Introduction

 

Potato has become the fourth major food crop after rice, maize and wheat in China. China is the largest potato producer, accounting for 1/4 of total planting area and 1/5 of total production in the world (Jin et al. 2018). However, due to limited cultivated lands, blind pursuit of economic interests and lack of scientific planting concept, a large amount of potato is generally planted by a continuous cropping pattern that results in continuous-cropping obstacle with poor growth as well as yield and quality reduction of potato (Qin et al. 2017a). Changes in soil physical properties, enrichment of soil-borne pathogens, and the autotoxicity of root exudates have been recognized as the key influencing factors to lead to the continuous-cropping obstacle (Bennett et al. 2012; Huang et al. 2013). At present, rhizosphere microenvironment of plant is commonly considered as the most important influencing factor (Dias et al. 2015). Several studies have compared the soil microenvironment between rotational cropping and continuous cropping patterns of some crops (Govaerts et al. 2007; Xuan et al. 2012). Therefore, understanding how rhizosphere microenvironment of potato is influenced by continuous cropping pattern can contribute to soil health and potato production.

The composition of soil microbial community and relative abundance of soil microorganism play essential roles in enhancing soil quality, improving soil ecosystem functions, and maintaining plant health and growth (Helgason et al. 2009; Kong et al. 2011). Soil microbial diversity, community composition and structure are influenced by multiple factors, including soil types, planting patterns and management practices (Garbeva et al. 2004; Berg and Smalla 2009; Jangid et al. 2011). Therefore, it is critically necessary to employ appropriate planting pattern to enhance soil ecosystem functions (Acosta-Martínez et al. 2010; Bender et al. 2016). Different planting patterns of crops change soil properties, leading to the changes of soil microbial communities (Helgason et al. 2009; Lienhard et al. 2013). Li et al. (2018) have showed that the bacterial community is altered in the sweet potato soils with continuous cropping pattern for 1, 2, 3, and 4 years by pyrosequencing approach. Liu et al. (2014) have found that soil bacterial communities exhibit differential responses to the potato with continuous cropping pattern using pyrosequencing approach. In addition, previous studies have mainly revealed that different crop planting patterns (mainly including continuous cropping and rotational cropping patterns) and different planting histories affect soil community composition, diversity and structure (Govaerts et al. 2007; Kong et al. 2011; Hurisso et al. 2013). However, the questions, such as how continuous cropping of potato affects soil microbial communities; which species in soil are changed; and what are the key factors of soil properties influencing corresponding alteration of microbial communities, remain largely unexplored.

In the present study, we aimed to (i) investigate the differences of soil microbial diversity, community composition and structure among continuous cropping, rotational cropping and new planting potato soils by utilizing high-throughput 16S rRNA gene Illumina sequencing; (ii) compare the differences of the soil physicochemical properties among continuous cropping, rotational cropping and new planting potato soils; (iii) and establish the correlation between soil properties and microbial community diversity and structure. Moreover, we attempt to more systematically reveal what changes would continuous cropping pattern bring to soil properties and microbial community. Our results provided data support and theoretical basis for promoting sustainable development of potato industry through appropriate planting pattern and improving soil microecological environment of continuous cropping potato soil.

 

Materials and Methods

 

Experimental Design and Soil Sampling

 

The experimental field was located in Experimental Base of Hunan Agricultural University, Hunan Province, China. Field experiments of continuous cropping and rotational cropping patterns began in 2012. The field was divided into nine plots, each of 18×13 m2 in size. Three plots were selected for continuous cropping and rotational cropping patterns each year, respectively. The other three plots of newly cultivated soil were designed for an new planting potato experiment in 2017. After 6 years of continuous cropping and rotational cropping patterns and 1 year of new planting potato experiment, nine plots were used up (three replicates). Soil samples were simultaneously collected from plots in the harvesting period of potato in May 2017. From each plot, 30 potato plants were randomly selected, one core for 0–20 cm layer soil was collected from each plant, and one soil sample consisted of 15 cores. All 18 soil samples (three plots × 2) were placed into sterile plastic bags. Each composite sample was passed through a 2 mm sieve and divided into two parts. One part was air-dried for soil property analysis, and the other part was stored at −80°C for DNA extraction.

 

Physicochemical Characteristics of Soils

 

The following physicochemical properties of collected soil samples were determined: pH, total organic carbon, nitrate nitrogen, ammonia nitrogen, total nitrogen, available phosphorus, available potassium, and total phosphorus. Analysis of soil properties was performed by the Department of Nanjing Institute of Geography, CAS, using the previously published methods (Tan et al. 2019).

 

DNA Extraction and Amplicon Sequencing

 

DNA extraction of soil samples and amplicon sequencing were performed following Tan et al. (2019). The V4 region of the 16S rRNA gene was amplified using the purified DNA as a template with following primers: 515F (5'-GTGCCAGCMGCCGCGGTAA-3)/806R (5'-GGACTACHVGGGTWTCTAAT-3'). PCR amplification was conducted on a SelectCycler II (Select BioProduct). The purified amplicons were quantified by using a Qubit fluorometer, and the library was constructed with VAHTSTM Nano DNA Library Prep Kit for Illumina® (Vazyme Biotech Co., Ltd., Nanjing, China). The samples were sequenced by Miseq-sequencing machine (Illumina).

