.China

Abstract
Saline area is an important reserve resource of arable land, however, the effects of soil microorganisms on the soil fertility
in saline coastal ecosystems remain poorly understood. The salinity effects on soil microorganisms, nutrient availabilities
and their relationships were studied in soils along a salinity gradient. A total of 80 soil samples were collected from 16 sites
at four salinity levels (non-saline soil, salt content<1 g kg–1; low salinity soil, salt content=1–2 g kg–1; middle salinity soil,
salt content=2–4 g kg–1; high salinity soil, salt content>4 g kg–1). The results showed that the salinity increased soil pH and
exchangeable Na percent, but decreased soil organic matter, soil exchangeable K, and soil microbial biomass. Both the
abundance and community composition of soil bacteria and fungi were significantly different between the non-saline and the
saline soils. The predominant genera of soil bacteria (Planctomyces and Archangium, positive for carbon fixation) and fungi
(Hydropisphaera, efficient in lignin degradation) changed with the increasing soil salinity and the decreasing soil organic
matter. In summary, soil salinity changed the abundances of soil bacterial, fungal, and arbuscular mycorrhizal communities
and, subsequently, affected their function in saline coastal ecosystems.

Keywords: soil salt content, soil organic matter, T-RFLP, soil health

land is affected by salt, of which more than 1.3 million ha is

1. Introduction
Soil salinization is one of the typical factors for land
degradation throughout the world (Rath and Rousk 2015).
Over 830 million ha of arable land globally is affected by
salinization (Rengasamy 2006). In China, 36 million ha of
Received 7 March, 2018 Accepted 24 July, 2018
ZHANG Wen-wen, Tel: +86-10-62734710, E-mail:
zhangwenwen419@126.com; Correspondence WANG Chong,
Tel: +86-10-62734710, E-mail: wangchong@cau.edu.cn
© 2019 CAAS. Published by Elsevier Ltd. This is an open
access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/).
doi: 10.1016/S2095-3119(18)62077-5
in coastal regions (Li et al. 2014). These coastal soils are
generally affected by salt due to sea-level rise, increased
groundwater abstraction and decreased sediment loads
(IPCC 2013). Salinity has been found to reduce soil
respiration, enzyme activity, soil microbial biomass, and
the bacterial growth rate, all above characteristics influence
biogeochemical cycling (Tripathi et al. 2006; Rousk et al.
2011). The understanding of the microbial community
structure and its function in saline soil represents a crucial
target in ecology because it will be helpful for clarifying the
biological regulation mechanisms for saline soil nutrient
cycles.
Soil microorganisms play a central role in regulating
ecosystem function (Perroni et al. 2014; Qi and Yang 2017).
A previous meta-analysis indicated that the global bacterial
composition of saline soil was affected more greatly by
 ZHANG Wen-wen et al. Journal of Integrative Agriculture 2019, 18(6): 1360–1368
salinity than by any other extreme chemical factors such as
acidity and nutrient availability (Lozupone and Knight 2007).
Soil microorganisms could drive nutrient cycles by affecting
soil organic matter, soil aggregation, porosity and nutrient
availability (Xu et al. 2016). Consequently, any effects of
salt on microbial processes will have large implications for
the soil organic matter concentration and nutrient availability
(Setia et al. 2012). Understanding of the effects of soil
salinity on soil microbial community and its soil ecological
function is of great importance to seek proper methods to
enhance soil fertility of saline land.
In the Bohai Gulf, the native coastal soils are highly
argillaceous saline soils with poor porosity (Zhang et al.
2015), which could directly impact the soil microbial
community and soil nutrient availability (Cui et al. 2016;
Hu et al. 2016). However, less is known about the effects
of salinity on the soil microbial community structure and
the relationship between the soil microorganisms and the
macronutrient availability in this region. Morrissey et al.
(2014) reported that salinity could decrease soil organic
matter by enhancing the activity of carbon-degrading
extracellular enzymes and affecting soil bacterial community.
This research aimed to evaluate the effect of salt on soil
fertility and microbial community structure along a coastal
salinity gradient, which might reveal the relationship
between the soil microorganisms and macronutrient
availability. We hypothesized that soil salinity will change soil
bacterial, fungal, and arbuscular mycorrhizae (AM) fungal
communities, subsequently, drive soil macronutrient cycles.
2. Materials and methods
2.1. Experimental site
The sampling site is in the north of the Bohai Gulf in Binzhou
City, Shandong Province, China (Fig. 1). The mean annual
air temperature is 12.7°C. The mean annual precipitation
is 574.8 mm (1950–2000), of which 70% falls from June to
August. The frost-free period ranges from 140 to 160 days.
The early frost is in November and a late frost in March.
Soil is frozen from December to February of the following
year. Maize (Zea mays), wheat (Triticum aestivum) and
cotton (Gossypium) are the major crops. The vegetation
characteristics for each sampling site were described in
Appendix A.
2.2. Experimental design
Soil samples (loamy soil) (Zhang et al. 2016) were randomly
collected from a saline coastal field (0–20 cm) in June 2014.
All sampling sites were selected at different saline soils
based on the electric conductivity determined by Handheld
1361
117°40´0´´E 118°0´0´´E 118°20´0´´E
N
S10
Bohai Sea
S9
38°0´0´´N
38°0´0´´N
S4(S5) S6
S8 S7
S1
S3(S16) S15
S2(S11, S12,
37°40´0´´N
37°40´0´´N
S13, S14)
Sampling site
117°40´0´´E 118°0´0´´E 118°20´0´´E
Fig. 1 Location of the reclaimed land in Binzhou City, Shandong
Province, China and the sampling sites. A total of 80 soil
samples from 16 sites were collected. All sampling soils were
divided into four salinity levels based on the determination of
soluble salt content (Bao 2005) as follows: non-saline soil (S7,
S11, S12 and S13 with salt content<1 g kg–1), low salinity soil
(S1, S3, S4, S9 and S14 with salt content =1–2 g kg–1), middle
salinity soil (S2, S6 and S15 with salt content=2–4 g kg–1), high
salinity soil (S5, S8, S10 and S16 with salt content>4 g kg–1).
Meter AZS-100 (Beijing Aozuo ecological Instrument Co.,
Ltd., China). The saline soils were collected at four salinity
levels according to Bao (2005) as follows: non-saline soil,
salt content<1 g kg–1; low salinity soil, salt content=1–2 g
kg–1; middle salinity soil, salt content=2–4 g kg–1; high salinity
soil, salt content>4 g kg–1. A total of 80 soil samples from 16
sites were collected and the sample number for each salinity
level was listed in the Tables 1 and 2. Five 1 m2 plots (at
least 10 m apart) were selected according to its determined
salinity by Handheld Meter AZS-100 at each study site. Each
soil sample was a composite of five separate cores (2 cm×
20 cm). Roots of plants (3–5 dominant plant species
with three replicates) within a sampling square were
collected and cleaned for determination of mycorrhizal
colonization. The sampling squares with salt content<4 g
kg–1 were covered with >40% plants, such as Zea mays,
Portulaca oleracea, Setaria viridis, Phragmites australis
and Echinochloa crusgalli. The sampling squares with salt
content>4 g kg–1 were covered with <10% weeds, such as
Aster tartaric, Portulaca oleracea, Phragmites australis and
Suaeda salsa. We selected the consistent dominant grass
covers of the sampling sites in same salinity level to minor
the influence of plants on soil microbes.
2.3. Soil and plant analysis
Each composited field soil sample was mixed, homogenized
and transported inside an ice box to the laboratory, and
1362 ZHANG Wen-wen et al. Journal of Integrative Agriculture 2019, 18(6): 1360–1368

