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Journal of Resources and Ecology >

2019 , Vol. 10 >Issue 4: 373 - 378

DOI: https://doi.org/10.5814/j.issn.1674-764X.2019.04.004

Resources and Ecology in the Qinghai-Tibet Plateau

Response of Microbial Communities in Soil to Multi-level Warming in a Highland Barley System of the Lhasa River

  • FU Gang ,
  • SUN Wei ,
  • LI Shaowei ,
  • ZHONG Zhiming , *
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  • Lhasa Plateau Ecosystem Research Station, Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China
*Corresponding author: ZHONG Zhiming, E-mail:

First author: FU Gang, E-mail:

Received date: 2018-12-28

  Accepted date: 2019-03-05

  Online published: 2019-07-30

Supported by

National Natural Science Foundation of China (31370458, 31600432, 41807331)

Bingwei Outstanding Young Talents Program of Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences (2018RC202)

National Key Research Projects of China (2016YFC0502005, 2016YFC0502006, 2017YFA0604801)

Youth Innovation Research Team Project of Key Laboratory of Ecosystem Network Observation and Modeling (LENOM2016Q0002) and Tibet Science and Technology Major Projects of Pratacultural Industry (XZ201801NA02).

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Abstract

No studies have examined the effect of experimental warming on the microbial biomass and community composition of soil in agricultural ecosystem on the Qinghai-Tibet Plateau. Thus it is unclear whether the influences of experimental warming on microbial communities in soil are related to warming magnitude in croplands on this Plateau. This study performed warming experiment (control, low- and high-level) in a highland barley system of the Lhasa River in May 2014 to examine the correlation between the response of microbial communities in soil to warming and warming magnitude. Topsoil samples (0-10 and 10-20 cm) were collected on September 14, 2014. Experimental warming at both low and high levels significantly increased soil temperature by 1.02 ℃ and 1.59 ℃, respectively at the depth of 15 cm. Phospho lipid fatty acid (PLFA) method was used to determine the microbial community in soil. The low-level experimental warming did not significantly affect the soil’s total PLFA, fungi, bacteria, arbuscular mycorrhizal fungi (AMF), actinomycetes, gram-positive bacteria (G+), gram-negative bacteria (G-), protozoa, the ratio of fungi to bacteria (F/B ratio), and ratio of G+ to G- (G+/G- ratio) at the 0-10 and 10-20 cm depth. The low-level experimental warming also did not significantly alter the composition of microbial community in soil at the 0-10 and 10-20 cm depth. The high-level experimental warming significantly increased total PLFA by 74.4%, fungi by 78.0%, bacteria by 74.0%, AMF by 66.9%, actinomycetes by 81.4%, G+ by 67.0% and G- by 74.4% at the 0-10 cm depth rather than at 10-20 cm depth. The high-level experimental warming significantly altered microbial community composition in soil at the 0-10 cm depth rather than at 10-20 cm depth. Our findings suggest that the response of microbial communities in soil to warming varied with warming magnitudes in the highland barley system of the Lhasa River.

Key words： infrared heater; microbial biomass; phospho lipid fatty acid; warming level

Cite this article

FU Gang , SUN Wei , LI Shaowei , ZHONG Zhiming . Response of Microbial Communities in Soil to Multi-level Warming in a Highland Barley System of the Lhasa River[J]. Journal of Resources and Ecology, 2019 , 10(4) : 373 -378 . DOI: 10.5814/j.issn.1674-764X.2019.04.004

