Effects of mixed biocrusts on soil nutrients and bacterial community structure：A case study from Hilly Loess Plateau, China

doi:10.21203/rs.3.rs-3223074/v1

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Effects of mixed biocrusts on soil nutrients and bacterial community structure：A case study from Hilly Loess Plateau, China

https://doi.org/10.21203/rs.3.rs-3223074/v1

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published 11 Sep, 2024

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In this paper, 16S rRNA sequencing analysis was carried out on the mixed crust and the surface layer of bare soil and soil under the crust in this area, and combined with the soil physical and chemical factors, the influence of the mixed crust on the bacterial community structure in the loess hilly area was explained. The results show that mixed crusts can significantly increase the conventional nutrient content of the soil in terms of fast acting phosphorus, total nitrogen and organic matter. In addition, the mixed crust layer develops its own specific bacterial community structure, with Rubrobacteria and Cyanobacteriia specifically enriched in the mixed crust layer. Redundancy analysis (RDA) showed that these particularly enriched species could be involved in the process of photosynthesis and nitrogen fixation, thereby increasing the levels of organic matter and organic nitrogen in the soil. The results of the study provide an important theoretical basis for the microbiology of ecological restoration in the hilly and gully areas of the Loess Plateau.

Biological sciences/Microbiology

Earth and environmental sciences/Ecology

Earth and environmental sciences/Environmental sciences

Mixed biocrusts

Bacteria

Soil nutrients

Biological crusts

Biocrusts can cover up to 70% of the soil surface in drylands ¹.They significantly influence ecosystem processes such as preventing soil erosion, nurturing ecosystems by fixing C and N from the atmosphere, altering soil albedo,regulating water relations, and supporting seed germination and optimum nutrient levels in vascular plants ². The biological crust on the Loess Plateau has the same composition and cementation mode as the biological crust in desert areas around the world. Both are organic complexes composed of microbial groups, lichen and bryophyte spore types and soil particles ^{3, 4, 5}. The physico-chemical and biological characteristics are obviously different from those of the physical crust. Drylands, which include dry sub-humid, semiarid, arid and hyper-arid areas, cover roughly 41% of the Earth’s terrestrial surface ⁶. Besides hosting 38% of the global human population, drylands also host c.a. 20% of plant and 30% of bird biodiversity hotspots, thus making these terrestrial biomes especially vulnerable to global environmental changes ⁷. Indeed, faced with a global need to sequester more carbon (C), drylands may store up to 25% of the world’s soil organic C, further prioritising soil conservation in these areas.

In terms of ecological functions, biological crusts can increase soil organic carbon and organic nitrogen through photosynthesis and nitrogen fixation, and improve soil fertility. On the other hand, biological crusts can maintain surface stability in different regions ^{8, 9, 10}. However, biological crusts on the Loess Plateau differ significantly from those in the desert in terms of ecological functions. On the Loess Plateau, different types of biological crusts can effectively reduce rainfall kinetic energy and runoff scour, reduce soil loss, maintain soil moisture, and promote vegetation succession^{11, 12}.Soil bacteria are one of the most diverse, abundant and functional groups of soil microorganisms¹³. They are important drivers of biogeochemical cycles, participate in the transformation of soil nutrients ¹⁴, and are key organisms in the material and energy cycles of ecosystems ¹⁵. Microbial diversity plays an important role in enhancing the local environment and ecological functions of the biological crust in the ecosystem ¹⁶.A lot of research has been done on the characteristics of the microbial community in the biological soil crust. A study of soil crusts in the Taberas Basin, Spain, found that cyanobacteria had a high abundance in the crusts and a low abundance in the subcrusts ¹⁷.The colonisation and development of a biological soil crust in the dune zone is beneficial for soil microbial characteristics and soil quality in the vegetation restoration area ¹⁸.At present, most research on biological crust focuses on changes in the bacterial community within the biological crust itself, or on comparisons between different types of crust, and there is a lack of detailed comparison and analysis of the composition and diversity of microbial communities between biological crust and the bare surface of the same thickness, as well as between the soil beneath.In this study, the soil of algal crust and subcutaneous layer, as well as the corresponding surface soil of bare land, were collected in the Loess Plateau area, and the effects of biological crust on the soil bacterial community and its living environment were comprehensively analysed. The results provide a theoretical basis for the study of microbial diversity, ecological function, artificial culture and ecological restoration of biological crust in the Loess Plateau.

