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European Journal of Soil Biology 71 (2015) 37e44

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European Journal of Soil Biology

journal homepage: http : / /www.elsevier .com/locate/ejsobi

Original article

Microbial responses to erosion-induced soil physico-chemicalproperty changes in the hilly red soil region of southern China

Zhongwu Li a, b, c, *, Haibing Xiao a, b, Zhenghong Tang d, Jinquan Huang e,Xiaodong Nie a, b, Bin Huang a, b, Wenming Ma a, b, f, Yinmei Lu a, b, Guangming Zeng a, b

a College of Environmental Science and Engineering, Hunan University, Changsha 410082, PR Chinab Key Laboratory of Environmental Biology and Pollution Control (Hunan University), Ministry of Education, Changsha 410082, PR Chinac State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Institute of Soil and Water Conservation, Chinese Academy of Sciences,Yangling, Shanxi 712100, PR Chinad Community and Regional Planning Program, 313 Architecture Hall, University of Nebraska e Lincoln, Lincoln, NE 68588-0105, USAe Department of Soil and Water Conservation, Yangtze River Scientific Research Institute, Wuhan 430015, PR Chinaf College of Tourism Historical Culture, Southwest University for Nationalities, Chengdu 610041, PR China

a r t i c l e i n f o

Article history:Received 2 July 2015Received in revised form7 October 2015Accepted 14 October 2015Available online 24 October 2015

Keywords:Soil erosionEnzyme activityBacterial communitySoil biological characteristicDissolved organic carbon

Abbreviations: DCA, detrended correspondence ancarbon; MBC, microbial biomass carbon; PCA, principDGGE, polymerase chain reaction-denaturing gradieredundancy analysis; SOC, soil organic carbon; TN, to* Corresponding author. College of Environment

Hunan University, Changsha 410082, PR China.E-mail address: lizw@hnu.edu.cn (Z. Li).

http://dx.doi.org/10.1016/j.ejsobi.2015.10.0031164-5563/© 2015 Elsevier Masson SAS. All rights res

a b s t r a c t

Water erosion can significantly alter soil physicochemical properties. However, little is known about soilmicrobial responses to erosion-induced soil physicochemical properties changes in the hilly red soilregion of southern China. This research was conducted to determine the impact of water erosion on soilbiological properties and the relationships between microbial community compositions and physico-chemical parameters. Soil samples of the 0e10 cm layer in one fallow depositional site and fiveerosional sites (including a Pinus massoniana Lamb. site, Elaeocarpus decipiens Hemsl. site, Micheliamaudiae Dunn site, Cinnamomum bodinieri Levl. site and Lagerstroemia indica Linn. site) were collected.Denaturing gradient gel electrophoresis (DGGE) profiles of 16S rDNA were generated to describe theinfluence of soil erosion on bacterial communities. The results showed that the depositional site hadgreater microbial biomass and enzyme activities compared to most erosional sites. Redundancy analysissuggested that all physico-chemical parameters together accounted for 79.6% of the variation in bacterialcommunity (P < 0.05). Among these parameters, dissolved organic carbon (DOC) showed a predominanteffect on the variation (19.3%; P < 0.05), while soil organic carbon (SOC) and total nitrogen individuallycontributed to only 3% and 2.5% of the variance in bacterial community, respectively (P > 0.05). Theseresults indicated that soil deposition is beneficial to enhance soil microbial biomass, while soil erosion isin reverse. DOC is a more important factor influencing soil biological characteristics in comparison toother measured physicochemical parameters. Relative to the quantity of SOC, the quality of C is moreimportant in influencing soil biological properties.

© 2015 Elsevier Masson SAS. All rights reserved.