1 Introduction

The surface temperature of the Tibetan Plateau is predicted to increase by 1.5-2.4 ℃ by the year 2100 (Ji and Kang, 2013) making the Tibetan Plateau one of the world’s most sensitive regions to climatic warming (Fu et al., 2015). In order to examine the effects of such warming on alpine ecosystems, many warming experiments have been conducted on the Tibetan Plateau (Fu and Shen, 2016; Fu and Shen, 2018; Fu et al., 2012). These previous studies have mainly investigated the responses of gross primary production, and aboveground biomass/net primary production to experimental warming (Fu et al., 2015; Zhang et al., 2015). The composition of microbial communities in soil may be more sensitive to environmental change than other microbial characteristics of soil (Papatheodorou et al., 2004). However, few studies have focused on the effect of experimental warming on the composition of microbial communities in soil in alpine ecosystems on the Tibetan Plateau (Rui et al., 2015; Xiong et al., 2014; Yu et al., 2019a; Zhao et al., 2014). To our knowledge, no studies report the biomass and composition of microbial communities in soil to experimental warming in croplands on the Tibetan Plateau. Therefore, it remains unclear that how climatic warming will affect microbial communities in soil in alpine croplands on the Tibetan Plateau.
Warming magnitudes vary with elevations and regions on the Tibetan Plateau and the increased magnitudes of surface temperatures vary among different Representative Concentration Pathways (RCPs) conditions (IPCC, 2013). That is, multi-magnitude warming is a common phenomenon. A recent meta-analysis showed that effects of experimental warming on microbial biomass carbon and nitrogen in soil were not significantly correlated with warming magnitude on the Tibetan Plateau (Zhang et al., 2015). In contrast, several studies have found that the effects of experimental warming on the biomass and composition of microbial communities in soil may vary with warming magnitude in alpine grasslands on the Tibetan Plateau (Xiong et al., 2014; Zhang et al., 2014). Therefore, the relationships between the effects of experimental warming on soil microbes and warming magnitudes on the Tibetan Plateau remains unclear.
In this study, a three level warming experiment (control,low-level and high-level experimental warming) was per-formed in a highland barley system at the Lhasa Agri-cultural Ecosystem Research Station. The main objective ofthis study was to examine whether the effects of experimental warming on microbial communities in soil can vary with warming level.

2 Materials and methods

2.1 Study area and experimental design

The study area was located at 91°21ʹ E, 29°41ʹ N, and has an annual mean air temperature of 7.9 ℃ and precipitation of 425 mm. The experimental design and the sowing and harvest dates (May 26 and September 14, 2014) of highland barleys are reported in previous studies (Fu et al., 2018; Zhong et al., 2016). Soil temperature (Ts) and moisture (SM) at the depths of 5 cm and 20 cm in the center of each experimental plot were measured continuously during the whole study period. Four sensors (two sensors of Ts, two sensors of SM) were connected to a data logger (HOBO weather station, Onset Computer, Bourne, MA, USA) within each plot. The data loggers sampled Ts and SM data every minute and provided average values every five minutes. Compared to the control, the low-level warming significantly increased Ts by 1.52 ℃ and 1.02 ℃ at the depths of 5 cm and 15 cm, respectively, but significantly decreased SM by 0.03 m3 m-3 at the depth of 15 cm (Fig. 1; Zhong et al., 2016). The high-level warming significantly increased Ts by 1.98 ℃ and 1.59 ℃ at the depths of 5 cm and 15 cm, respectively, but significantly decreased SM by 0.03 m3 m-3 and 0.05 m3 m-3 at the depths of 5 cm and 15 cm, respectively (Fig. 1; Zhong et al., 2016).
Fig. 1 Warming effects on soil (a) temperature and (b) moisture
Note: C: control; LW: low-level warming; HW: high-level warming. Error bars represent standard errors (n = 3). Different letters mean a significant difference at P < 0.05. Soil temperature and moisture data were measured at the depth of 15 cm