 

Sequence Preprocessing

 

Sequence preprocessing was consistent with the methods of Gu et al. (2019). The barcodes were assigned to the raw reads. After removal of barcodes and primers. The pair-ended sequences were quality-filtered by using Flash program (Feng et al. 2017). UPARSE algorithm was applied to remove chimeras and generate OTU table (Magoc and Salzberg 2011). All the sequence preprocessings were performed in an in-house pipeline (http://mem.rcees.ac.cn:8080) with various bioinformatics tools (such as FLASH, Btrim and UPARSE program).

 

Ecological and Statistical Analysis

 

Shannon and Richness diversity indices were calculated according to the methods of Gu et al. (2019). Unweighted

 

 

Fig. 1: Diversity indices based on 16S rRNA gene of bacterial community in continuous cropping, rotational cropping and new planting potato soils. (a) Shannon index; (b) Richness index. Different letters represent the significant difference among soils at P = 0.05. CC: continuous cropping, RC: rotational cropping, NP: new planting, similarly hereinafter

 

 

Fig. 2: Principal component analysis (PCA) of bacterial community structures in continuous cropping, rotational cropping and new planting potato soils

 Table 1: Physicochemical properties of continuous cropping, rotational cropping and new planting potato soils. CC: continuous cropping, RC: rotational cropping, NP: new planting. TOC, total organic carbon; TN, total nitrogen; NO3-N, nitrate nitrogen; NH4-N, ammonia nitrogen; AP, available phosphorus; AK, available potassium; WC, water content; TP, total phosphorus.

 

Sample

TP (mg kg-1)

TN (mg kg-1)

NH4-N (mg g-1)

NO3-N (mg kg-1)

AP (mg kg-1)

TOC (%)

pH

AK (mg kg-1)

CC

759.56 ± 41.78b

873.96 ± 32.76b

15.30 ± 4.53a

121.51 ± 5.24a

91.75 ± 6.45b

0.91 ± 0.06c

4.86 ± 0.09c

80.66 ± 2.80b

RC

891.12 ± 89.45a

1107.68 ± 133.69a

19.46 ± 14.97a

124.62 ± 15.02a

127.4 ± 16.71a

1.41 ± 0.20a

6.22 ± 0.25a

106.57 ± 5.99a

NP

336 ± 26.48c

930.29 ± 57.24b

14.51 ± 3.18a

116.17 ± 6.78a

15.45 ± 8.46c

1.13 ± 0.14b

5.54 ± 0.08b

46.4c ± 3.28c

Different letters represent the significant difference among soils at P = 0.05

principal coordinate analysis (PCoA) was performed to evaluate the alteration of microbial community structure (Gu et al. 2019). The Pearson correlation approaches were used to construct the relationship between microbial diversity and soil properties (PCC: Pearson correlation coefficient). Mantel test and canonical correspondence analysis (CCA) were used to analyze the contributions of soil properties to bacterial community.

 

Results

 

Physicochemical Properties of Continuous Cropping, Rotational Cropping and New Planting Potato Soils

 

ANOVA showed that there were significant differences in soil properties (P = 0.05) among continuous cropping, rotational cropping and new planting soils, except for NO3-N and NH4-N contents (Table 1). TP, AP, TOC and AK contents as well as pH value in rotational cropping soil were significantly higher than those in continuous cropping and new planting soils. However, the TOC content and pH value in continuous cropping soil were lower than those in other samples. The lowest TP, AP, TOC and AK contents were observed in new planting soil. In addition, TP, TN, AP, TOC and AK contents as well as pH value were significantly lower in continuous cropping soils when only compared with rotational cropping soil.

 

Bacterial Diversity and Community Structure of Continuous Cropping, Rotational Cropping and New Planting Potato Soils

 

After data processing, 716,221 valid reads were obtained from the 18 soil samples. All the reads were classified into 31,167 OTUs. The Shannon (Fig. 1a) and Richness (Fig. 1b) indices were used to analyze the alpha-diversity of bacterial communities in continuous cropping, rotational cropping and new planting soils. We found that continuous cropping soil had the lowest microbial diversity, while rotational cropping and new planting soils had the similar levels of bacterial diversity. Moreover, we further analyzed beta-diversity of microbial communities in continuous cropping, rotational cropping and new planting soils. The PCoA showed a perfect separation among bacterial community structures of continuous cropping, rotational cropping and new planting potato soils (Fig. 2). In addition, the dissimilarity tests of bacterial communities were carried out using ANOSIM and MRPP based on Bray-Curtis distance, and the results showed that the significant differences also existed in soil bacterial communities among continuous cropping, rotational cropping and new planting soils (Table 2). In summary, we concluded that there were significant differences for alpha- and beta-diversity among continuous cropping, rotational cropping and new planting soil bacterial communities.