1. Introduction

Soil microorganisms play important roles in soil ecosystems byregulating the decomposition of organic matter, the formation ofhumus and cycling of nutrient elements [1,2]. In addition, soil

alysis; DOC, dissolved organical component analysis; PCR-nt gel electrophoresis; RDA,tal nitrogen.al Science and Engineering,

erved.

microbes release various enzymes which have widely been used asindicators for soil biological properties and sustainability of eco-systems [3,4]. Soil enzymes can catalyze nutrient recycling in formsavailable for plants and other organisms and mediate most soilbiological processes. Thus, soil microorganisms and enzymes arethe main driving force in soil biochemical processes [4,5].Compared with soil physical and chemical properties, both soilmicroorganisms and enzymes are more sensitive to the environ-mental change and disturbance and can better indicate current soilenvironmental conditions [6]. Soil erosion is the most widespreadform of soil degradation and represents one of the most importantbut poorly quantified environmental problems [7,8]. Soil erosion is

Delta:1_given nameDelta:1_surnameDelta:1_given nameDelta:1_surnameDelta:1_given nameDelta:1_surnameDelta:1_given nameDelta:1_surnameDelta:1_given namemailto:lizw@hnu.edu.cnhttp://crossmark.crossref.org/dialog/?doi=10.1016/j.ejsobi.2015.10.003&domain=pdfwww.sciencedirect.com/science/journal/11645563http://www.elsevier.com/locate/ejsobihttp://dx.doi.org/10.1016/j.ejsobi.2015.10.003http://dx.doi.org/10.1016/j.ejsobi.2015.10.003http://dx.doi.org/10.1016/j.ejsobi.2015.10.003

Z. Li et al. / European Journal of Soil Biology 71 (2015) 37e4438

usually coupled with changes in local soil properties and biologicalprocesses, and can affect soil carbon dynamics through manydifferent ways [9e11]. For example, erosion-induced soil aggre-gates destruction can strongly impact the stability of carbon insoils.

In the past decades, substantial research efforts were performedto characterize the impact of water erosion on the distribution ofsediment as well as the associated carbon within landscapes[12e14], showing that water erosion disturbed carbon-rich topsoiland preferentially removed the finer particles and associated soilorganic carbon (SOC) from the eroding slope to the depositional site[15e17]. However, little information is available on the response ofsoil microbial community to changes of erosion-induced physico-chemical properties in the hilly red soil region of southern China.Altered SOC, total nitrogen (TN), and labile organic carbon (e.g.,dissolved organic carbon) storage in soils may induce significanteffects on the composition and activity of microbial communities.Previous research confirmed that among all organic matter frac-tions, the labile dissolved organic carbon accounted for the largestamount of variation in microbial functional diversity [18]. While inthe study by Fierer and Jackson [19], the differences in the diversityand richness of soil bacterial communities were largely explainedby soil pH. A complete and systematic understanding of soil mi-crobial responses to physicochemical properties changes is stilllacking. Previous research that addressed the microbiologicalproperties were mainly restricted to the effects of field manage-ment, fertilization and vegetation patterns, while the impact ofwater erosion on soil biological properties was rarely examined.

In this study, we hypothesized that soil deposition is beneficialto enhance soil biological activities, and the heterogeneity in soilbiological characteristics between erosional and depositional sitesis closely correlated to erosion-induced soil physicochemicalproperties changes, particularly to labile organic carbon. To test ourhypotheses, the spatial variabilities of soil microbial diversity andenzyme activities were studied in a closed basin with six differentvegetation types in the hilly red soil region. Due to high tempera-ture and frequent high-intensity thunderstorms, accelerated soilerosion has become widespread there. In addition, PCR-DGGE wasapplied to intuitively discern the dynamic of microbial commu-nities in different sites [20]. Information on soil microbial com-munity composition in combination with soil enzyme activitiesinformed us the long-term effects of soil erosion on organic matterdecomposition andmaintenance in both erosional and depositionalsites of mountain ecosystems. The main objectives of this studywere to (a) investigate the distinctions of soil biological propertiesin erosional and depositional sites; and (b) quantify the relation-ships between soil physicochemical parameters and microbialcommunities.