2.2 Soil sampling and analyses

Topsoil samples (0-10 and 10-20 cm) were collected using a probe of 5 cm in diameter on September 14, 2014. Three subsamples were collected from random locations in the plot and composited into one soil sample for each plot. The soil samples were immediately refrigerated. All composited soil samples were sieved using a sieve of 1 mm in diameter and any roots visible were picked out from the sieved soil.
The method of Baath and Anderson (2003) was used to determine the phospho lipid fatty acid (PLFA). Briefly, 8 g of dry-weight-equivalent fresh soil sample was extracted using chloroform : methanol : phosphate buffer (1 : 2 : 0.5). The extracted lipids were analyzed on a Thermo ISQ gas- chromatography mass-spectroscopy (GCMS) system (TRACE GC Ultra ISQ). The fatty acids i13:0, a13:0, 14:0, i14:0, 15:0, i15:0, a15:0, i16:0, 10Me16:0, 16:1w7c, 16:1w9c, 17:0, 10Me17:0, i17:0, a17:0, cy17:0w7c, 17:1w8c, 10Me18:0, 18:1w5c, 18:1w7c and cy19:0w7c were used as biomarkers for bacteria. The fatty acids 16:1w5c, 18:1w9c and 18:2w6c were used as indicators for fungi. The fatty acid 20:0 was used as a biomarker for protozoa. The fatty acid 16:1w5c was used as a biomarker for arbuscular mycorrhizal fungi (AMF) (Olsson et al., 1995). The fatty acids 10Me16:0, 10Me17:0 and 10Me18:0 were used as indicators for actinomycetes. The fatty acids i13:0, a13:0, i14:0, i15:0, a15:0, i16:0, i17:0 and a17:0 were used as biomarkers for gram-positive bacteria (G+). The fatty acids 16:1w7c, 16:1w9c, cy17:0w7c, 17:1w8c, 18:1w5c, 18:1w7c and cy19:0w7c were used as biomarkers for gram-negative bacteria (G-). The universal fatty acids 16:0, 18:0, 22:0 and 24:0 were also used for data analysis. We calculated the ratio of soil fungi to bacteria (F/B ratio) and ratio of G+ to G- (G+/G- ratio), which can reflect the change in the composition of microbial communities in soil. The ratios of (cy17:0w7c+cy19:0w7c)/(16:1w7c+18:1w7c) and (i17:0+ i15:0)/(a17:0+a15:0) were used as biomarkers for stress (Kieft et al., 1994).

2.3 Statistical analysis

A two-way ANOVA was used to estimate the effect of warming and soil depth on total PLFA, fungi, bacteria, protozoa, AMF, actinomycetes, G+, G-, F/B ratio, G+/G- ratio, (cy17:0w7c+cy19:0w7c)/(16:1w7c+18:1w7c) and (i17:0+ i15:0)/(a17:0+a15:0). Duncan multiple comparisons were performed. A redundancy analysis (RDA) was carried out using CANOCO for Windows v4.5 (Microcomputer Power, Ithaca, USA).

3 Results and discussion

ANOVA showed that experimental warming significantly changed total PLFA, fungi, bacteria, AMF, actinomycetes, G- and protozoa (Table 1). Specifically, at the 0-10 cm depth, both the low and high-level warming significantly increased protozoa by 28.9% and 104.1%, respectively, compared to the control (Fig. 2). Compared to the control, the high-level warming significantly increased total PLFA by 74.4%, fungi by 78.0%, bacteria by 74.0%, AMF by 66.9%, actinomycetes by 81.4%, G+ by 67.0% and G- by 74.4% at the 0-10 cm depth (Fig. 2). These findings were consistent with those of a recent meta-analysis which demonstrated that warming significantly increased microbial biomass carbon and nitrogen in soils across forests and grasslands on the Tibetan Plateau (Zhang et al., 2015).
Table 1 Two-way ANOVA for effects of warming (W) and soil depth (SD) on soil microbial biomass
Model PLFA (nmol g-1) Fungi (nmol g-1) Bacteria(nmol g-1) AMF(nmol g-1) Actinomycetes(nmol g-1) G+(nmol g-1) G-(nmol g-1) Protozoa(nmol g-1) F/B G+/G- (i17:0+i15:0)/(a17:0+a15:0) (cy17:0 w7c+cy19:0 w7c)/(16:1w7c+18:1w7c)
Warming (W) 6.66* 7.71** 5.97* 5.68* 7.53** 3.47 7.09** 10.33** 0.89 0.29 0.76 0.84
Soil depth (SD) 0.52 0.10 0.49 0.72 0.54 0.77 0.12 0.19 0.04 0.75 0.06 0.48
W×SD 0.80 1.17 0.68 0.41 0.63 0.95 0.48 0.13 1.01 1.37 1.44 1.37