 

Microbial Community Compositions of Continuous Cropping, Rotational Cropping and New Planting Potato Soils

 

All bacterial operational taxonomic units (OTUs) of 18 soil samples were identified into 949 genera and 36 phyla at a similarity level of 97%. The cladogram indicated the phylogenetic distribution of bacterial lineages among continuous cropping, rotational cropping and new planting Table 2: Dissimilarity test of bacterial community structure in continuous cropping, rotational cropping and new planting potato soils based on Bray-Curtis distance. CC: continuous cropping, RC: rotational cropping, NP: new planting

 

Comparison

MRPP

ANOSIM

Delta

P

R

P

NP VS. CC

0.6017

0.002**

1

0.004**

NP VS. RC

0.6074

0.001***

1

0.002**

CC VS. RC

0.6094

0.004**

0.987

0.003**

**Difference is significant at P = 0.01 level. ***Difference is significant at P = 0.001 level.

 

 

Fig. 3: Comparison of microbial community compositions in continuous cropping, rotational cropping and new planting potato soils. (a) Cladogram indicating the phylogenetic distribution of the most differentially abundant taxa in continuous cropping, rotational cropping and new planting potato soils. Each circle’s diameter is relative to the abundance of taxa in different potato soil communities, different colors represent the differences of the most differentially abundant taxa in continuous cropping, rotational cropping and new planting potato soil communities (red indicates CC, green indicates RC, blue indicates NP), circles represent phylogenetic levels from domain to genus; (b) Comparison of the soil community composition at the phylum level (relative abundance higher than 1%) ; (c) Comparison of the soil community composition at the genus level (relative abundance higher than 1%)

soils under different agricultural management practices (Fig. 3a), suggesting that there were significant differences of the microbial community composition among continuous cropping, rotational cropping and new planting soils from phylum to genus levels (P < 0.05). The 12 dominant phyla (relative abundance >1%) across 18 samples were Proteobacteria, Acidobacteria, Bacteroidetes, Firmicutes, Actinobacteria, Planctomycetes, Verrucomicrobia, Chloroflexi, Gemmatimonadetes, candidate division WPS-1, Thaumarchaeota and unclassified bacteria. The relative abundances (Table 3) of phyla Firmicutes (4.043%), Chloroflexi (3.19%) and candidate division WPS-1 (2.92%) in rotational cropping soil were significantly higher than those of continuous cropping and new planting soils (P < 0.05), while the lowest abundances of Acidobacteria (10.447%), Planctomycetes (0.926%), Verrucomicrobia (1.948%) and candidate division WPS-1 (0.424%) were observed in continuous cropping soil (P < 0.05; Fig. 3b).

Table 3: Relative abundances of dominant phyla and genera in soil bacterial communities of continuous cropping, rotational cropping and new planting potato soils. CC: continuous cropping, RC: rotational cropping, NP: new planting

 

Dominant phyla (>1%)

Relative abundance in potato soil communities

CC

RC

NP

Proteobacteria

48.88a

37.199a

43.656a

Acidobacteria

10.447b

12.8ab

15.344a

Bacteroidetes

17.337a

15.403a

9.912b

Actinobacteria

7.435a

5.96a

6.242a

Unclassified

2.474b

5.319a

3.921ab

Firmicutes

1.583b

4.043a

0.861b

Planctomycetes

0.926b

1.374a

1.227a

Verrucomicrobia

1.948b

5.016a

4.267a

Chloroflexi

1.39b

3.144a

0.835b

Gemmatimonadetes

1.889a

1.946a

1.382a

Candidate division WPS-1

0.424b

1.544a

0.957b

Thaumarchaeota

3.928b

3.629b

9.324a

Dominant genera (>1%)

 

 

 

Sphingomonas

5.006b

3.929b

10.884a

Nitrososphaera

3.926b

3.612b

9.32a

Gp6

0.472c

1.431b

3.916a

Gp4

0.049b

0.147b

2.738a

Terrimonas

0.081b

0.715b

2.658a

Spartobacteria genera incertae sedis

0.389c

1.045b

2.145a

Arthrobacter

0.971b

1.002b

1.953a

Enterobacter

0.291b

1.068ab

1.593a

Subdivision3 genera incertae sedis

0.936c

2.139a

1.53b

Flavisolibacter

0.184b

0.686ab

1.414a

Gemmatimonas

1.889a

1.946a

1.382a

Gp3

1.119a

1.428a

1.313a

Luteimonas

0.199b

0.779b

1.294a

Rhodanobacter

9.604a

0.835b

1.226b

Gp1

1.728ab

2.486a

1.198b

WPS-1 genera incertae sedis

0.424b

1.544a

0.957ab

Gaiella

2.443a

1.781ab

0.883b

Flavobacterium

6.817a

3.000b

0.728c

Gp2

1.904b

3.32a

0.565c

Rhizomicrobium

1.747a

1.241a

0.507b

Burkholderia

1.986a

0.54b

0.464b

Pseudomonas

0.444b

2.634a

0.381b

Terriglobus

1.126a

0.094b

0.123b

Others

55.797

61.488

50.485

Different letters represent the significant difference among soils at P = 0.05

 