Table 1 Soil chemical properties in saline coastal soils at different salinity levels
Sample Salt content Organic matter Available P Exchangeable K
Salinity1) pH ESP (%)2)
number (g kg–1) (g kg–1) (mg kg–1) (mg kg–1)
Non-saline n=20 0.75±0.04 d 8.15±0.04 b 5.91±0.53 c 12.74±0.19 a 11.4±2.4 a 278.4±16.2 a
Low n=25 1.55±0.06 c 8.14±0.04 b 16.54±1.23 b 11.58±0.50 b 14.0±2.1 a 282.1±19.7 a
Middle n=15 2.75±0.26 b 8.18±0.06 b 24.28±2.60 a 8.82±0.52 c 16.4±2.4 a 199.7±18.7 b
High n=20 4.93±0.20 a 8.34±0.05 a 25.24±2.55 a 7.54±0.53 d 17.7±2.9 a 219.1±14.3 ab
1)
Non-saline, non-saline soil (salt content<1 g kg–1); Low, low salinity soil (salt content=1–2 g kg–1); Middle, middle salinity soil (salt
content=2–4 g kg–1); High, high salinity soil (salt content>4 g kg–1).
2)
ESP, the exchangeable sodium percentage.
Data are mean±SD. Different letters indicate significant differences (P<0.05) at different salinity levels.

Table 2 Soil biological characteristics in saline coastal soils

Salinity1) Sample number Root colonization (%) Microbial biomass carbon (mg kg–1) Microbial biomass nitrogen (mg kg–1)
Non-saline n=20 53.8±5.7 a 298.8±56.6 a 23.7±3.3 a
Low n=25 42.9±4.6 a 417.1±36.0 a 7.6±0.9 b
Middle n=15 41.5±6.6 a 349.5±67.1 a 8.2±1.5 b
High n=20 41.3±5.7 a 177.3±28.1 b 5.1±0.9 b
1)
Non-saline, non-saline soil (salt content<1 g kg–1); Low, low salinity soil (salt content=1–2 g kg–1); Middle, middle salinity soil (salt
content=2–4 g kg–1); High, high salinity soil (salt content>4 g kg–1).
Data are mean±SD. Different letters indicate significant differences (P<0.05) at different salinity levels.