Note: PLFA: phospho lipid fatty acid; AMF: arbuscular mycorrhizal fungi; G+: gram-positive bacteria; G-: gram-negative bacteria; F/B: the ratio of fungi to bacteria; G+/G-: the ratio of G+ to G-; *and ** mean P < 0.05 and P < 0.01, respectively.

Fig. 2 Warming effects on (a) PLFA, (b) fungi, (c) bacteria, (d) G+, (e) G-, (f) actinomycetes, (g) AMF and (h) protozoa of soil.
Note: PLFA: phospho lipid fatty acid; G+: gram-positive bacteria; G-: gram-negative bacteria; AMF: arbuscular mycorrhizal fungi; C: control; LW: low-level warming; HW: high-level warming. Error bars represent standard errors (n = 3). Different letters mean a significant difference at P < 0.05.
Neither low-level nor high-level warming significantly affected the F/B ratio, G+/G- ratio, (cy17:0w7c+cy19:0w7c)/ (16:1w7c+18:1w7c) and (i17:0+i15:0)/(a17:0+a15:0). This finding was in line with those of several previous studies (Streit et al., 2014; Zhang et al., 2013).
Redundancy analysis demonstrated that the first and second axes accounted for 59.1% and 2.8%, respectively, of the total variance of the PLFA data at the 0-10 cm depth, and 13% and 3.9%, respectively, of the total variance of the PLFA profile at the 10-20 cm depth (Fig. 3). Soil temperature significantly accounted for 59% of the total variance of the PLFA data at the 0-10 cm depth (Fig. 3). The average RDA score along the first axis for the high-level warming but not for the low-level warming was significantly lower than that for the control at the 0-10 cm depth (Fig. 4). These findings imply that the microbial biomass and community composition of soil did not significantly change when the warming magnitude was lower than 1.60 ℃, while a 1.98 ℃ increase in Ts significantly affected microbial biomass and community composition. Similarly, microbial biomass and community composition of soil did not change due to a relatively low increase in Ts (0.45 ℃), but was significantly affected by a relatively high increase in Ts (1.10 ℃) in an alpine swamp meadow on the Tibetan Plateau (Zhang et al., 2014).
Fig. 3 Redundancy analysis (RDA) of PLFA at (a) 0-10 cm and (b) 10-20 cm
Note: PLFA: phospho lipid fatty acid; Ts: soil temperature; SM: soil moisture; ** mean P < 0.01. The circle, star and square symbols indicate the control, low- and high-level warming, respectively.
Fig. 4 Redundancy analysis (RDA) scores of PLFA at (a) 0-10 cm and (b) 10-20 cm
Note: C: control; LW: low-level warming; HW: high-level warming.
Although the high-level warming did not significantly change F/B ratio and G+/G- ratio, the high-level warming significantly alter the composition of microbial community in soil. It is not possible, just based on an examination of the F/B ratio of soil to draw any conclusions about changes of the composition of microbial community.
There were no significant differences in total PLFA, fungi, bacteria, AMF, actinomycetes and G- between the low- and high-level warming treatments. This finding can be attributed to the following mechanisms. First, greater increases in soil temperature generally can cause more soil drying (Fu et al., 2019; Shen et al., 2016; Xu et al., 2013; Yu et al., 2019b), which may, in turn, result in greater negative effects on the microbial biomass of soil (Blankinship et al., 2011; Fu et al., 2012). However, this indirect effect of experimental warming on the composition of microbial community in soil may be relatively low (Yu et al., 2019a). Second, warming generally may reduce the utilization efficiency of microbial carbon in soil, meaning that microbial communities in soil may be more efficient at lower temperatures (Feng and Simpson, 2009; Steinweg et al., 2008). Third, communities in soil may be more sensitive at lower temperatures (Hamdi et al., 2013). Fourthly, the difference of soil temperature between the low- and high-level warming treatments was lower than 0.60 ℃, and this was obviously lower than 1.98 ℃.