The 23 dominant genera (relative abundance >1%) across all samples were Spartobacteria genera incertae sedis, Arthrobacter, Enterobacter, Subdivision 3 genera incertae sedis, Flavisolibacter, Gemmatimonas, Gp3, Luteimonas, Rhodanobacter, Gp1, WPS-1 genera incertae sedis, Gaiella, Flavobacterium, Gp2, Rhizomicrobium, Burkholderia, Pseudomonas and Terriglobus (Fig. 3c). The relative abundances (Table 3) of genera Subdivision3 genera incertae sedis (2.139%), Gp1 (2.486%), WPS-1 genera incertae sedis (1.544%), Gp2 (3.32%) and Pseudomonas (6.817%) in rotational cropping soil were significantly higher than those of continuous cropping and new plantingsoils (P=0.05) and the highest relative abundances of genera Rhodanobacter (9.604%), Gaiella (2.443%), Flavobacterium (2.443%), Burkholderia (1.986%) and Terriglobus (1.126%) and the lowest relative abundances of genera Flavisolibacter (0.184%), Gp6 (0.472%), Spartobacteria genera incertae sedis (0.389%), Enterobacter (0.291%), Subdivision3 genera incertae sedis (0.936%) and WPS-1 genera incertae sedis (0.424%) were observed in continuous cropping soil. Overall, the microbial composition and relative abundance of bacterial phyla and genera were significantly different among continuous cropping, rotational cropping and new planting soils.

 

The Relationship Between Soil Properties and Bacterial Community

 

Table 4 shows the relationship analysis between soil properties and five alpha-diversity indices of bacterial communities by Pearson correlation approach. The results showed that TP content was significantly positively correlated with Shannon (PCC = 0.519, P = 0.027) and Pelou_evenness (PCC = 0.593, P = 0.010). AP content was significantly positively correlated with Simpson (PCC = 0.592, P = 0.010) and Chao1 (PCC = 0.471, P = 0.048). TOC content was significantly positively correlated with Shannon (PCC = 0.687, P = 0.002) and Richness (PCC = 0.701, P = 0.001) as well as Pelou_evenness (PCC = -0.630, P = 0.005). Moreover, pH was significantly positively correlated with Shannon (PCC = 0.628, P = 0.005) and Richness (PCC = 0.633, P = 0.005) as well as Pelou_evenness (PCC = 0.583, P = 0.011). Table 4: Relationship between soil properties and alpha-diversity of continuous cropping, rotational cropping and new planting potato soils

 

Soil properties

Shannon

Simpson

Richness

Pelou_evenness

Chao1

PCC

P

PCC

P

PCC

P

PCC

P

PCC

P

TP

0.519

0.027*

0.681

0.002**

0.269

0.280

0.593

0.010**

0.002

0.994

TN

-0.010

0.970

-0.302

0.223

0.156

0.536

-0.074

0.771

0.295

0.234

NH4-N

0.195

0.437

0.099

0.697

0.197

0.432

0.188

0.455

0.163

0.519

NO3-N

0.225

0.368

0.383

0.117

0.001

0.998

0.309

0.213

-0.126

0.619

AP

0.135

0.593

0.592

0.010**

0.186

0.459

0.263

0.292

0.471

0.048*

TOC

0.687

0.002**

0.220

0.380

0.701

0.001***

0.630

0.005**

0.436

0.071

pH

0.628

0.005**

0.343

0.163

0.633

0.005**

0.583

0.011*

0.462

0.054

AK

0.372

0.128

0.739

0.001***

0.059

0.816

0.479

0.044*

-0.260

0.297

PCC= Pearson correlation coefficient. *Difference is significant at P = 0.05 level. **Difference is significant at P = 0.01 level. ***Difference is significant at P = 0.001 level

AK was significantly positively correlated with Simpson (PCC = 0.739, P = 0.001) and Pelou_evenness (PCC = 0.479, P = 0.044). Therefore, the TP, AP, TOC and AK contents as well as pH value were were important physicochemical factors to affect alpha-diversity of bacterial communities in continuous cropping, rotational cropping and new planting soil. To investigate the contribution of above-mentioned soil factors to microbial community of continuous cropping, rotational cropping and new planting potato soils, a CCA was conducted to study the relationship between soil properties and microbial community structures (Fig. 4). The CCA plots also clearly showed that pH, TP, AP, AK and TOC contents were the five long vectors, and pH was the longest vector. To identify the most important factors influencing the soil bacterial community, the Mantel test based on both Bray-Curtis and Jaccard distances was adopted. The results further confirmed that pH, TP, AP, AK and TOC contents were Table 5: Correlation analysis between soil properties and bacterial community structures based on Mantel test

 

Soil properties

r.BC

p.BC

r.JC

p.JC

TP

0.1962

0.016*

0.1930

0.029*

TN

-0.0099

0.479

0.0566

0.192

NH4_N

0.0012

0.395

-0.0313

0.698

NO3_N

-0.0085

0.478

-0.0981

0.919

AP

0.6436

0.001***

0.7175

0.001***

TOC

0.2978

0.005**

0.2636

0.007**

pH

0.5054

0.001***

0.4534

0.001***

AK

0.635

0.001***

0.7138

0.001***

*Difference is significant at P = 0.05 level. **Difference is significant at P = 0.01 level. ***Difference is significant at P = 0.001 level

 

 

Fig. 4: CCA plots of bacterial community structures correlated with soil physicochemical properties

 

significantly positively correlated with microbial community (Table 5). Overall, it was concluded that pH, TP, AP, AK and TOC contents were the important soil factors to powerfully drive the bacterial community assembly in continuous cropping, rotational cropping and new planting potato soils.