2. Materials and methods

2.1. Experimental sites

The study was conducted at the Soil and Water ConservationMonitoring Station of Shaoyang City, Hunan Province, China (Fig. 1).This region has a typical subtropical monsoon climate, with annualmean minimum and maximum precipitations of 1218.5 mm and1473.5 mm, respectively. The maximum rainfall usually occurs inJune and theminimum in December. Themean annual temperatureis 17.1 �C, and the hottest month is July with an average tempera-ture of 26.6 �C. The soil in the study area is typically Quaternary redclay, which is extremely eroded and characterized by low pH andinsufficient available nutrients for vegetations [17]. Soil with clay toloam texture was classified as Ultisol in U.S. Soil Taxonomy. Topo-graphically, the slopes are generally

Fig. 1. Sampling locations of the study area (PE: Pinus massoniana Lamb. site; EE: Elaeocarpus decipiens Hemsl. site; ME:Michelia maudiae Dunn site; CE: Cinnamomum bodinieri Levl.site; LE: Lagerstroemia indica Linn. site; GD: Fallow grass site).

Z. Li et al. / European Journal of Soil Biology 71 (2015) 37e44 39

activities of two representative soil enzymes, including urease andcatalase, were measured using analysis techniques modified byGuan [26]. Soil urease (EC 3.5.1.5; URE) activity was measured byindophenol colorimetry with urea as the substrate. Briefly, 5 g(passed through 1 mm sieve) of soil and 1 ml of methylbenzenewere combined in a 50 ml conical flask. After 15 min, 10 ml of 10%urea solution (weight/volume) and 20 ml of citrate buffer solution(pH 6.7) were mixed and then incubated at 37 �C for 24 h. Afterfiltration, 1 ml of the filtrate was reacted with 4 ml sodium phenolsolution (1.35 mol L�1) and 3 ml of 0.9% (active chlorine concen-tration) sodium hypochlorite solution and then diluted to 50 mlwith ultrapure water in volumetric flask. The amounts of releasedammonium were analyzed by UV spectrophotometer at 578 nmand expressed as mmol NH4þeN g�1 dry soil [27]. Soil catalase (EC1.11.1.6; CAT) activity was measured by UV spectrophotometry withhydrogen peroxide as the substrate. Soil samples of 2 g (passedthrough 1 mm sieve) were amended with 5 ml of 0.3% (weight/volume) hydrogen peroxide solution and 40ml ultrapurewater in a100 ml conical flask. After 20 min of incubation at 37 �C, 1 mlsaturated aluminum potassium alum solution was added to flaskand then filtered. The supernatant of the solution was analyzed at240 nm and the activity was expressed as mmol KMnO4 g�1 dry soil.

2.3.3. DNA extraction and PCR-DGGEThe total genomic DNA of soil samples was extracted according

to the method described by Yang [28]. The extracted DNA waspurified with a Purification Kit (TIANquick Midi Purification Kit,Tiangen biotech, Beijing, China) and stored at �20 �C before use.Subsequently, the variable V3 region of the bacterial 16S rDNA

genes was amplified with bacterial universal primers 338F/518R[29]. A GC clamp was attached to the forward primer (338F) toprevent complete separation of the strands during DGGE. Targetedgene fragments were amplified using a 50 ml mixture containing2 U of Taq polymerase (Tiangen biotech, Beijing, China), 5 ml of10 � PCR Buffer, 1 ml of dNTPs (10 mM each), 1 ml each primer(20 mM), 2 ml of BSA (Bovine serum albumin, 10 mg ml�1), 1 mltemplate DNA. PCR amplificationwas performedwith theMyCyclerthermal cycle (Bio-Rad, USA) using conditions as follows: 94 �C for5 min; followed by 35 cycles of 94 �C for 45 s, 55 �C for 40 s, 72 �Cfor 40 s; and single extension at 72 �C for 7 min, and end at 4 �C[30].

DGGE was carried out using a Dcode Universal MutationDetection System (Bio-Rad, USA). The PCR-amplified DNA products(25 mL) were loaded on the 8% polyacrylamide gel with a lineargradient of 30e70%. Gel was run 12 h at 120 V in 1 � TAE buffermaintained at 60 �C. Subsequently, gel was stained with SYBRGreen I nucleic acid gel stain for 10 min [31]. The DGGE image wasscanned and analyzed with the QuantityOne software (version 4.5,Bio-Rad, USA) to determine the microbial diversity in soil samples.

