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Sciences in Cold and Arid Regions ›› 2019, Vol. 11 ›› Issue (2): 139-149.doi: 10.3724/SP.J.1226.2019.00139.

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Shifts in community structure and function of ammonia-oxidizing archaea in biological soil crusts along a revegetation chronosequence in the Tengger Desert

LiNa Zhao1,2,4,XinRong Li1,2,ShiWei Yuan3,4,YuBing Liu1,2()   

  1. 1. Shapotou Desert Research and Experiment Station, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou, Gansu 730000, China
    2. Key Laboratory of Stress Physiology and Ecology in Cold and Arid Regions of Gansu Province, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou, Gansu 730000, China
    3. Key Laboratory of Remote Sensing of Gansu Province, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou, Gansu 730000, China
    4. University of Chinese Academy of Sciences, Beijing 100049, China
  • Received:2018-12-24 Accepted:2019-02-28 Online:2019-04-01 Published:2019-04-29
  • Contact: YuBing Liu E-mail:liuyb@lzb.ac.cn
  • About author:Professor YuBing Liu, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences. No. 320, West Donggang Road, Lanzhou, Gansu 730000, China. Tel: +86-931-4967199; E-mail: liuyb@lzb.ac.cn

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Abstract:

Metagenomic studies have demonstrated the existence of ammonia-oxidizing archaea (AOA) and revealed they are responsible for ammoxidation in some extreme environments. However, the changes in compositional structure and ammonia-oxidation capacity of AOA communities in biological soil crusts (BSCs) of desert ecosystems remain poorly understood. Here, we utilized Illumina MiSeq sequencing and microbial functional gene array (GeoChip 5.0) to assess the above changes along a 51-year revegetation chronosequence in the Tengger Desert, China. The results showed a significant difference in AOA-community richness between 5-year-old BSCs and older ones. The most dominant phylum during BSC development was Crenarchaeota, and the corresponding species were ammonia-oxidizing_Crenarchaeote and environmental_samples_Crenarchaeota. Network analysis revealed that the positive correlations among dominant taxa increased, and their cooperation was reinforced in AOA communities during BSC succession. Redundancy analysis showed that the dominant factor influencing the change in AOA-community structure was soil texture. GeoChip 5.0 indicated that the amoA gene abundances of AOA and ammonia-oxidizing bacteria (AOB) were basically the same, demonstrating that AOA and AOB played an equally important role during BSCs development. Our study of the long-term succession of BSC demonstrated a persistent response of AOA communities to revegetation development in desert ecosystems.

Key words: ammonia-oxidizing archaea, biological soil crusts, GeoChip 5.0, network analysis

Figure 1

Rarefaction curves of the amoA clone libraries based on 97% identity in different ages of BSCs. 5YR, 15YR, 28YR, 34YR, and 51YR represents 5-, 15-, 28-, 34-, and 51-year-old BSCs, respectively"

Figure 2

PCoA of AOA communities in BSCs at five different ages at the OTU level defined, based on 97% identity. 5YR, 15YR, 28YR, 34YR, and 51YR represents 5-, 15-, 28-, 34-, and 51-year-old BSCs, respectively"

Figure 3

Sobs index of AOA communities in BSCs at five different ages at the OTU level defined, based on 97% identity. All bars represent mean ± standard deviation (n = 3); different lowercase letters represents a significant difference between samples (P <0.05). 5YR, 15YR, 28YR, 34YR, and 51YR represent 5-, 15-, 28-, 34-, and 51-year-old BSCs, respectively"

Figure 4

Composition of AOA communities in BSCs at five different ages at the (a) phylum and (b) species level. 5YR, 15YR, 28YR, 34YR, and 51YR represents 5-, 15-, 28-, 34-, and 51-year-old BSCs, respectively"

Figure 5

Network visualizations showing interactions between major categories of AOA communities in BSCs at five different ages. (a), (b), (c), (d), and (e) correspond to interactions within 5YR, 15YR, 28YR, 34YR, and 51YR, respectively; and (f) is a brief summary of node and link numbers, and ratios of positive and negative links for five groups of subnetworks. Node sizes indicate OTU abundance. Line thicknesses represent the correlation coefficient. Red links indicate positive correlations between nodes. Green links indicate negative correlations between nodes. C nodes, U nodes, T nodes, and P/N correspond to Crenarchaeota nodes, Unclassified_norank_Archaea nodes, Thaumarchaeota nodes, and the ratios of positive and negative links respectively. 5YR, 15YR, 28YR, 34YR, and 51YR represents 5-, 15-, 28-, 34-, and 51-year-old BSCs, respectively"

Figure 6

Archaea and bacterial amoA genes abundance among BSCs at different ages. The ratios of AOA to AOB amoA genes abundance (AOA:AOB) are shown in the boxes above the chart. All bars represent mean ± standard deviation (n = 3); different lowercase letters, uppercase letters, and Greek letters represent significant differences between AOA abundance, AOB abundance, and the ratio of AOA:AOB (P <0.05), respectively. 5YR, 15YR, 28YR, 34YR, and 51YR represents 5-, 15-, 28-, 34-, and 51-year-old BSCs, respectively"