 

Discussion

 

Continuous-cropping problem, also called the continuous-cropping obstacle, is common phenomenon in the cultivation of potato in China. It has been reported that long-term continuous cropping pattern brings negative effects to soil micro-ecosystem, leading to the deterioration of soil physicochemical properties, occurrence of various soil-borne diseases and decline of the crop yield (Huang et al. 2013; Zhang et al. 2018). Recently, the comparative studies on soil properties of crop under continuous cropping and rotational cropping pattern have been reported (Liu et al. 2017; Li et al. 2018). TOC content and pH value were significantly lower in continuous cropping soils than those in rotational cropping and new planting soils which were consistent with the previous studies that continuous cropping of sweet potato causes soil acidification and a significant decline in soil organic carbon (Li et al. 2018). In addition, when only compared with rotational cropping soil, TP, TN, AP, TOC and AK contents as well as pH value were significantly lower in continuous cropping soils, which was consistent with the previous studies that long-term continuous cropping pattern leads to the decreased soil available nutrients in potato (Liu et al. 2015; Zhou et al. 2018). Moreover, several studies have revealed that the accumulation of allelochemicals in plant exudates may contribute to continuous-cropping obstacle (Song et al. 2018), while it is a far more controversial idea (Wu et al. 2016). Thus, more studies tend to focus on the response of soil microbial communities and their correlations with the changes of soil properties to continuous-cropping obstacle (Xiong et al. 2015).

Soil microbial diversity and community structure are closely associated with soil quality, ecosystem functions, and sustainable development (Govaerts et al. 2007; Kong et al. 2011), thereby impairing the plant growth, development, health and productivity. Our results showed that continuous cropping soil had the lowest level of alpha-diversity compared with rotational cropping and new planting potato soils according to Shannon and Chao1 indices. This finding was consistent with some previous reports that long-term continuous cropping pattern decreases microbial diversity and alters community structure compared with the crop rotation system of tobacco (Chen et al. 2018), soybean (Liu et al. 2017), cotton (Zhang et al. 2013), rice (Xuan et al. 2012) and sweet potato (Li et al. 2018). The soil of higher microbial diversity was more likely to maintain the function of soil ecosystems, enhance the resistance of abiotic and biotic environmental stresses and give defense against soil-borne diseases (Garbeva et al. 2004; Li et al. 2010). However, rotational cropping and new planting soils had similar level of alpha-diversity, indicating that crop rotation was an effective planting pattern for maintaining the function of soil ecosystems. It has been reported that long-term continuous cropping pattern leads to soil-borne diseases in potato (Qin et al. 2017b), indicating that lower level of soil microbial diversity may be associated with the occurrence of soil-borne diseases (Shi et al. 2019). In addition, beta-diversity analysis based on PCoA and dissimilarity tests showed that the microbial community structure of continuous cropping, rotational cropping and new planting potato soils was significantly different. Microbial community structure is also regarded as an indicator of soil health (Valadares-Pereira et al. 2017). Overalls, continuous cropping pattern of potato decreased soil microbial diversity and altered community structure that affected directly or indirectly the soil quality and ecosystems, consequently resulting in negatively influenced potato production.