2.1. Field experiment design

The study area is located in the Yangwangou land consolidation project area (36°10 '36"~37°02' 05" N, 109°14 '10"~110°05' 43" E) of Nanniwan Town, Yan'an City, Shaanxi Province. This area belongs to the hilly and gully region of the Loess Plateau, which is mainly dominated by loess bar hills due to the erosion of the tree-like river system. The climate type is a plateau continental warm temperate semi-arid climate, dry and windy spring, hot and rainy summer. The average annual temperature is 7.7 ~ 10.6℃. Annual sunshine is 2445h, annual rainfall is 450 ~ 650mm, frost-free period is 155 ~ 188 days. The soil type is mainly yellow soil and brown soil. As the gully and slope have been severely scoured and cut down for a long time, the slope gravity erosion is active, the collapse and landslide phenomenon are easy to occur, and the ecological environment is very fragile. Biological crusts are the most common surface micro-landscape in this region and can be found in large quantities under different types of land use.

Based on the field survey, field sampling and laboratory testing will be carried out in 2021. In this study area, the algae-moss mixed crust is the most important. Sampling sites were selected from three areas (S1-S3) at the front, middle and back of the gully (Fig. 1). From each area, three samples were taken, each 0.5m×0.5m in size, and mixed with a shovel three times along the diagonal as a sample (the sampling of bare soil samples followed the above scheme). Samples of the cortex (0 ~ 1.5cm) and soil below the cortex (1.5 ~ 11.5cm) were collected. The adjacent bare soil (undisturbed soil) was taken as a control (the distance was less than 10 m) and a total of 3 treatments (bare soil (BS), algae-moss mixed crust (MC) and soil below the crust (MCS)) were used. The collected soil samples were kept at low temperature during sampling, the subsequent samples for microbial diversity were kept at -80℃, and the samples for physicochemical properties were air dried for use through 20 and 100 mesh sieves.

2.2. Determination of basic physico-chemical properties and microbial diversity of soils

Soil pH was determined by pH meter, soil available phosphorus (AP) was determined by sodium bicarbonate leaching and molybdenum-antimony resistance spectrophotometry, soil organic matter (SOM) was determined by potassium dichromate volumetric method, soil available potassium (AK) was determined by sodium nitrate leaching and turbidimetric method, and soil total nitrogen (TN) was determined by persulfate digestion method. Soil microbial samples were collected and sent to Shanghai Meiji Biomedicine Technology Co., Ltd. for high-throughput sequencing of 16S rRNA gene amplicons. Primers 338F (5 '-ACTCCTACGGGAGG CAGCAG-3') and 806R (5 '-GGACTACHVGGGTWTCTAAT-3') ^[11] were used for PCR amplification of V3-V4 variable region.