Figure 7

RDA of soil biochemical characteristics in relation to AOA compositional structures. Each dot represents the AOA community in each sample. Red arrows indicate the direction and magnitude of the impact of environmental factors on the AOA community, and the length of the red arrow indicates the intensity of the correlation. 5YR, 15YR, 28YR, 34YR, and 51YR represents 5-, 15-, 28-, 34-, and 51-year-old BSCs, respectively"

Table S-1

Soil characteristics of topsoil (0?5 cm) under BSCs in revegetated areas. 5YR, 15YR, 28YR, 34YR, and 51YR represents 5-, 15-, 28-, 34-, and 51-year-old BSCs, respectively"

Soil characteristics 5YR 15YR 28YR 34YR 51YR
pH 8.22±0.07 8.24±0.08 8.20±0.03 8.25±0.02 8.09±0.05
Sand (%) 99.10±0.12 93.88±0.71 93.51±1.27 90.16±1.47 85.74±1.24
Silt (%) 0.76±0.14 5.86±0.75 6.09±1.31 9.32±1.53 13.64±1.22
Clay (%) 0.14±0.03 0.26±0.05 0.40±0.05 0.52±0.06 0.62±0.06
Organic Matter (g/kg) 0.54±0.03 2.10±0.18 1.67±0.63 2.79±0.52 2.93±0.26
Carbon: Nitrogen ratio 2.54±1.16 4.51±0.35 4.12±0.17 4.66±0.25 4.68±0.40
Total Carbon (g/kg) 0.45±0.07 3.53±0.61 3.08±2.03 6.53±1.15 7.23±0.15
Total Nitrogen (g/kg) 0.14±0.05 0.27±0.01 0.24±0.09 0.35±0.07 0.36±0.01
Total Phosphorus (g/kg) 0.28±0.03 0.49±0.03 0.48±0.13 0.62±0.09 0.63±0.03
Available Nitrogen (mg/kg) 10.16±1.80 17.55±2.17 21.35±3.31 26.99±5.77 29.96±14.83
Available Phosphorus (mg/kg) 1.30±0.48 7.22±0.30 4.70±3.21 7.41±2.47 6.68±1.40
Urease (μg N-NH 4 + /(g?h)) 0.79±0.00 3.85±0.25 3.96±0.04 6.80±0.04 10.46±0.16

Dehydrogenase

(μg triphenyl formazan/(g?h))

 0.64±0.02 0.71±0.02 0.74±0.02 0.76±0.02 0.90±0.01
Invertase (μg glucose/(g?h)) 11.61±3.26 54.27±1.56 44.33±12.75 39.62±8.40 38.33±3.39

Table S-2

Sequence information from all samples. 5YR, 15YR, 28YR, 34YR, and 51YR represents 5-, 15-, 28-, 34-, and 51-year-old BSCs, respectively"

Sample ID Sequences numbers Mean length OTU
5YR1 14,959 272.668828 26
5YR2 13,765 271.275699 23
5YR3 17,437 272.507140 26
Even 15,387 272.150556 25
15YR1 12,705 271.997403 40
15YR2 16,331 271.610618 45
15YR3 18,192 274.208828 39
Even 15,743 272.605616 41
28YR1 12,032 270.735206 38
28YR2 17,346 271.312810 29
28YR3 16,824 272.688421 32
Even 15,401 271.578812 33
34YR1 17,985 274.157687 43
34YR2 17,306 271.427135 37
34YR3 10,409 271.250841 37
Even 15,233 272.278554 39
51YR1 18,602 272.207773 36
51YR2 12,914 270.748335 40
51YR3 10,190 271.624436 38
Even 13,902 271.526848 38

Table S-3

he Pearson correlations between soil biochemical characteristics of the topsoil (0?5 cm) under BSCs"

Attributes IT DHA UE AP AN TP TN TC C:N OM Clay Silt Sand pH
pH 0.032 -0.629* -0.548* -0.175 -0.366 -0.31 -0.426 -0.382 0.024 -0.313 -0.459 -0.526* 0.525* 1
Sand -0.397 -0.925** -0.972** -0.634* -0.742** -0.838** -0.819** -0.917** -0.726** -0.885** -0.896** -1.000** 1
Silt 0.395 0.922** 0.970** 0.634* 0.735** 0.836** 0.818** 0.916** 0.725** 0.884** 0.888** 1
Clay 0.404 0.901** 0.932** 0.559* 0.818** 0.789** 0.765** 0.857** 0.665** 0.827** 1
OM 0.572* 0.759** 0.858** 0.884** 0.773** 0.965** 0.953** 0.971** 0.784** 1
C:N 0.675** 0.586* 0.675** 0.702** 0.659** 0.711** 0.573* 0.703** 1
TC 0.415 0.801** 0.901** 0.796** 0.730** 0.956** 0.946** 1
TN 0.488 0.719** 0.800** 0.863** 0.687** 0.955** 1
TP 0.495 0.717** 0.803** 0.899** 0.734** 1
AN 0.342 0.701** 0.732** 0.686** 1
AP 0.599* 0.483 0.586* 1
UE 0.364 0.962** 1
DHA 0.373 1
IT 1
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