The cladogram analysis showed that the microbial community components of continuous cropping, rotational cropping and new planting soils had significant differences from phylum to genus levels (P < 0.05). This finding was consistent with that the microbial community composition is significantly different among continuous cropping, rotational cropping and new planting soils of other plants according to Sun et al. (2014) and Liu et al. (2017). In addition, the relative abundance of some bacterial phyla and genera was significantly altered among continuous cropping, rotational cropping and new planting potato soils. The relative abundances of phyla Firmicutes (4.043%), Chloroflexi (3.19%) and candidate division WPS-1 (2.92%) in rotational cropping soil were significantly higher than those of continuous cropping and new planting soils, while the lowest abundances of Acidobacteria (10.447%), Planctomycetes (0.926%), Verrucomicrobia (1.948%) and candidate division WPS-1 (0.424%) were observed in continuous cropping soil (P = 0.05). Previous reports have indicated that phylum Firmicutes may be involved in the defense against vanilla Fusarium wilt disease in soils of sugar beet (Li et al. 2018). The phyla Verrucomicrobia and Acidobacteriacan play important roles in soil biogeochemical cycling processes (Shen et al. 2017) and nutrient cycling (Yang et al. 2019a), respectively. The phylum Planctomycetes is involved in the absorption of plant nutrients, especially in the utilization of carbon and nitrogen sources (Bhattacharyya et al. 2017). The phylum candidate division WPS-1 shows a significantly positive relationship with soil nutrient cycling (Ji et al. 2018). Phylum Chloroflexi can also play an important role in the biogeochemical chlorine cycle (Krzmarzick et al. 2012), which may explain why the pH value was increased in rotational cropping soil. In addition, the highest relative abundances of genera Rhodanobacter (9.604%), Gaiella (2.443%), Flavobacterium (2.443%), Burkholderia (1.986%) and Terriglobus (1.126%) were observed in continuous cropping soil. Some of these genera are regarded as non-beneficial bacteria in soils according to previous studies. For example, Rhodanobacter and Flavobacterium have the denitrification ability that is defined as the reduction of nitrate or nitrite to gaseous nitrogen (Prakash et al. 2012; Hatayama et al. 2016), thus leading to the decreased content of nitrogen nutrition in soil (Green et al. 2012; Liu et al. 2019), which is unfavorable to agricultural production. Gaiella is negatively correlated with microbial activity and biomass in soils that plays the important role in nutrient cycling and ecosystem sustainability (Yao et al. 2003; Yang et al. 2019b). Some species of Burkholderia are recognized as pathogens of plants and animals (Bergmark and Poulsen 2012). Overall, rotational cropping pattern significantly increased the relative abundances of beneficial bacteria that could significantly promote the absorption of nutrients, improve the utilization efficiency of organic matter and enhance the resistance against diseases. However, continuous cropping pattern increased the relative abundances of non-beneficial bacteria that were unfavorable for soil quality development and agricultural production.

Furthermore, evaluation of the relationship between the soil physicochemical properties and bacterial community in continuous cropping, rotational cropping and new planting soils provides direct insights into the mechanisms of continuous-cropping obstacle (Li et al. 2018), which can contribute to improvement of soil productivity and health for continuous cropping potato soil. In this study, pH value as well as TP, AP, AK and TOC contents were the important soil factors to powerfully drive the bacterial community assembly in continuous cropping, rotational cropping and new planting potato soils, and the CCA plots also showed that pH was the longest vector. Previous studies have indicated that the microbial community and diversity of the bacterial communities in continuous cropping and rotational cropping soybean soils are affected by pH, TN, TP, AK, AN and AP contents (Liu et al. 2017), and soil pH has also been proved to be the most important influential factor (Fierer and Jackson 2006). In addition, the alterations of bacterial community in the sweet potato soils with continuous cropping pattern are mainly driven by soil pH and soil organic matter (Li et al. 2018). Our results showed that TOC content and pH value were significantly lower in continuous cropping soils than those in rotational cropping and new planting soils. Overall analyses of relationship between the soil physicochemical properties and bacterial community revealed that the pH value and TOC content are the most important physicochemical factors to alter the microbial community in continuous cropping potato soils.

 

Conclusion

 

This study investigated the divergence of bacterial communities among continuous cropping, rotational cropping and new planting potato soils. In general, the continuous cropping pattern of potato decreased the microbial diversity, increased the abundances of non-beneficial bacteria, and altered the community structure compared with rotational cropping and new planting potato soils. In addition, the pH value and TOC content were determined as the most important physicochemical factors to alter the microbial community in continuous cropping potato soils. This study provided valuable insights into the occurrence mechanisms of potato continuous-cropping obstacle, which might contribute to improving soil microbial diversity and enhancing soil productivity of continuous cropping potato soil.

 

Acknowledgement

 

Financial supports from the National Key Research and Development Program of China (2018YFD0200800 and 2018YFD1000400), the project of Hunan Provincial Key Laboratory of Crop Germplasm Innovation and Utilization, Hunan Agricultural University (2018KFXM02), and the National Natural Science Foundation of China (31772352).

 

Reference

 

Acosta-Martínez V, G Burow, TM Zobeck, VG Allen (2010). Soil microbial communities and function in alternative systems to continuous cotton. Soil Sci Soc Amer J 74:1181–1192

Bender SF, C Wagg, MGVD Heijden (2016). An underground revolution: biodiversity and soil ecological engineering for agricultural sustainability. Trends Ecol Evol 6:440–452

Bennett AJ, GD Bending, D Chandler, S Hilton, P Mills (2012). Meeting the demand for crop production: the challenge of yield decline in crops grown in short rotations. Biol Rev 87:52–71

Berg G, K Smalla (2009). Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13

Bergmark L, PHB Poulsen, W Abu Al-Soud, A Norman, LH Hansen, SJ Sorensen (2012). Assessment of the specificity of Burkholderia and Pseudomonas qPCR assays for detection of these genera in soil using 454 pyrosequencing. FEMS Microbiol Lett 333:7784

Bhattacharyya P, KS Roy, AK Nayak, M Shahid, B Lal, P Gautam, T Mohapatra (2017). Metagenomic assessment of methane production-oxidation and nitrogen metabolism of long-term manured systems in lowland rice paddy. Sci Total Environ 586:12451253

