globalchange  > 气候变化事实与影响
DOI: doi:10.1038/nclimate2806
论文题名:
Relationship between soil fungal diversity and temperature in the maritime Antarctic
作者: Kevin K. Newsham
刊名: Nature Climate Change
ISSN: 1758-744X
EISSN: 1758-6864
出版年: 2015-09-28
卷: Volume:6, 页码:Pages:182;186 (2016)
语种: 英语
英文关键词: Microbial ecology ; Biogeochemistry ; Biodiversity
英文摘要:

Soil fungi have pivotal ecological roles as decomposers, pathogens and symbionts1, 2. Alterations to their diversity arising from climate change could have substantial effects on ecosystems, particularly those undergoing rapid warming that contain few species3, 4. Here, we report a study using pyrosequencing to assess fungal diversity in 29 soils sampled from a 1,650km climatic gradient through the maritime Antarctic, the most rapidly warming region in the Southern Hemisphere5, 6. Using a ‘space-for-time substitution approach, we show that soil fungal diversity is higher in warmer habitats, with increases of 4.7 (observed) and 11.3 (predicted) fungal taxa per degree Celsius rise in surface temperature along the transect. Among 22 predictor variables, air temperature was the strongest and most consistent predictor of diversity. We propose that the current rapid warming in the maritime Antarctic (0.34°C per decade6) will facilitate the colonization of soil by a wider diversity of fungi than at present, with data from regression models suggesting 20–27% increases in fungal species richness in the southernmost soils by 2100. Such increases in diversity, which provide a sentinel for changes at lower latitudes, are likely to have substantial effects on nutrient cycling and, ultimately, productivity in the species-poor soils of maritime Antarctica.

The maritime Antarctic is undergoing rapid climate change. Surface air temperatures in the region, which broadly encompasses the Antarctic Peninsula and islands of the Scotia Arc, have risen by up to 2.8°C over the past 50 years, at rates several times that of the global mean5, 6. Rising temperatures in the region have led to changes to the physical environment, including ice shelf collapses and glacial retreats5. However, in recent years, biological responses to warming have also become apparent across the region7. These include order of magnitude increases in the population sizes of the two native angiosperms, increased moss growth rates, and the establishment of non-native plant species8, 9, 10. The range expansions of native plant populations and the establishment of non-native species in the typically unvegetated soils of the region are thought to be associated with new areas of land becoming exposed following glacial retreat, enhanced plant growth and reproduction, and accelerated soil nutrient cycling7, 10, 11.

Although climate change effects on the maritime Antarctic flora have recently become apparent, far less is known of soil microbial responses to warming in the region. Artificial warming experiments in the natural environment have shown relatively minor changes to the composition of bacterial communities in response to increased soil temperatures (0.5–2°C annual means), which is not surprising, as the experiments have only lasted for one to three years12, 13. However, the responses of soil fungi to climate warming in the maritime Antarctic have yet to receive attention. Despite their pivotal importance in terrestrial ecosystems as decomposers, pathogens and symbionts1, 2, the majority of fungi are filamentous in form and—especially for the lichens—grow slowly in the natural environment14, hampering assessments of their responses to warming treatments. For instance, in the low Arctic, substantial changes to root symbiotic fungal communities in response to warming only become apparent after 17 years of treatment15. Here, to circumvent the problem of detecting the responses of these slow-growing microbes to warming manipulations, we studied fungi in soil sampled from along a natural climatic gradient through the maritime Antarctic. Using a similar approach to previous ‘space-for-time substitution studies16, 17, we employ the gradient as a proxy to predict changes to soil fungal communities arising from climate warming in the region. We show that surface air temperature is a significant factor shaping the diversity and composition of soil fungal communities. On the basis of our observations, we predict that future warming in the region will lead to 20–27% increases in the numbers of fungal species present in the southernmost soils of the region by the end of the century, and that this will have consequent effects on biological productivity.