2.4. Statistical analysis

One-way analysis of variance (ANOVA) was performed tocompare the mean values for different sites and test whether therewere any significant differences among the mean values at the 95%confidence level by using SPSS 19.0 for Windows. Linear fitting wasconducted to determine the correlation intensity between param-eters (SPSS 19.0).

Z. Li et al. / European Journal of Soil Biology 71 (2015) 37e4440

The Shannon index of species diversity (H) based on DGGEbanding number and relative intensity was calculated according toLi [29].

H ¼ �Xs

i¼1pi logðPiÞ (2)

where Pi is the proportion of band i in the DGGE profile and s is thetotal number of the bands. The H index is used as a representationof microbial diversity that takes into account the richness andproportion of each species in a population. Detrended correspon-dence analysis (DCA) was carried out first to decide between thelinear and unimodal response model for these microbial data. Thelength of the first DCA ordination axis was 1.379, which did notindicate clear unimodal species responses. Therefore, PCA and RDAwere performed using Canoco (version 4.5) for determination ofmultivariate relationships between bacterial community composi-tions and soil physicochemical properties. Additionally, variationpartitioning was conducted using partial RDA analysis to distin-guish the proportion of variation solely explained by each physico-chemical parameter separately [30].

3. Results

3.1. Erosion-induced changes in soil physicochemical properties

Fundamental physico-chemical characteristics of the studiedsoils are summarized in Table 1. A comparison of the soil 137Csconcentrations to the undisturbed reference inventory(1920 ± 126 Bq m�2) confirms that the PE, EE, ME, CE and LE sitesare primarily erosional, with 137Cs inventory below the referencevalue. In contrast, the GD site with elevated 137Cs concentration(2619 ± 192 Bq m�2) is predominantly depositional. Remarkabledifferences in soil physico-chemical characteristics betweenerosional and depositional sites were observed. The average soilbulk density in the GD site was (1.32 g cm�3) significantly lowerthan that in erosional sites (P < 0.05), and the value in the PE site(1.75 g cm�3) was substantially greater than that in other sites.Compared with erosional soils, the deposited sediments at the GDsite showed a remarkable decline in sand content. Moisture contentwas great at the GD site, and the value in the PE site was obviouslylower than that in other measured sites (Table 1). As for soil pH, thevalue in the PE site was significantly lower than that in other sites(P < 0.05).

No significant difference in the SOC contents of the upper 10 cmsoils was found among the EE, CE and LE sites. The SOC concen-tration in sites EE, CE and LE was considerably higher than(P < 0.05) that in other sites (Fig. 2). The distribution pattern of TNwas similar to that of SOC and a strong positive correlation(r ¼ 0.858, P < 0.05) between the TN and SOC was observed

Table 1Physicochemical characteristics of soil samples collected from erosional and depositionaletters are not significantly different at the P < 0.05 level.

Sites Status 137Csa (Bq m�2) C:N Sand (%) Silt (%)

PE Eroding 317 (87)c 10.2 (0.88)a 35 (2.97)b 27 (2.3EE Eroding 438 (65)c 11.2 (1.15)a 54 (1.79)a 18 (2.4ME Eroding 732 (198)b 10.3 (1.23)a 41 (1.56)b 31 (0.0CE Eroding 735 (131)b 10.2 (1.26)a 48 (3.20)a 26 (1.2LE Eroding 538 (158)c 10.6 (1.36)a 38 (2.75)b 32 (2.4GD Depression 2619 (192)a 8.4 (0.07)b 25 (3.52)c 32 (2.6

Note: (PE: Pinus massoniana Lamb. site; EE: Elaeocarpus decipiens Hemsl. site; ME: MicheLinn. site; GD: Fallow grass site).

a 137Cs reference value is 1920 ± 126 Bq m�2.