sieved through 2-mm mesh screen within 24 h. The
soil for DNA analysis was then stored at –80°C. The
soil for soil microbial carbon and nitrogen extraction was
stored at 4°C. The soil was air-dried for pH, salt content,
exchangeable Na percent, organic matter, available P and
exchangeable K determination. The total salt concentration
was determined with 50 mL of extracts (1:5 soil:water (w/v),
vacuum filtered<0.45 μm) (Bao 2005). Exchangeable Na
was determined by NH4OAc-NH4OH (pH 9) extraction, and
the total exchangeable cations were determined by 1 mol
L–1 NaOAc (pH 8.2) extraction (Bao 2005). Soil organic
carbon was determined from K2Cr2O7 colorimetric oxidization
(Organic matter=1.724×Organic carbon) (Walkley 1947). A
1:5 soil:water (w/v) solution was used to determine the soil
pH. The soil microbial biomass carbon and nitrogen were
measured following fumigation extraction (Brookes et al.
1985; Vance et al. 1987). Briefly, 20 g soil was fumigated
with ethanol-free chloroform for 24 h. Fumigated and non-
fumigated soils were extracted with 40 mL of 0.5 mol L–1
K2SO4. The microbial biomass carbon (Cmic) was calculated
as follows:
Cmic=2.64×(Cfumigated soil−Cnon-fumigated soil) (1)
Where, 2.64 is a conversion factor, Cfumigated soil indicates
soil carbon from the fumigated soil and C non-fumigated soil
indicates soil carbon from the non-fumigated soil.
The microbial biomass nitrogen (Nmic) was calculated
as follows:
Nmic=5.0×(Nfumigated soil−Nnon-fumigated soil) (2)
Where, 5.0 is a conversion factor, Nfumigated soil indicates soil
nitrogen from the fumigated soil and Nnon-fumigated soil indicates
soil nitrogen from the non-fumigated soil. Mycorrhizal
colonization was measured according to the method of Li
et al. (2012).
2.4. Terminal restriction fragment length polymor-
phism (T-RFLP) analysis
Soil DNA was extracted (0.5 g sample) with five replicates
for each site (total 16 sites) by the PowerSoil ® DNA
Isolation Kit (MoBio Laboratories, Carlsbad, CA, USA).
Polymerase chain reaction (PCR) amplification of the
bacterial 16S rDNA (about 880-bp fragment, primers
27F and 907R) and the fungal ITS rDNA (600–650 bp,
primers EF3RCNL and ITS4) and the T-RFLP analyses
were conducted according to Cao et al. (2015). Nested-
PCR amplification for the AM fungal community was
conducted. The first PCR reaction was performed with AML1
(5´-ATCAACTTTCGATGGTAGGATAGA-3´) and AML2
(5´-GAACCCAAACACTTTGGTTTCC-3´) to amplify an
approximately 795-bp fragment of small subunit ribosomal
RNA (SSU rRNA) (Lee et al. 2008). Nested-PCR reaction
mixtures and thermal profile were referenced to Li et al.
(2015). The quantity of PCR products was determined using
a 1% agarose gel. Acceptable products were the second
PCR template with the primers NS31-FAM (5´-TGGAGG
GCAGTCTGTC-3´) and AM1 (5´-GTTTCCCGTAAGGCG
CCG AA-3´) (Li et al. 2015). The purified PCR products were
digested by the restriction enzymes MspI and HinfI (New
England Biolabs, Beverly, MA, USA) for bacteria and fungi,
respectively. The T-RFs with the fluorescent labels were
determined using a 3130xl Genetic Analyzer (Applied Bio-
systems, CA, USA). The relative abundance of each T-RF
 ZHANG Wen-wen et al. Journal of Integrative Agriculture 2019, 18(6): 1360–1368
was represented by the percentage calculated relative to the
total peak area in a given T-RFLP profile. T-RFs displayed a
relative abundance<1% were ignored and fragments ranged
from 50 to 500 bp were analysed.
2.5. Cloning and sequencing
The PCR products of the 16S rRNA gene, ITS rRNA gene
and SSU rRNA gene were purified and ligated into the
pGEM-T easy vector. Three clone libraries (16S rRNA gene,
ITS rRNA gene and SSU rRNA gene) were constructed to
assign T-RFs. Each library contained 100 clones, which
were determined by the ABI 3730xl (Applied Biosystems).
Sequences were blasted and aligned by the CLUSTALW
algorithm in MEGALIGN 5.07. The reference sequences
were chosen based on the highest sequence match and
the lowest expected value (E value=1e-10). T-RFs were
compared to the clones by the TRAMP with the fragment