We studied 29 soils sampled during the 2007–2008 austral spring and summer from along a 1,650km gradient between 72° S and 60° S (Fig. 1 and Supplementary Table 1). The soils were free of vegetation (Supplementary Fig. 1), and were hence representative of the barren soils that are frequent in maritime Antarctic terrestrial ecosystems. Data from the Regional Atmospheric Climate Model18 indicated a significant increase in mean annual surface air temperature (MASAT) between south-eastern Alexander Island (72° S; MASAT −11°C) and Signy Island in the South Orkney Islands (60° S; MASAT −4°C), with a 0.62°C increase in air temperature for each degree decrease in latitude (Fig. 1, upper inset; Supplementary Table 2). To determine whether other abiotic parameters varied along the transect, we analysed soils for a suite of 20 physicochemical parameters (including pH, electrical conductivity and the concentrations of 11 elements and five dissolved ions). Soil C:N ratio declined significantly at lower latitudes (R2 = 33%, P = 0.001; Fig. 1, lower inset; Supplementary Table 2) and was negatively associated with MASAT (R2 = 31%, P = 0.002). This is consistent with previous observations that soils in cold ecosystems have higher C:N ratios than those in warmer ecosystems19, most likely because of slow organic matter decay1. The strong influence of latitude on MASAT, and its weaker effect on soil C:N ratio, were also confirmed by structural equation modelling (Supplementary Fig. 2). None of the other parameters that we measured, including the altitude from which the samples were taken, varied significantly with latitude (Supplementary Table 2).

Figure 1: Locations of sampling sites along the climatic gradient.
Locations of sampling sites along the climatic gradient.

Site names, latitudes, longitudes and altitudes are shown in Supplementary Table 1. Upper inset shows mean annual surface air temperature at each sampling location for 2007, derived from the Regional Atmospheric Climate Model18, as a function of latitude. Lower inset shows soil C:N ratio as a function of latitude.

Soil sampling.

To eliminate any effects of the presence of plants on soil fungal diversity, we sampled only soils without plant cover from along the climatic gradient. The uppermost five centimetres of soil was collected in 50ml DNA/RNAase-treated plastic tubes (30mm diam.) from each of five locations at each site and was bulked. The soil was then immediately snap-frozen by immersion in a mixture of dry ice and ethanol (c. −80°C). Samples were maintained at −80°C from the time of sampling until they were processed.

Air temperature data.

The inaccessible nature of most of the sites studied precluded the measurement of soil temperature, and so mean annual surface air temperature (MASAT) data, derived from the Regional Atmospheric Climate Model over Antarctica18, gridded at a horizontal resolution of 55 × 55km, were used as predictors of soil fungal diversity. MASAT values for the year 2007 in the grids in which each of the sampling sites occurred were used in statistical analyses (see below).

DNA extraction, PCR amplification and 454 pyrosequencing.

Total DNA was extracted under sterile conditions from 10g of soil using a PowerMax Soil DNA isolation kit (MO BIO Laboratories) as per the manufacturers instructions. The internal transcribed spacer 2 (ITS2) region of the ribosomal RNA encoding genes was amplified by polymerase chain reaction (PCR) using the primers gITS7 (5′-GTGARTCATCGARTCTTTG-3′ (ref. 27)) and ITS4 (5′-TCCTCCGCTTATTGATATGC-3′ (ref. 28)), which target sites in the 5.8S gene and ribosomal large subunit, respectively. The gITS7 primer was 5′-labelled with the 454 FLX sequencing primer adaptor B sequence and the ITS4 primer was 5′-labelled with a sample-specific barcode sequence and the 454 FLX sequencing primer adaptor A sequence. PCRs were performed in duplicate 50μl reactions, each containing 5 ng template DNA, ×1 Phusion High Fidelity PCR Buffer (New England Biolabs), 0.2mM of each of the dNTPs (Invitrogen), 0.3μM of the ITS4 primer, 0.5μM of the gITS7 primer, and 1U of 1× Phusion High Fidelity DNA Polymerase (New England Biolabs). Thermocycling conditions were as follows: 98°C for 30s, 35 cycles of 98°C for 10s, 56°C for 30s, 72°C for 15s and a final extension at 72°C for 7min. Negative controls, consisting of sterile water in place of template DNA, did not yield amplicons. Amplicons were purified using a Wizard SV Gel and PCR Clean-Up System (Promega), quantified with a Qubit fluorometer with a Quant-iT dsDNA HF assay kit and then 72ng of each sample was pooled. The pooled sample was purified again using a QIAquick PCR Purification Kit (Qiagen), and then sent to Macrogen for 454 pyrosequencing29.

Processing of sequence data.

Sequences were quality filtered and dereplicated using the QIIME script split_libraries.py with the homopolymer filter deactivated30. Homopolymer errors were corrected using Acacia v. 1.48 (ref. 31) and fungal ITS2 sequences were then extracted using ITSx v. 1.0.9 (ref. 32) and checked for chimeras against ITS2 sequences in UNITE v. 6 (ref. 33) using UCHIME v. 3.0.617 (ref. 34). At least 1,435 non-chimeric quality-filtered ITS2 sequences were derived from each soil sample. The sequences were clustered at 97% similarity using UCLUST v. 1.2.22. UNITE v. 6 (ref. 35) taxonomy was assigned to representative OTU sequences using BLAST + v. 2.2.30. Tables containing the abundances of different OTUs and their taxonomic assignments in each sample were generated and the number of reads was rarefied to 1,400 per sample. The mean number of observed OTUs and the estimated total number of OTUs (Chao 1) were calculated using QIIME.