2.3. Sequence analysis of 16S rRNA amplicons

Miseq PE300 platform off-board data using QIIME2 platform for data processing.The QIIME2 (Quantitative Insights Into Microbial Ecology 2) Linux analysis platform was used for the raw next-generation high throughput sequencing data derived from the Illumina Miseq platform ¹⁹.Raw data were imported using q2-demux, and sequence primers and linkers were removed using the cutadapt plugin. double-ended sequenced sequences were merged using vsearch ^{20, 21}.Sequences with q-score > 25 quality were retained for the next step of analysis. Denoise the sequences using the deblur plugin ²².The sequencing error bases were corrected and the retained sequence length was ensured to have more than 99.50% of the sequences meeting the requirements. Microbial data mining was performed using the feature table generated after denoising, and OTUs were annotated at 97% similarity using the SILVA database ^{23, 24}.Microbial community structural diversity was calculated using the diversity plugin of QIIME2, alpha diversity was generated and non-parametric tests were performed using Kruskal-Wallis test, distance matrices for beta diversity were generated and plotted in R language (version 4.0.3) using the vegan package and ggplot2 package PCoA plots, and ANOSIM analysis was performed on each distance matrix using the vegan package. Species stacked histograms were generated using the taxa plugin for QIIME2 to count microbial species at different taxonomic levels and plotted using ggplot2 in the R language. Differential microbial analyses were performed using the online LEfSe (Linear discriminant analysis Effect Size) program (http://huttenhower.sph.harvard.edu/galaxy/) on biomarkers from different treatments ²⁵.

3.1. Analysing soil physical and chemical properties at different sampling sites in the hilly and gulleyed Loess Plateau.

According to the analysis of BS data in Table 1, the initial soil fertility in the hilly and gully region of the Loess Plateau was low. After the formation of the algae-moss mixed crust, the soil chemical indices of the MC samples were significantly higher than those of the other two soil samples, except for pH (Table 1). In addition, it is interesting to note that the contents of total nitrogen, available phosphorus, available potassium and organic matter in MC and MCS are higher than those in BS samples, indicating that the algae-moss mixed crust formed on both sides of the channel in the Loess Plateau can effectively activate soil nutrients and enrich and transfer the activated nutrients to the adjacent soil layers.

Table 1

Analysis of soil physical and chemical properties of different samples
sample type	SOM/(g·kg^-1)	TN/(g·kg^-1)	AP/(mg·kg^-1)	AK/(mg·kg-1)	PH
MC	5.79 ± 0.41 a	0.51 ± 0.05 a	12.65 ± 0.41 a	70.00 ± 0.81 a	8.07 ± 0.04 b
MCS	4.22 ± 0.47 b	0.40 ± 0.04 b	11.15 ± 0.85 ab	68.33 ± 7.85 a	8.26 ± 0.08 a
BS	3.25 ± 0.41 b	0.31 ± 0.01 b	9.51 ± 0.98 b	64.00 ± 7.48 a	8.05 ± 0.09 b
Note: 1) Means ± standard error, different letters in the same row mean the significant difference between treatments ( Duncan method, P < 0.05 ). 2) MC, Mixed crust; MCS, Mixed crust subsoil; BS,Bare soil on the surface; AP, available phosphorus, AK, available potassium, TN, total nitrogen, OM, organic matter. The same below.

3.2. Impact of crust on soil bacterial diversity

The richness analysis of soil microbial diversity, including the Shannon-Wiener index and the Chao richness estimator in Fig. 2, showed that the microbial diversity index of the soil in the Jiexiao area (MC) was significantly lower than that of the Jiexiao area (MCS) and the surface bare soil (BS). According to Fig. 2C, regarding the variation of microbial community structure in different soil types, the first principal component (PC1) explained 83.23% of the variation, and the second principal component (PC2) explained 6.07% of the variation, which can fully reflect the characteristics of microbial community structure in different soil types. PC1 can well distinguish the microbial community structure of soil in the subcutaneous layer (MC) from that in the subcutaneous layer (MCS). It was also shown that there were significant differences in the bacterial community composition between the nodules (MC) and the other two soil samples. Interestingly, the subcutaneous square soil (MCS) and the surface bare soil (BS) differed in the dimensions of PC1 and PC2, but could not be effectively distinguished.

3.3. Effect of crust on soil bacterial community composition

The Circos diagram of the bacterial community composition was drawn at the class level (Fig. 3) and the bacteria with a relative abundance of less than 0.01 were classified as others (the top 17 bacterial classes in relative abundance are shown in the figure).