size error±2 bp (Toljander et al. 2007). The taxonomy of
the representatives from each operational taxonomic unit
was blasted at the 97% similarity level.
2.6. Statistical analysis
A natural log transformation was necessary for all chemical
and biological measures. Site differences were tested by
one-way analysis of variance (ANOVA) with the Student-
Newman-Keuls (S-N-K) test (Appendix B). The main effect
of salinity was tested using mixed models that contained
both fixed (salinity level) and random (site) effects (Tables 1
and 2). Data were statistically analysed by the SPSS 16.0
(SPSS Inc., Chicago, USA). The exchangeable sodium
percentage (ESP) was defined as: ESP (%)=(Exchangeable
Na+/CEC)×100, where, Na+ is the exchangeable Na+ (meq
100 g –1), and CEC is the measured cation exchange
capacity (meq 100 g–1). Analysis of similarity (ANOSIM)
was performed with the R vegan package to examine the
significance of salinity effects on the T-RFLP profiles of
soil bacteria, fungi and AM fungi. Principle component
analysis (PCA) was conducted using Canoco 4.5. Pearson’s
correlation analyses were carried out to determine the
parameter correlations.
3. Results
3.1. Soil chemical characteristics in saline coastal
soils
The soil pH, ESP, organic matter and exchangeable K were
significantly changed with increasing salinity (Table 1).
Soil soluble salt content statistically significantly increased
with increasing salinity (P<0.05). Soil pH was higher in
1363
the high salinity soil compared to the non-saline, low, and
middle salinity soils (P<0.05). The soil ESP was increased
while the soil organic matter was decreased with the
salinity increasing (P<0.05). The soil exchangeable K was
statistically significantly lower in the middle salinity soils than
that in the non-saline soils (P<0.05).
3.2. Mycorrhizal colonization and soil microbial
biomass
The plants roots were tested positive for arbuscular
mycorrhizal colonization in soils of all four salinity levels
(Table 2). Average percent root colonization ranged
from 41.3 to 53.8%. The microbial biomass carbon was
statistically significantly decreased in the high salinity soils
(Table 2, P<0.05). The greatest soil microbial biomass
carbon was recorded in the low salinity soil. The microbial
biomass nitrogen in the non-saline soils was statistically
significantly higher than that in the saline soils (Table 2,
P<0.05). The data indicated that the soil microbial biomass
nitrogen in the saline soils was less than 35% of that in the
non-saline soil.
3.3. Genetic profiling of soil bacterial community in
saline coastal soils
Totally 60 T-RFs were detected across the salinity levels. A
total of 90 16S rRNA gene sequences were obtained from the
16S rRNA gene clone library. Over 80% of the T-RFs can be
assigned from the 16S rRNA gene library, confirming a good
coverage of diversity. The T-RFLP analysis of the bacteria
showed that the 16S rRNA sequences were clustered into
Proteobacteria (31.0–38.4%), Actinobacteria (6.8–14.7%),
Planctomycetacia (5.2–6.2%) and Bacteroidetes (1.9–3.3%)
(Fig. 2-A). Planctomyces, Archangium, Aquamicrobium,
Piscinibacter and Bosea were the predominant genera,
accounting for 5.2–6.2, 4.3–7.3, 8.1–9.7, 3.0–6.7 and
7.7–11.1% of the total bacterial population in all sampling
soils, respectively. Compared to the non-salinity, soil salinity
decreased the relative abundance of Planctomyces and
Archangium, while increased the relative abundance of
Piscinibacter and Aquamicrobium (P<0.05). The structure
of bacterial community differed across the salinity levels
(non-parametric multivariate analysis of variance (NP-
MANOVA) F=2.75, P<0.001); all pairwise comparisons
between sites yielded P<0.05. The salinity gradient shifted
soil bacterial composition and their structure in the saline
coastal soils (Fig. 3). The PCA analysis revealed that
bacterial composition distinct between the non-saline and
the middle and high saline conditions (Fig. 3-A). This was
further confirmed by an ANOSIM of the non-saline and
saline soils (Table 3).
1364 ZHANG Wen-wen et al. Journal of Integrative Agriculture 2019, 18(6): 1360–1368