(Fig. 3a). The value of TN tended to be lower in both the GD and PEsites than that in the EE, ME, CE and LE sites, and the lowest value(0.94 mg g�1) was found in the PE site (Fig. 2). DOC, as a mea-surement of labile organic carbon, was greatest in the GD sitewith amaximum value of 0.33 mg g�1 dry soil. Statistical analysis showedthat there was no significant difference of DOC values among theEE, ME, LE, and GD sites, and their DOC contents were significantlylarger than those of the PE and CE sites (P < 0.05).

3.2. Erosion-induced variations in soil biological properties

Soil MBC exhibited large variations among the experimentalsites. The MBC concentrations ranged from 0.33 to 0.90 mg C g�1

dry soil, with the largest value in the GD site and the lowest in thePE site. No significant difference in MBC concentrations wasobserved among the EE, ME, CE and LE sites. Urease activity wasfound to be highest at the LE site, with the maximum value of88.08 mmol NH4þeN g�1 dry soil, followed by GD, and lowest in thePE site (Table 2). Compared to eroded sites, catalase activity in thetopsoil was greater at the GD site. The value in the PE site wasobviously lower than that in other studied sites, with the lowestvalue of 46.00 mmol KMnO4 g�1 dry soil (Table 2).

The DGGE profiles of 16S rDNA revealed complex banding pat-terns and displayed distinct shifts in the bacterial communitystructure of each study site (Fig. 4), inwhich each band representeda group of bacterial species. The analysis of two replicates for eachstudy soil showed good reproducibility of the DGGE banding pat-terns. High bacterial community diversity was observed in the GDandME sites, which was reflected by highH value. In contrast, theHindex in the PE site was found to be obviously lower than that inother sites (Table 2). The PCA analysis also showed that the bacterialcommunity structure at sites GD and ME was similar to each other(Fig. 5).

3.3. Relationships between microbial community compositions andsoil physicochemical characteristics

According to the RDA analysis, all of the physicochemical pa-rameters together explained 79.6% of the bacterial communityvariation. The first two canonical axes for bacterial DGGE finger-prints explained 40.3% and 18.0% of the variation in bacterial spe-cies data (Table 3), respectively. Monte Carlo tests for the first andall canonical axes were highly significant (P < 0.05). DOC and TNtogether was found to significantly explain the variation (P < 0.05)of the bacterial community. The RDA model (i.e., DOC and TN)statistically explained up to 34.8% of the variation. However, thepartial RDA verified that only DOC had a statistically significantindividual contribution to the variation (19.3% of the variation,P ¼ 0.014). In contrast, SOC and TN solely explained only 3.0% and2.5% (P > 0.05) of the variation in the bacterial DGGE profiles,

l sites. Brackets in figures are standard errors of the means. Values with the same

Clay (%) Moisture (%) pH Bulk density (g cm�3)

6)b 38 (1.39)a 17.1 (0.63)c 4.19 (0.46)d 1.75 (0.01)a6)c 28 (2.47)b 21.0 (0.68)b 5.02 (0.19)b 1.45 (0.01)c6)a 28 (1.05)b 19.4 (0.30)b 4.61 (0.16)c 1.45 (0.03)c0)b 26 (3.76)b 20.4 (0.30)b 5.41 (0.45)a 1.51 (0.02)bc6)a 30 (0.71)b 20.5 (0.70)b 4.76 (0.16)b 1.56 (0.01)b6)a 43 (2.25)a 34.2 (0.82)a 4.94 (0.26)bc 1.32 (0.05)d

lia maudiae Dunn site; CE: Cinnamomum bodinieri Levl. site; LE: Lagerstroemia indica

Fig. 2. The concentrations of soil organic carbon (SOC), total nitrogen (TN), dissolved organic carbon (DOC) and microbial biomass carbon (MBC) in top soils (0e10 cm) of erosionaland depositional sites (PE: Pinus massoniana Lamb. site; EE: Elaeocarpus decipiens Hemsl. site; ME: Michelia maudiae Dunn site; CE: Cinnamomum bodinieri Levl. site; LE: Lager-stroemia indica Linn. site; GD: Fallow grass site). The error bars represent the standard errors of the means. The plots labeled with different letters indicate that the differences ofaverage values among the different sites are significant at P < 0.05.