Soil physicochemistry.

Soil pH and electrical conductivity were measured in 1:2.5 and 1:5 soil:water (vol:vol) slurries, respectively. Total nitrogen and organic carbon concentrations were determined using an Exeter Analytical CE440 Elemental Analyzer (EAI) following desiccation at 105°C and treatment with HCl to remove inorganic carbon. Concentrations of Ca, Cu, Fe, K, Mg, Mn, Ni, P and Zn (mgkg−1 dry soil) were determined using inductively coupled plasma mass spectrometry (ICP-MS) following reverse aqua regia digests. Water extractable PO43−, SO42− and Cl concentrations (mgkg−1 dry soil) were determined using Dionex ion chromatography. Soil NH4+–N, NO3–N/NO2–N and dissolved organic carbon (DOC) concentrations (mgkg−1 dry soil) were determined in 1M KCl (1:4 dry soil equivalent to solution ratio) followed by automated flow injection analysis (Skalar Analytical B.V.). The moisture content of each soil sample was determined gravimetrically. All analyses were based on soil passed through a 4mm sieve.

Statistical analyses.

The influence of MASAT and soil physicochemical parameters on changes in the composition of soil fungal communities between sites (beta diversity) was assessed using Redundancy Analysis (RDA) with Monte Carlo permutation tests to assess the significance of the constraints. Parameters were chosen for inclusion in the final RDA model by forward selection based on Akaikes Information Criterion (AIC). When the inclusion of a new parameter led to other terms becoming insignificant (P > 0.05), it was dropped, leaving the final minimally adequate model. All models were built for Hellinger-transformed OTU abundances. All analyses were implemented in R. Associations between soil fungal diversity, latitude, MASAT and soil physicochemical parameters were examined using polynomial and multivariate regressions. For the univariate models we adopted a principle of parsimony, accepting the model with the least number of coefficients commensurate with the greatest amount of variation (R2 value) explained. As some of the covariates were themselves related and causally linked (for example, latitude and MASAT), we hypothesized that each could have both direct effects on the response variables and indirect effects through their direct effects on other predictors. For this reason we used structural equation modelling (SEM) to investigate the direct and indirect effects of latitude, MASAT and soil physicochemical parameters on soil fungal richness. On the basis of the output from our univariate models, we created a full SEM model to test the hypotheses that latitude directly affected MASAT, soil C:N ratio and fungal richness, that MASAT directly affected fungal richness, that soil K concentration directly affected fungal richness and that MASAT directly affected soil C:N ratio. The hypothetical full model was then challenged with the data and goodness of fit assessed using Chi-squared tests and root mean square error of approximation (RMSEA) values. Variables and associated relationships were then removed progressively if they were not significant. The Chi-squared goodness of fit tested the difference between the hypothetical model pathway and the observed data. RMSEA values of <0.05 for the model were considered a good fit to the data. SEM analyses were performed in Amos version 22 (SPSS Software).

Accession numbers.

The amplicon sequences associated with this study have been deposited in the NCBI SRA under accession PRJNA282894.

  1. Swift, M. J., Heal, O. W. & Anderson, J. M. Decomposition in Terrestrial Ecosystems (Blackwell Scientific Publications, 1979).
  2. Tedersoo, L. et al. Global diversity and geography of soil fungi. Science 346, 1078 (2014).
  3. Setälä, H. & McLean, M. A. Decomposition rate of organic substrates in relation to the species diversity of soil saprophytic fungi. Oecologia 139, 98107 (2004).
  4. Tiunov, A. & Scheu, S. Facilitative interactions rather than resource partitioning drive diversity-functioning relationships in laboratory fungal communities. Ecol. Lett. 8, 618625 (2005).
  5. Adams, B. et al. in Antarctic Climate Change and the Environment (eds Turner, J. et al.) 183
URL: http://www.nature.com/nclimate/journal/v6/n2/full/nclimate2806.html
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资源类型: 期刊论文
标识符: http://119.78.100.158/handle/2HF3EXSE/4572
Appears in Collections:气候变化事实与影响
科学计划与规划
气候变化与战略

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Kevin K. Newsham. Relationship between soil fungal diversity and temperature in the maritime Antarctic[J]. Nature Climate Change,2015-09-28,Volume:6:Pages:182;186 (2016).
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