4 Conclusions

This study has, for the first time to our knowledge, used controlled warming conditions to quantify warming effects at multiple levels of total phospho lipid fatty acid (PLFA), fungi, bacteria, gram-positive bacteria (G+), gram-negative bacteria (G-), actinomycetes, arbuscular mycorrhizal fungi (AMF) and protozoa of soil in agricultural ecosystems on the Tibetan Plateau. There were significant primary effects of experimental warming on total PLFA, fungi, bacteria, AMF, actinomycetes, G- and protozoa in soil. High-level experimental warming did not significantly change F/B ratio and G+/G- ratio, but high-level warming significantly alter the composition of microbial community in soil at the 0-10 cm soil depth. The responses of microbial biomass and community composition of soil to experimental warming may vary with warming magnitudes.

References

Publishing order | Descend order by publishing year | Descend order by cited within
[1]
Baath E, Anderson T H.2003. Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques.Soil Biology & Biochemistry, 35(7): 955-963.

[2]
Blankinship J C, Niklaus P A, Hungate B A.2011. A meta-analysis of responses of soil biota to global change.Oecologia, 165(3): 553-565.

[3]
Feng X, Simpson M J.2009. Temperature and substrate controls on microbial phospholipid fatty acid composition during incubation of grassland soils contrasting in organic matter quality.Soil Biology & Biochemistry, 41(4): 804-812.

[4]
Fu G, Shen Z X, Zhang X Z, et al.2012. Response of soil microbial biomass to short-term experimental warming in alpine meadow on the Tibetan Plateau.Applied Soil Ecology, 61(SI): 158-160.

[5]
Fu G, Shen Z X, Zhang X Z.2018. Increased precipitation has stronger effects on plant production of an alpine meadow than does experimental warming in the Northern Tibetan Plateau.Agricultural and Forest Meteorology, 249: 11-21.

[6]
Fu G, Shen Z X.2016. Environmental humidity regulates effects of experimental warming on vegetation index and biomass production in an alpine meadow of the Northern Tibet. PLoS ONE, 11(10): 10.1371/journal.pone.0165643.

[7]
Fu G, Sun W, Li S W, et al.2018. Response of plant growth and biomass accumulation to short-term experimental warming in a highland barley system of the Tibet.Journal of Resources and Ecology, 9(2): 203-208.

[8]
Fu G, Zhang H R, Sun W.2019. Response of plant production to growing/non-growing season asymmetric warming in an alpine meadow of the Northern Tibetan Plateau.Science of the Total Environment, 650: 2666-2673.

[9]
Fu G., Shen Z X, Sun W, et al.2015. A meta-analysis of the effects of experimental warming on plant physiology and growth on the Tibetan Plateau.Journal of Plant Growth Regulation, 34(1): 57-65.

[10]
Hamdi S, Moyano F, Sall S, et al.2013. Synthesis analysis of the temperature sensitivity of soil respiration from laboratory studies in relation to incubation methods and soil conditions.Soil Biology & Biochemistry, 58: 115-126.

[11]
IPCC.2013.Summary for Policymakers. In: Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press, United Kingdom and New York, NY, USA.