Fig. 3. Relationship (a) between the soil organic carbon (SOC) and total nitrogen (TN), (b) between the dissolved organic carbon (DOC) and catalase activity in the measured sites.

Table 2Microbiological characteristics of soil samples collected from erosional and depositional sites (PE: Pinus massoniana Lamb. site; EE: Elaeocarpus decipiens Hemsl. site; ME:Michelia maudiaeDunn site; CE: Cinnamomum bodinieri Levl. site; LE: Lagerstroemia indica Linn. site; GD: Fallowgrass site). Figures in brackets are standard errors of themeans.Values with various letters are significantly different at the P < 0.05 level.

Parameters PE EE ME CE LE GD

MBC (mg g�1) 0.33 (0.04)c 0.63 (0.10)b 0.54 (0.07)bc 0.57 (0.06)b 0.49 (0.08)bc 0.90 (0.01)aUrease (mmol NH4þeN g�1 dry soil) 55.20 (6.00)bc 74.40 (11.04)ab 76.32 (3.84)a 48.72 (1.44)c 88.08 (12.72)a 81.60 (16.56)aCatalase (mmol KMnO4 g�1 dry soil) 46.00 (4.00)b 59.60 (5.80)ab 49.60 (6.00)ab 49.00 (11.20)ab 60.20 (10.60)ab 69.4 (16.4)aBacterial diversity (H) 2.61 (0.10)b 2.84 (0.11)a 2.94 (0.04)a 2.86 (0.07)a 2.87 (0.00)a 2.94 (0.08)a

Z. Li et al. / European Journal of Soil Biology 71 (2015) 37e44 41

respectively (Table 4). In addition, an extremely significant positivecorrelation (r ¼ 0.958, P ¼ 0.001) between urease activity and DOCcontent was observed in measured sites (Fig. 3b).

4. Discussion

Soil microorganisms are actively involved in soil biochemicalprocesses, including organic matter decomposition, nutrientmineralization and cycling [2,32]. Given the important role of mi-crobes in soil ecosystems, dynamic changes in microbial biomassand community composition will consequentially affect the soil

nutrition dynamic. In this study, we researched the impact of watererosion on soil biological properties and investigated the relation-ships between microbial community compositions and physico-chemical parameters in erosion-affected soils. The result indi-cated that soil erosion led to microbial depletion, which was inagreement with other studies [9,31]. In the same study region andfor the same type of soil, Huang [31] also reported that severewatererosion can significantly reduce microbial abundance. Watererosion can promote breakdown of aggregates, accelerate trans-portation of sediment and reduce the soil water-holding capacity[12,33,34]. For example, low soil pH and water holding capacity

Fig. 4. The DGGE profiles of amplified 16S rDNA fragments from the erosional anddepositional soil samples. The initials (including PE, EE, ME, CE, LE and GD) denotedifferent study sites (PE: Pinus massoniana Lamb. site; EE: Elaeocarpus decipiens Hemsl.site; ME: Michelia maudiae Dunn site; CE: Cinnamomum bodinieri Levl. site; LE:Lagerstroemia indica Linn. site; GD: Fallow grass site). The numbers refer to differentsoil samples at each study site.

Fig. 5. Principal component analysis (PCA) for bacterial community structure. Inbacterial species and sample bi-plots diagrams based on PCA, bacterial species wereindicated by different lowercase letters and shown using blue solid lines with filledarrows. Samples were represented by open circles. The initials of soil samples indicateddifferent study sites (PE: Pinus massoniana Lamb. site; EE: Elaeocarpus decipiens Hemsl.site; ME: Michelia maudiae Dunn site; CE: Cinnamomum bodinieri Levl. site; LE:Lagerstroemia indica Linn. site; GD: Fallow grass site), followed by numbers referring todifferent soil samples from each study site. (For interpretation of the references tocolor in this figure legend, the reader is referred to the web version of this article.)