The top 6 bacteria in relative abundance were Actinobacteria, Alphaproteobacteria, Rubrobacteria, Thermoleophilia, Chloroflexia and Cyanobacteria. Interestingly, compared to the other two soil sample groups, cyanobacteria in the substrate layer (MC) accounted for 77.37%, which was much higher than that in the surface bare soil (BS) (15.02%) and the substrate layer (MCS) (7.61%). Another ternary diagram at the class level (Fig. 4) shows that Rubrobacteria, Thermoleophilia and Cyanobacteria are enriched in the soil samples in the nodal cortex (MC).

2.4. Species differences between groups

The top 50 species with relative abundance at class level were selected to analyse the difference between groups. Figure 5A shows the analysis of species differences between the MC and MCS soil sample groups. In MC and MCS, Cyanobacteria, Chloroflexi, Rubrobacteria, Bacilli, Acidimicrobiia and Thermoleophilia were observed in the comparison and there were significant differences between the different treatments. Acidimicrobacteria and Pyrophilic Oleobacteria are two of the earlier evolved branches of the phylum Actinomycetes. Their abundance in soil (MCS) below the nodule cortex is much higher than that of the nodule cortex. More interestingly, the relative abundance of Cyanobacteria is much higher in MC than in MCS. Furthermore, analysis of the differences between MC and BS soil samples showed that Rubrobacteria and Cyanobacteria were specifically enriched in MC (Fig. 5B).

2.5. Relationship between environmental factors and soil bacterial community composition

Figure 6 shows the relationship between soil chemical properties and bacterial community composition using RDA (Redundancy Analysis). The interpretative values of RDA1 axis and RDA2 axis are 74.0% and 3.79% respectively. The effects of all environmental factors on the composition of the bacterial community were total organic matter (SOM), total nitrogen (TN), available phosphorus (AP), PH and available potassium. In Figure. 6 the sampling points are distributed in two regions. Region Ⅰ is the positive semi-axial part of RDA1 where the sample points of MCS and BS are distributed. Region Ⅱ is the negative axis of RDA1 where MC sample points are distributed. The bacterial community composition of BS and MCS in region Ⅰ was negatively correlated with pH and negatively correlated with other factors. The bacterial community composition of the MC sample group distributed in zone Ⅱ was positively correlated with other factors except pH. In addition, detailed analysis showed that Rubrobacter tended to be enriched in the biological cortex, and correlation analysis showed that Rubrobacter was significantly positively correlated with organic matter content.

4.1 Biocrust Bacterial Communities

Multipoint analysis of microbial community composition of field test soils over many years revealed a high similarity in the composition of microbial communities in the same area ²⁶, indicating that bacterial communities in soils are stable and can be studied in depth. In addition, amplicon sequencing analysis revealed that soil microbial communities in biocrusts had higher species diversity compared to in situ soils in the field, with higher abundance of Nitrosomonadaceae and Pseudomonadaceae at the OTU level. Analysis of nitrogen-fixing microorganisms revealed that nitrogen cycling was more active in biocrusts ²⁷.This finding further supports the idea that nitrogen turnover is higher in biocrusts than in bulk soils. Previous studies have shown that nitrogen fixation potential is higher in biocrusts compared to in situ soils ²⁸.In this study, Rubrobacter was found to be significantly enriched in the biocrust layer, and RDA (redundancy analysis) revealed a significant positive correlation between Rubrobacter and soil effective phosphorus, nitrogen and organic matter content (Fig. 6). The higher relative abundance of Rubrobacter may be due to the increased organic matter and fast-acting phosphorus in the biocrusts and possibly to the increased density of bacteria in the biocrusts, although bacterial biomass was not measured in our study, other studies have confirmed higher bacterial biomass in biocrusts compared to bulk soils ²⁹.