Chen S, GF Qi, T Luo, HC Zhang, QK Jiang, R Wang, XY Zhao (2018). Continuouscropping tobacco caused variance of chemical properties and structure of bacterial network in soils. Land Degrad Dev 29:4106–4120

Dias TD, A Dukes, PM Antunes (2015). Accounting for soil biotic effects on soil health and crop productivity in the design of crop rotations. J Sci Food Agric 95:447–454

Feng K, ZJ Zhang, WW Cai, WZ Liu, MY Xu, HQ Yin, AJ Wang, ZL He, Y Deng (2017). Biodiversity and species competition regulate the resilience of microbial biofilm community. Mol Ecol 26:61706182

Fierer N, RB Jackson (2006). The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626631

Garbeva P, JAV Veen, JDV Elsas (2004). Microbial diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppressiveness. Annu Rev Phytopathol 42:243–270

Govaerts B, M Mezzalama, Y Unno, KD Sayre, M Luna-Guido, K Vanherck, L Dendooven, J Deckers (2007). Influence of tillage, residue management, and crop rotation on soil microbial biomass and catabolic diversity. Appl Soil Ecol 37:18–30

Green SJ, O Prakash, P Jasrotia, WA Overholt, E Cardenas, D Hubbard, JM Tiedje, DB Watson, CW Schadt, SC Brooks, JE Kostka (2012). Denitrifying Bacteria from the Genus Rhodanobacter Dominate Bacterial Communities in the Highly Contaminated Subsurface of a Nuclear Legacy Waste Site. Appl Environ Microbiol 78:10391047

Gu S, Q Hu, Y Cheng, L Bai, Z Liu, W Xiao, Z Gong, Y Wu, K Feng, Y Deng, L Tan (2019). Application of organic fertilizer improves microbial community diversity and alters microbial network structure in tea (Camellia sinensis) plantation soils. Soil Till Res 195:104356

Hatayama K, A Ushida, K Teruaki (2016). Flavobacterium aquicola spp. Nov., isolated from river water. Intl J Syst Evol Microbiol 66:27892796

Helgason BL, FL Walley, JJ Germida (2009). Fungal and bacterial abundance in long term no-till and intensive-till soils of the Northern Great Plains. Soil Sci Soc Amer J 731:120–127

Huang LF, LX Song, XJ Xia, WH Mao, K Shi, YH Zhou, JQ Yu (2013). Plant-soil feedbacks and soil sickness: from mechanisms to application in agriculture. J Chem Ecol 39:232–242

Hurisso TT, JG Davis, JE Brummer, ME Stromberger, MM Mikha, ML Haddix, MR Booher, EA Paul (2013). Rapid changes in microbial biomass and aggregate size distribution in response to changes in organic matter management in grass pasture. Geoderma 193194:6875

Jangid K, MA Williams, AJ Franzluebbers, TM Schmidt, DC Coleman, WB Whitman (2011). Land-use history has a stronger impact on soil microbial community composition than aboveground vegetation and soil properties. Soil Biol Biochem 43:2184–2193

Ji LF, ZD Wu, ZM You, XY Yi, K Ni, SW Guo, JY Ruan (2018). Effects of organic substitution for synthetic N fertilizer on soil bacterial diversity and community composition: A 10-year field trial in a tea plantation. Agric Ecosyst Environ 268:124132

Jin JH, DA Ramírez, KY Xie, WJ Li, W Yactayo, LP Jin, R Quiroz (2018). Is partial root-zone drying more appropriate than drip irrigation to save water in China? A preliminary comparative analysis for potato Cultivation. Potato Res 61:391–406

Kong AYY, KM Scow, AL Córdova-Kreylos, WE Holmes, J Six (2011). Microbial community composition and carbon cycling within soil microenvironments of conventional low-input, and organic cropping systems. Soil Biol Biochem 43:20–30

Krzmarzick MJ, BB Crary, JJ Harding, OO Oyerinde, AC Leri, SC Myneni, PJ Novak (2012). Natural niche for organohalide-respiring Chloroflexi. Appl Environ Microbiol 78:393401

Li CG, XM Li, WD Kong, Y Wu (2010). Effect of monoculture soybean on soil microbial community in the Northeast China. Plant Soil 330:423–433

Li H, JP Wang, Q Liu, ZF Zhou, FL Chen, D Xiang (2018). Effects of consecutive monoculture of sweet potato on soil bacterial community as determined by pyrosequencing analysis. J Basic Microbiol 59:181191

Lienhard P, S Terrat, N Prévost-Bouré, V Nowak, T Régnier, S Sayphoummie, K Panyasiri, F Tivet, O Mathieu, J Levęque (2013). Pyrosequencing evidences the impact of cropping on soil bacterial and fungal diversity in Laos tropical grassland. Agron Sustain Dev 2:525–533

Liu JJ, ZH Yu, Q Yao, XJ Hu, W Zhang, G Mi, XL Chen, GH Wang (2017). Distinct soil bacterial communities in response to the cropping system in a Mollisol of northeast China. Appl Soil Ecol 119:407416

Liu X, L Liu, P Leng, Z Hu (2019). Feasible and effective reuse of municipal sludge for vegetation restoration: physiochemical characteristics and microbial diversity. Sci Rep 9; Article 879