A 100 Uncultured bacterium

Pontibacter Bacteroidetes
90 Chloroflexus Chloroflexi
Anaerolineaceae
80 Planctomyces Planctomycetes
Nonomuraea
Relative abundance of

70
Micromonosporaceae
60 Arthrosphaerae Actinobacteria
bacteria (%)

Catellatospora
50 Streptomyces
40 Variovorax
Azospirillum
30 Rhodoplanes
Archangium Proteobacteria
20 Bosea
Piscinibacter
10 Aquamicrobium
0 Sphingopyxis
Non-saline Low Middle High Skermanella
B 100
90 Uncultured fungus
80 Fusarium
Relative abundance of

70 Thielavia Ascomycota
60 Hydropisphaera
fungi (%)

Myrothecium
50
Trichoderma
40 Chaetomium
30 Spizellomyces Chytridiomycota
20
10
0
Non-saline Low Middle High
C
100
Uncultured AM fungus
90
Septoglomus
Relative abundance of

80
70 Sclerocystis
Glomeromycota
AM fungi (%)

60 Rhizophagus
50 Glomus
40
30
20
10
0
Non-saline Low Middle High

Fig. 2 Distributions of 16S rRNA phylotypes (A), ITS rRNA phylotypes (B) and the small subunit ribosomal rRNA (SSU rRNA)
phylotypes (C) within the clone libraries. AM, arbuscular mycorrhizae. Non-saline, non-saline soil (salt content<1 g kg–1);
Low, low salinity soil (salt content=1–2 g kg–1); Middle, middle salinity soil (salt content=2–4 g kg–1); High, high salinity soil (salt
content>4 g kg–1).