4.2 Effect of Crust Type on Biocrust and Underlying Soil Chemistry

The positive effects of biocrusts upon surface C and N accumulation have been demonstrated in different ecosystems ^{30, 31, 32, 33}. Here we found that the C and N content of the biological crusts was significantly higher than that of the top bare soil and the soil below the crust. The microbial diversity index of the soil in the crust layer is significantly lower than that of the soil below the crust and the top bare soil. Additionally, the positive impacts of biocrust on underlying soil nutrients have also been documented. In a sandy dune system, Xu et al. ³⁴ detected higher organic matter, total N and available N in soils underneath biocrusts, compared to non-crusted soil. Though leaching of available N from biocrusts has been clearly demonstrated ^{35, 36}, this has not been uniformly observed. As such, the fate of available biocrust N remains a controversial topic ^{34, 36, 37}. lichen-type crusts was not considered in the present results, although it also has the function of increasing soil nutrients, but in the loess plateau area lichen crust cover is less than 10% ³⁸. Therefore, the contribution of lichen-type crusts to soil nutrients in this zone is usually ignored. Using biocrust as a model ecosystem, this study confirmed the relationship between biocrust bacterial community structure and soil nutrients, i.e. the organic carbon and effective nitrogen contents of mixed biocrust soils were closely associated with significant enrichment of specific bacterial communities, and the results have important implications for predicting the accumulation of soil nutrients by mixed biocrust on a larger scale. larger scale.

Taken together, Algae-moss crust can significantly increase the content of available phosphorus, total nitrogen and organic matter in soils in the hilly and gully region of the Loess Plateau. This study revealed the effects of biological crust on soil physical and chemical properties and bacterial community structure in the loess hilly region. A significant increase in the relative abundance of many potentially beneficial microorganisms, such as Rubrobacteria and Cyanobacteria, was observed in the bionode cortex. Redundancy analysis indicated that these particularly enriched species may be involved in photosynthesis and nitrogen fixation processes to increase soil organic matter and organic nitrogen. Taken together, these results suggest that the microbial flora can be regulated to accelerate the development of the algae-moss hybrid junction cortex and thus promote ecological restoration in the hilly and gully region of the Loess Plateau.

Author Contributions: Conceptualization, L.Z.; methodology, L.Z.; software, L.Z.; validation, L.Z.; formal analysis, L.Z.; investigation, L.Z.; resources, L.Z.; data curation, L.Z.; writing—original draft preparation, L.Z.; writing—review and editing, L.Z.; visualization, L.Z.; supervision, L.Z.; project administration, L.Z.; funding acquisition, L.Z. All authors have read and agreed to the published version of the manuscript.

Acknowledgements: This research was funded by Shaanxi Province Natural Science Basic Research Program (2022JQ-457), Shaanxi Province Enterprises Talent Innovation Striving to Support the Plan (2021-1-2-2), Inner scientific research project of Shaanxi Land Engineering Construction Group (DJNY-YB-2023-48).

Data Availability Statement: The datasets generated and analysed during the current study are not publicly available due [The data are sourced from government classified projects] but are available from the corresponding author on reasonable request.

Competing Interests Statement: The authors declare no conflict of interest.

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No competing interests reported.

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You are reading this latest preprint version

Effects of mixed biocrusts on soil nutrients and bacterial community structure：A case study from Hilly Loess Plateau, China

Status:

Journal Publication

Version 1

Abstract

Figures

1. Introduction

2. Materials and Methods

2.1. Field experiment design

2.2. Determination of basic physico-chemical properties and microbial diversity of soils

2.3. Sequence analysis of 16S rRNA amplicons

3. Results

3.2. Impact of crust on soil bacterial diversity

3.3. Effect of crust on soil bacterial community composition

2.4. Species differences between groups

2.5. Relationship between environmental factors and soil bacterial community composition

4. Discussion

4.1 Biocrust Bacterial Communities

4.2 Effect of Crust Type on Biocrust and Underlying Soil Chemistry

5. Conclusions

Declarations

References

Additional Declarations

Status:

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