Liu X, HZ Qiu, D Wang, JL Zhang, QR Shen (2015). Evaluation on fungal community structure of rhizosphere soils of potato under rotation and continuous cropping systems in Yellow River Irrigation Areas of Middle Gansu Province. Acta Ecol Sin 35:39383948

Liu X, J Zhang, T Gu, W Zhang, Q Shen, S Yin, H Qiu (2014). Microbial community diversities and taxa abundances in soils along a seven-year gradient of potato monoculture using high throughput pyrosequencing approach. PLoS One 9; Article 86610

Magoc T, SL Salzberg (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:29572963

Prakash O, SJ Green, P Jasrotia, WA Overholt, A Canion, DB Watson, SC Brooks, JE Kostka (2012). Rhodanobacter denitrificans spp. Nov., isolated from nitrate-rich zones of a contaminated aquifer. Intl J Syst Evol Microbiol 62:24572462

Qin S, S Yeboah, L Cao, J Zhang, S Shi, Y Liu (2017a). Breaking continuous potato cropping with legumes improves soil microbial communities, enzyme activities and tuber yield. PLoS One 12; Article e0175934

Qin S, Y Yeboah, X Xu, Y Liu, B Yu (2017b). Analysis on fungal diversity in rhizosphere soil of continuous cropping potato subjected to different furrow-ridge mulching managements. Front Microbiol 8; Article 845

Shen CC, Y Ge, HY Chu (2017). Verrucomicrobial elevational distribution was strongly influenced by soil pH and carbon/nitrogen ratio. J Soils Sedim 17:24492456

Shi W, M Li, G Wei, R Tian, C Li, B Wang, R Lin, C Shi, X Chi, B Zhou, Z Gao (2019). The occurrence of potato common scab correlates with the community composition and function of the geocaulosphere soil microbiome. Microbiome 7:118

Song X, Y Pan, L Li, X Wu, Y Wang (2018). Composition and diversity of rhizosphere fungal community in Coptis chinensis Franch. continuous cropping fields. PLoS One 13; Article e0193811

Sun J, Q Zhang, J Zhou, Q Wei (2014). Illumina amplicon sequencing of 16S rRNA tag reveals bacterial community development in the rhizosphere of apple nurseries at a replant disease site and a new planting site. PLoS One 9; Article e111744

Tan L, S Gu, S Li, Z Ren, Y Deng, Z Liu, Z Gong, W Xiao, Q Hu (2019). Responses of microbial communities and interaction networks to different management practices in tea plantation soils. Sustainability 11; Article 4428

Valadares-Pereira ADA, ECAM Oliveira, AA Navarrete, WPDO Junior, SM Tsai, JM Peluzio, PBD Morais (2017). Fungal Community Structure as an Indicator of Soil Agricultural Management Effects in the Cerrado. Rev Bras Cienc Solo 41:112

Wu L, J Chen, H Wu, J Wang, Y Wu, S Lin, M Khan, Z Zhang, W Lin (2016). Effects of consecutive monoculture of Pseudostellaria heterophylla on soil fungal community as determined by pyrosequencing. Sci Rep 6; Article 26601

Xiong W, Z Li, H Liu, C Xue, R Zhang, H Wu, R Li, Q Shen (2015). The effect of long-term continuous cropping of black pepper on soil bacterial communities as determined by 454 pyrosequencing. PLoS One 10; Article e0136946

Xuan DT, VT Guong, A Rosling, S Alström, B Chai, N Högberg (2012). Different crop rotation systems as drivers of change in soil bacterial community structure and yield of rice, Oryza sativa. Biol Fert Soils 48:217–225

Yang AN, YF Lu, JH Zhang, JS Wu, JL Xu, ZK Tong (2019a). Changes in Soil Nutrients and Acidobacteria Community Structure in Cunninghamia lanceolata Plantations. Sci Silv Sin-Chin 55:119127

Yang SX, FM Li, XZ Peng, JB Cao, ZX Gao (2019b). Effects of amendments with different C/N/P ratios on the microbial community structure in Pb-Zn mine tailings. J Agro-Environ Sci-Chin 38:12561264

Yao HY, JM Xu, CY Huang (2003). Substrate utilization pattern, biomass and activity of microbial communities in a sequence of heavy metal-polluted paddy soils. Geoderma 115:139148

Zhang W, X Long, X Huo, Y Chen, K Lou (2013). 16S rRNA-based PCR-DGGE analysis of actinomycete communities in fields with continuous cotton cropping in Xinjiang, China. Microb Ecol 66:385–393

Zhang Y, Y Liu, G Zhang, X Guo, T Li (2018). The effects of rice straw and biochar applications on the microbial community in a soil with a history of continuous tomato planting history. Agronomy 8; Article 8050065

Zhou SM, SL Zheng, WJ Long, PP Wang, Q Zhang, JC Yuan (2018). Study on different potato continuous cropping ways on rhizosphere soil nutrients and enzyme activities. Intl J Environ Agric Biotechnol 3:1779–1786