3.4. Genetic profiling of soil fungal community in
saline coastal soils
Totally 55 T-RFs were detected across the salinity levels.
A total of 89 ITS rRNA gene sequences were obtained
from the ITS rRNA gene clone library. Over 80% of the
abundant T-RFs can be assigned from the ITS rRNA
gene library, confirming a good coverage of diversity. The
ITS rRNA sequences were clustered into Ascomycota
(72.6–84.5%) and Chytridiomycota (6.3–12.8%) (Fig. 2-B).
Fungal community of all treatments were dominated by
Hydropisphaera (26.5–40.2%) and Trichoderma (21.0–
36.3%). Compared to the non-saline soils, the high salinity
soils increased the relative abundance of Hydropisphaera,
while decreased the relative abundance of Trichoderma.
There were significant differences of the community
structure of fungi across the salinity levels (F=4.73, P<0.002)
and all pairwise comparisons between the salinity levels
(P<0.03). The PCA analysis revealed a difference in fungal
community between non-saline and saline soils (Fig. 3-B).
The fungal community of non-saline and low salinity soils
separated clearly from that of the middle and high salinity
soils along the second axis. There were also differences in
community composition evidenced by the ANOSIM analysis
between the non-saline soils and the middle salinity soils
(Table 3, P<0.05).
 ZHANG Wen-wen et al. Journal of Integrative Agriculture 2019, 18(6): 1360–1368 1365

Non-saline soil, salt content<1 g kg–1 Middle salinity, salt content=2–4 g kg–1
Low salinity, salt content=1–2 g kg–1 High salinity, salt content>4 g kg–1

A 1.0 B
S10 1.0
S2
Trichoderma
S16
Pontibacter Micromonospora.

S15 S8
Catellatospora
Skermanella
S16
Rhodoplanes S2
Thielavia1

PC2 (13.4%)
Microbacterium S10 Uncultured fungus
S3 S5
PC2 (27.7%)

Variovorax S6 S15
S13 S8 S6
Hydropisphaera
Aquamicrobium S5 Pelobacter S3
Piscinibacter S11 Fusarium
S12 S13
Sphingopyxis Streptomyces
S9
S12
Bosea S7
Planctomyces S1 Spizellomyces
S14 Chaetomium
S7 Azospirillum S1
S11 S4 S14
S9 Myrothecium S4

–0.8
Uncultured bacterium Archangium –0.8
–1.0 1.0 –1.0 1.2
PC1 (36.0%) PC1 (76.8%)
C
1.0
Rhizophagus

S8
S5
S10
PC2 (29.5%)

S16
S12

S15
S13
Uncultured fungus

Sclerocystis S3
S11
S14 S2 S7 Septoglomus
S1
S4 S6
Glomus S9 Fig. 3 Principal component plots generated from the terminal
–0.6 restriction fragment profiles of soil bacteria (A), fungi (B) and
–1.0 1.0 arbuscular mycorrhizae fungi (C). S1–S14 present the centroids
PC1 (55.2%) for each sampling site.

Table 3 Analysis of similarity (ANOSIM) for comparisons of bacterial, fungal and arbuscular mycorrhizal (AM) fungal communities
using the data of terminal restriction fragment length polymorphism
Bacteria Fungi AM fungi
Salinity1)
R-value P-value R-value P-value R-value P-value
Non-saline–Low 0.18 0.002 0.190 0.001 0.04 0.120
Non-saline–Middle 0.32 0.001 0.120 0.030 0.06 0.110
Non-saline–High 0.13 0.003 0.002 0.350 0.16 0.005
Low–Middle 0.17 0.020 0.060 0.130 0.16 0.007
Low–High 0.11 0.020 0.130 0.006 0.13 0.004
Middle–High 0.06 0.090 0.003 0.390 0.08 0.060
1)
Non-saline, non-saline soil (salt content<1 g kg–1); Low, low salinity soil (salt content=1–2 g kg–1); Middle, middle salinity soil (salt
content=2–4 g kg–1); High, high salinity soil (salt content>4 g kg–1).