Z. Li et al. / European Journal of Soil Biology 71 (2015) 37e4442

were observed in erosional sites, particularly for the PE site(Table 1). The deteriorated environment in erosional sites mightalter the normal succession of soil microorganisms. Additionally,the topsoil was most precious and valuable, in which more mi-croorganisms survived than in the subsoil given superior condi-tions [35]. Serious water erosion caused topsoil microbial migrationthrough runoff action, which affected the spatial distribution ofmicroorganisms in sites and reduced the microbial biomass inerosional sites. Nevertheless, no significant difference in the mi-crobial community diversities was observed among the EE, CE, ME,LE and GD sites (Table 2). This phenomenon might be related to thenonselective migration of runoff in soil microbial species. Further-more, it also indicated that water erosion provided greater impacton level of microbial biomass than community composition. Finally,the availability of carbon fractions is regarded as one of the mostimportant environment factors in influencing soil microbialbiomass and activity [36e38]. For example, Churchland [39] re-ported that labile organic carbon was the main source of C thatinfluenced the microbial biomass and soil respiration rates. In ourresearch, long-term water erosion resulted in a significant declineof the available nutrient (e.g., DOC) in the PE and CE sites. Moreover,the DOC content in the EE, ME and LE sites was slightly but notsignificantly lower than that in the GD site. The inferior availablenutrients might be an important factor for the decreasing of mi-crobial biomass and enzyme activities in most erosional sites, andfurther limited the growth and development of soil microorgan-isms. Therefore, taking immediate and effective protective mea-sures before further erosion deterioration is strongly recommendedin erosional sites.

Compared with erosional sites, the depositional site showedgreater microbial biomass. These results support our hypothesisthat soil deposition is beneficial to enhance soil biological activities.Water erosion disturbs carbon-rich topsoil and preferentiallyremoves the finer particles and associated SOC from the erodingslope to the depositional site [12e14]. Therefore, the depositionalsite is generally considered as a sink of carbon [40,41]. Furthermore,numerous studies confirmed that, due to selective transportation,labile organic carbon fractions (e.g., DOC) are more possibly withthe runoff transported to the depositional site compared to SOC[16], and the carbon in depositional site is more available than thatin erosional site [33]. In our research, the maximum value of DOCwas observed in the GD site (Fig. 2). High availability of carbonfractions may be an important reason resulted in a great microbialbiomass in the depositional site. However, large input of relativelyfresh and labile C and its fast turnover, in turn, could stimulate themineralization of old organic matter as well, which might be adirect explanation for the low concentrations of C and N in thedepositional site [42]. Additionally, compared with erosional sites,higher clay content was also found in the depositional site. Clay actsas a bridge between particles which can effectively bind particlestogether [43]. Efficient aggregation in the depositional site may beanother explanation for the great biomass. Soil aggregates canprovide so effective protection for microorganisms that they cansurvive during a hardship period [44].

As evidenced in this study, most of the soil properties of thestudy sites were significantly influenced by water erosion. Thevariations in soil microbial communities were strongly correlatedwith the dynamics of the soil properties. It was shown that the ninechosen physico-chemical parameters accounted for 79.6% of thevariation in the community composition by RDA. Some variationremained unexplained (20.4% for bacterial species data). Perhapspart of the unexplained variations could relate to other microbialspecies (e.g., fungi) and physico-chemical parameters (e.g., soilporosity) which were not measured here [45]. The relative impor-tance of each significant parameter was calculated through the

Table 3Redundancy analysis results of bacterial DGGE profiles.

Axis Eigen value Species-environment correlation Cumulative variation of species Cumulative variation of species-environment Sum of all canonical Eigen values

Axis1 0.403 0.965 40.3 50.6 0.796Axis2 0.180 0.875 58.2 73.2Axis3 0.117 0.888 70.0 87.9Axis4 0.045 0.884 74.5 93.5

Table 4Eigen values, P values and F values obtained from the partial RDAs testing the influence of the primary parameters on the bacterial community composition.