[12]
Ji Z M, Kang S C.2013. Double-nested dynamical downscaling experiments over the Tibetan Plateau and their projection of climate change under two RCP Scenarios.Journal of the Atmospheric Sciences, 70(4): 1278-1290.

[13]
Kieft T L, Ringelberg D B, White D C.1994. Changes in ester-linked phospholipid fatty acid profiles of subsurface bacteria during starvation and desiccation in a porous medium.Applied and Environmental Microbiology, 60(9): 3292-3299.

[14]
Olsson P A, Baath E, Jacobsen I, et al.1995. The use of phospholipid and neutral lipid fatty acids to estimate biomass of arbuscular mycorrhizal fungi in soil.Mycological Research, 99(9): 623-629.

[15]
Papatheodorou E M, Argyropoulou M D, Stamou G P.2004. The effects of large- and small-scale differences in soil temperature and moisture on bacterial functional diversity and the community of bacterivorous nematodes.Applied Soil Ecology, 25: 37-49.

[16]
Rui J P, Li J B, Wang S P, et al.2015. Responses of bacterial communities to simulated climate changes in alpine meadow soil of the Qinghai-Tibet Plateau.Applied and Environmental Microbiology, 81(17): 6070-6077.

[17]
Shen Z X, Wang J W, Sun W, et al.2016. The soil drying along the increase of warming mask the relation between temperature and soil respiration in an alpine meadow of Northern Tibet.Polish Journal of Ecology, 64: 125-129.

[18]
Steinweg J M, Plante A F, Conant R T, et al.2008. Patterns of substrate utilization during long-term incubations at different temperatures.Soil Biology & Biochemistry, 40(11): 2722-2728.

[19]
Streit K, Hagedorn F, Hiltbrunner D, et al.2014. Soil warming alters microbial substrate use in alpine soils.Global Change Biology, 20(4): 1327-1338.

[20]
Xiong J, Sun H, Peng F, et al.2014. Characterizing changes in soil bacterial community structure in response to short-term warming.FEMS Microbiology Ecology, 89(2): 281-292.

[21]
Xu W F, Yuan W P, Dong W J, et al.2013. A meta-analysis of the response of soil moisture to experimental warming. Environmental Research Letters, 8(4): doi:10.1088/1748-9326/1088/1084/044027.

[22]
Yu C Q, Han F S, Fu G.2019a. Effects of 7 years experimental warming on soil bacterial and fungal community structure in the Northern Tibet alpine meadow at three elevations.Science of the Total Environment, 655: 814-822.

[23]
Yu C Q, Wang J W, Shen Z X, et al.2019b. Effects of experimental warming and increased precipitation on soil respiration in an alpine meadow in the Northern Tibetan Plateau.Science of the Total Environment, 647: 1490-1497.

[24]
Zhang B, Chen S, He X, et al.2014. Responses of soil microbial communities to experimental warming in alpine grasslands on the Qinghai-Tibet Plateau.PLoS ONE, 9(8): e103859. doi:103810.101371/journal.pone. 0103859

[25]
Zhang N, Liu W, Yang H, et al.2013. Soil microbial responses to warming and increased precipitation and their implications for ecosystem C cycling.Oecologia, 173(3): 1125-1142.

[26]
Zhang X Z, Shen Z X, Fu G.2015. A meta-analysis of the effects of experimental warming on soil carbon and nitrogen dynamics on the Tibetan Plateau.Applied Soil Ecology, 87: 32-38.

[27]
Zhao C Z, Zhu L Y, Liang J, et al.2014. Effects of experimental warming and nitrogen fertilization on soil microbial communities and processes of two subalpine coniferous species in Eastern Tibetan Plateau, China.Plant and Soil, 382(1-2): 189-201.

[28]
Zhong Z M, Shen Z X, Fu G.2016. Response of soil respiration to experimental warming in a highland barley of the Tibet. SpringerPlus, 5(137): doi: 10.1186/s40064-40016-41761-40060.

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