3.5. Genetic profiling of soil AM-fungal community be assigned from the SSU rRNA gene library, confirming
in saline coastal soils a good coverage of diversity despite its limited sequence
numbers. The SSU rRNA sequences were clustered
Totally 12 T-RFs were detected across the profiles. A total into Glomeromycota (93.2–96.2%) (Fig. 2-C). Glomus
of 35 SSU rRNA gene sequences were obtained from the (30.1–50.7%) and Sclerocystis (21.4–29.1%) were the
SSU rRNA gene clone library. Over 90% of the T-RFs can first two dominant AM fungal species, while Rhizophagus
1366 ZHANG Wen-wen et al. Journal of Integrative Agriculture 2019, 18(6): 1360–1368

(7.0–25.4%) and Septoglomus (8.2–13.9%) were abundant There was a significantly negative correlation between soil
Glomeromycota species. Compared to the non-saline soils, salt content and organic matter (Fig. 4-A). Morrissey (2014)
the abundance of Glomus increased in low and middle attributed the decrease of soil organic matter under saline
salinity soils, and it decreased in the high salinity soils. conditions to the following: (i) the decrease of plant input
The relative abundance of Sclerocystis and Septoglomus for scarce vegetation cover and (ii) the enhancement of
decreased in all saline soils. The relative abundance of the activity of carbon-degrading extracellular enzymes and
Rhizophagus decreased in low salinity soils while increased microbial decomposition rates. Setia et al. (2013) further
in high salinity soils compared to the non-saline soils. demonstrated that lower organic matter in saline soil is
The structure of AM-fungal community differed across all more likely to be due to the decreased plant input than the
salinity levels (F=3.04, P<0.01); all pairwise comparisons increased decomposition.
between the salinity levels yielded P<0.05. The PCA result
demonstrated that the AM-fungal community in high salinity 4.2. Effects of soil salinity on soil microbial biomass
soils was different from those in the other three sampling
soils (Fig. 3-C). This difference was further confirmed by an Soil microbial biomass is considered to be a labile soil
ANOSIM between the high salinity soils and the non-saline organic fraction and the important source and sink for plant
and low salinity soils (Table 3). available nutrients (Ajwa et al. 1999). In this study, soil
salinity decreased microbial biomass nitrogen, which was
4. Discussion negatively correlated with the salt content and ESP (Fig. 4-B
and C). Zhou et al. (2017) attributed this decrease of
4.1. Effects of soil salinity on soil organic matter in microbial nitrogen to the inhibited microbial N immobilization
the saline coastal system under salt stress.
Soil microbes are essential in soil carbon mineralization
In the present study, the middle and high salinities exhibited and accumulation, which determines soil fertility. The soil
greater salt content and ESP, and less organic matter salinity decreased the soil microbial biomass carbon, which
compared to the non-saline and low salinity soils (Table 2). was positively correlated with organic matter (Fig. 4-D).

A B C D
7 60 60
1 000
6
Soil microbial biomass

Soil microbial biomass

Soil microbial biomass

50 50
Soil SC (g kg–1)

nitrogen (mg kg–1)

5 800
nitrogen (mg kg–1)

carbon (mg kg–1)

40 40
4 600
30 30
3
20 20 400
2
1 10 10 200
0 0 0 0
0 5 10 15 20 0 2 4 6 8 0 25 50 0 10 20
Soil OM (g kg–1) Soil SC (g kg–1) Soil ESP (%) Soil OM (g kg–1)
E
F G
0.4 H
0.4 0.4
Hydropisphaera (%)

0.4
Hydropisphaera (%)
The abundunce of

The abundunce of

The abundunce of
The abundunce of
Septoglomus (%)

Septoglomus (%)

0.3 0.3 0.3 0.3

0.2 0.2 0.2 0.2
0.1 0.1 0.1 0.1

0 0 0 0
0 5 10 0 5 10 15 20 0 2 4 6 8 0 5 10 15 20
Soil SC (g kg–1) Soil OM (g kg–1) Soil SC (g kg–1) Soil OM (g kg–1)