Parameters include in the model Eigen value Variation explains solely P F

DOC (dissolved organic carbon) 0.193 19.3% 0.016 4.12SOC (soil organic carbon) 0.030 3.0% 0.626 0.610TN (total nitrogen) 0.025 2.5% 0.676 0.528

Z. Li et al. / European Journal of Soil Biology 71 (2015) 37e44 43

variation partitioning analysis. The results showed that the mi-crobial community composition was substantially influenced byDOC, as DOC explained up to 19.3% (P < 0.05) of the variation in thebacterial DGGE profiles, while SOC and TN individually onlycontributed to 3% and 2.5% of the variance in the microbial com-munity, respectively (Table 4). Compared to DOC, SOC and TNshowed inferior contributions to the variation of soil microbialcommunity. This finding is consistent with that of Tian [18], theheterogeneity in soil microbial diversity was closely correlatedwiththe soil organic matter (SOM) source, particularly to labile SOM forits availability. Zhang [30] also found that water-soluble carbonshowed a predominant effect on the bacterial and fungal commu-nity composition. Relative to the quantity of soil carbon, the qualityof carbon (indicated by labile organic carbon fractions) may be amore important driving factor influencing microbial communityvariation. SOC and TN also apparently affected the bacterial com-munity, but this effect was caused by its interaction with the othervariables. By contrast, SOC and TN exerted no significant individualinfluence on microbial community structure variation. These re-sults further supported our hypothesis that erosion-induced soilphysico-chemical properties changes, particularly to labile organiccarbon, have a significant effect on the soil microbiologicalcharacteristics.

It was shown that the chosen physicochemical parametersaccounted for a significant amount of the variation in the com-munity composition by RDA. It is necessary for researchers todetermine and better interpret how the erosion-induced changesof soil biogeochemical properties affect microbial community infuture. Additionally, there is little known about the influences ofsoil labile organic carbon fractions on the microbial biomass andcommunity composition. Considering the importance of availablenutrients in soils, more research is required to obtain a better un-derstanding of erosion-induced changes in the quality of soil car-bon along with the abundance and activity of microbialcommunity.

5. Conclusions

Greater microbial biomass was observed in the depositional sitethan that in eroding sites, while no significant difference in mi-crobial community diversities was observed between mosterosional sites and depositional site. This results indicated that soildeposition is beneficial to enhance soil microbial biomass, whilehas no significant impact on improving microbial community di-versity. Water erosion provided greater impact on level of soil mi-crobial biomass than community composition. Changes in soilphysico-chemical parameters accounted for 79.6% of the variation

in the community composition. Among these parameters, DOCshowed a primary contribution to the variance in bacterial com-munity structure. This result confirmed that the DOC is a moreimportant parameter affecting soil biological characteristics,compared to other environmental factors. Relative to the quantityof the soil C, the quality of C is more important in influencing soilmicrobial community. Therefore, we suggest that more researchshould be conducted to clarify the influence of the changes in soillabile organic carbon components induced by water erosion on soilmicrobiological characteristics.

Acknowledgments

This study was financially supported by the National NaturalScience Foundation of China (41271294) and the ‘Hundred-talentProject’ of the Chinese Academy of Sciences.Wewould like to thankLinjing Deng and Shuang Nie of Hunan University for their assis-tance with DGGE analysis, and Yanbiao Hu, Hongbo Yao of HunanUniversity for the sampling and laboratory analysis.

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Microbial responses to erosion-induced soil physico-chemical property changes in the hilly red soil region of southern China1. Introduction2. Materials and methods2.1. Experimental sites2.2. Soil sampling2.3. Laboratory analyses2.3.1. Measurement of physicochemical parameters2.3.2. Soil biological characteristic analyses2.3.3. DNA extraction and PCR-DGGE

2.4. Statistical analysis

3. Results3.1. Erosion-induced changes in soil physicochemical properties3.2. Erosion-induced variations in soil biological properties3.3. Relationships between microbial community compositions and soil physicochemical characteristics

4. Discussion5. ConclusionsAcknowledgmentsReferences