Fig. 4 Correlations between the abundance of soil microbes and the soil salt content (SC), organic matter (OM), soil exchangeable
sodium percentage (ESP) and microbial biomass nitrogen and carbon. Soil salt content was negatively correlated with soil OM
(A; R=–0.691, P<0.01), microbial biomass nitrogen (B; R=–0.418, P<0.01) and the abundance of Septoglomus (G; R=–0.250,
P<0.05), while positively correlated with the abundance of Hydropisphaera (E; R=0.525, P<0.01). The soil ESP was negatively
correlated with soil microbial biomass nitrogen (C; R=–0.658, P<0.01). The soil OM had a significantly positive correlation with
microbial biomass carbon (D; R=0.516, P<0.01), but a significantly negative correlation with the abundance of Hydropisphaera (F;
R=–0.599, P<0.01). The soil OM had a significant positive correlation with the abundance of Septoglomus (H; R=0.291, P<0.01).
 ZHANG Wen-wen et al. Journal of Integrative Agriculture 2019, 18(6): 1360–1368
Wong et al. (2008) demonstrated that the low soil microbial
carbon was attributed to the low soil organic carbon that
resulted from little carbon input into the soils for the scarcity
of vegetation under high salt condition.
4.3. Effects of salinity on the soil microbial commu-
nity and soil fertility
Soil salinization could change soil microbial community,
which is well known to driving soil nutrient cycle in various
land ecosystems. Some bacterial classes including
Actinobacteria, Proteobacteria and Planctomyces could help
promote dissolved inorganic carbon fixation (DeLorenzo
et al. 2012). Archangium was affiliated Proteobacteria
phylum which was negatively correlated with soil carbon
mineralization rates in harsh environments (Fierer et al.
2007). In the present study, soil salinity decreased the
relative abundance of Planctomyces and Archangium
(Fig. 3-A), which was positively correlated with the soil
organic matter (R>0.230, P<0.01). These results suggested
that soil salinization decreased the soil bacteria which might
help soil organic matter input or stabilization.
The distribution and activity of soil fungi could affect soil
nutrient transformation (Babu and Reddy 2011). Moreta
(2002) demonstrated that Hydropisphaera belonging to
Ascomycota phylum was capable to degrading lignin in a
salt marsh. The high salinity soils increased the relative
abundance of Hydropisphaera, which was positively
correlated with the salt content while negatively correlated
with the organic matter (Fig. 4-E and F). These results
indicated that the dominant Hydropisphaera possibly
decreased soil fertility by promoting organic matter
decomposition.
AM fungi could improve host plant nutrition and
physiological adaptation under salinity stress (Porcel
et al. 2012). Glomus could enhance the phosphorus and
potassium uptakes of plants under salt stress (Porcel
et al. 2012). In this study, the high salinity decreased the
relative abundances of Glomus, indicating a harm effect
of soil salinity on the plant growth-promoting AM fungi.
The native AM fungal strains Rhizophagus intraradices,
Claroideoglomus etunicatum and Septoglomus constrictum
could increase the plant survival rate and promote the
plant growth performance under salt stress (Estrada et al.
2013). In present study, the salinity decreased the relative
abundance of Septoglomus, which was positively correlated
with the soil organic matter and negatively correlated with
the salt content (Fig. 4-G and H). Future studies using more
accuracy molecular method are needed to create a holistic
view of soil microbial succession and function in the saline
coastal ecosystem.
1367
5. Conclusion
High salinity increased the soil salt content and ESP, and
decreased the soil organic matter, soil exchangeable K and
soil microbial biomass. There were different compositions of
bacterial and fungi communities between in the non-saline
and saline soils, while AM fungal community was different
in the high salinity soils. There were correlations between
soil nutrients and soil microbial gene sequences across all
salinity level soils. This study stressed the potential role of
soil microbial compositions on the fertility of saline coastal
soil.
Acknowledgements
This work was funded by the National Key Research and
Development Program of China (2016YFE0101100), the
National Natural Science Foundation of China (31570514),
the Key Technologies R&D Program of China during the 12th
Five-year Plan period (2013BAD05B03).
Appendices associated with this paper can be available on
http://www.ChinaAgriSci.com/V2/En/appendix.htm
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Executive Editor-in-Chief ZHANG Wei-li
Managing editor SUN Lu-juan